The effect of global change on soil phosphatase activity.
N and P fertilization
atmospheric CO2 increment experiment
drought
global change
invasive species
meta-analysis
phosphorus cycle
soil phosphatase activity
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
received:
09
07
2021
accepted:
20
07
2021
pubmed:
13
8
2021
medline:
3
11
2021
entrez:
12
8
2021
Statut:
ppublish
Résumé
Soil phosphatase enzymes are produced by plant roots and microorganisms and play a key role in the cycling of phosphorus (P), an often-limiting element in terrestrial ecosystems. The production of these enzymes in soil is the most important biological strategy for acquiring phosphate ions from organic molecules. Previous works showed how soil potential phosphatase activity is mainly driven by climatic conditions and soil nitrogen (N) and carbon. Nonetheless, future trends of the activity of these enzymes under global change remain little known. We investigated the influence of some of the main drivers of change on soil phosphatase activity using a meta-analysis of results from 97 published studies. Our database included a compilation of N and P fertilization experiments, manipulation experiments with increased atmospheric CO
Substances chimiques
Soil
0
Phosphorus
27YLU75U4W
Phosphoric Monoester Hydrolases
EC 3.1.3.2
Nitrogen
N762921K75
Types de publication
Journal Article
Meta-Analysis
Langues
eng
Sous-ensembles de citation
IM
Pagination
5989-6003Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Achat, D. L., Augusto, L., & Denis, A. G. (2016). Future challenges in coupled C-N-P cycle models for terrestrial ecosystems under global change: A review. Biogeochemistry, 131(1), 173-202. https://doi.org/10.1007/s10533-016-0274-9
Alguacil, M. D. M., Lozano, Z., Campoy, M. J., & Roldán, A. (2010). Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biology and Biochemistry, 42(7), 1114-1122. https://doi.org/10.1016/j.soilbio.2010.03.012
Ali, M. A., Louche, J., Duchemin, M., & Plassard, C. (2014). Positive growth response of Pinus pinaster seedlings in soils previously subjected to fertilization and irrigation. Forest Ecology and Management, 318, 62-70. https://doi.org/10.1016/j.foreco.2014.01.006
Allan, R. P., & Soden, B. J. (2008). Atmospheric warming and the amplification of precipitation extremes. Science, 321(5895), 1481-1484. https://doi.org/10.1126/science.1160787
Allen, M. F. (2007). Mycorrhizal fungi: Highways for water and nutrients in arid soils. Vadose Zone Journal, 6(2), 291-297. https://doi.org/10.2136/vzj2006.0068
Allison, S. D., Nielsen, C., & Hughes, R. F. (2006). Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana. Soil Biology and Biochemistry, 38(7), 1537-1544. https://doi.org/10.1016/j.soilbio.2005.11.008
Angert, A., Biraud, S., Bonfils, C., Henning, C. C., Buermann, W., Pinzon, J., Tucker, C. J., & Fung, I. (2005). Drier summers cancel out the CO2 uptake enhancement induced by warmer springs. Proceedings of the National Academy of Sciences of the United States of America, 102(31), 10823-10827. https://doi.org/10.1073/pnas.0501647102
Aragón, R., Sardans, J., & Peñuelas, J. (2014). Soil enzymes associated with carbon and nitrogen cycling in invaded and native secondary forests of northwestern Argentina. Plant and Soil, 384(1-2), 169-183. https://doi.org/10.1007/s11104-014-2192-8
Barichivich, J., Osborn, T., Harris, I., Van Der Schrier, G., & Jones, P. (2020). Monitoring global drought using the self-calibrating Palmer Drought Severity Index [in "State of the Climate in 2019"]. Bulletin of the American Meteorological Society, 101, S51-S52. https://doi.org/10.1175/BAMS-D-20-0104.1
Bhattacharyya, P., Roy, K. S., Dash, P. K., Neogi, S., Shahid, M. D., Nayak, A. K., Raja, R., Karthikeyan, S., Balachandar, D., & Rao, K. S. (2014). Effect of elevated carbon dioxide and temperature on phosphorus uptake in tropical flooded rice (Oryza sativa L.). European Journal of Agronomy, 53, 28-37. https://doi.org/10.1016/j.eja.2013.10.008
Caldwell, B. A. (2005). Enzyme activities as a component of soil biodiversity: A review. Pedobiologia, 49(6), 637-644. https://doi.org/10.1016/j.pedobi.2005.06.003
Caldwell, B. A. (2006). Effects of invasive scotch broom on soil properties in a Pacific coastal prairie soil. Applied Soil Ecology, 32, 149-152. https://doi.org/10.1016/j.apsoil.2004.11.008
Chapuis-Lardy, L., Vanderhoeven, S., Dassonville, N., Koutika, L. S., & Meerts, P. (2006). Effect of the exotic invasive plant Solidago gigantea on soil phosphorus status. Biology and Fertility of Soils, 42(6), 481-489. https://doi.org/10.1007/s00374-005-0039-4
Ciais, P. H., Reichstein, M., Viovy, N., Granier, A., Ogée, J., Allard, V., Aubinet, M., Buchmann, N., Bernhofer, C., Carrara, A., Chevallier, F., De Noblet, N., Friend, A. D., Friedlingstein, P., Grünwald, T., Heinesch, B., Keronen, P., Knohl, A., Krinner, G., … Valentini, R. (2005). Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature, 437(7058), 529-533. https://doi.org/10.1038/nature03972
Cregger, M. A., Sanders, N. J., Dunn, R. R., & Classen, A. T. (2014). Microbial communities respond to experimental warming, but site matters. PeerJ, 2014(1), 1-13. https://doi.org/10.7717/peerj.358
Cusack, D. F., Karpman, J., Ashdown, D., Cao, Q., Ciochina, M., Halterman, S., Lydon, S., & Neupane, A. (2016). Global change effects on humid tropical forests: Evidence for biogeochemical and biodiversity shifts at an ecosystem scale. Reviews of Geophysics, 54, 523-610. https://doi.org/10.1002/2015RG000510
DeForest, J. L., Smemo, K. A., Burke, D. J., Elliott, H. L., & Becker, J. C. (2012). Soil microbial responses to elevated phosphorus and pH in acidic temperate deciduous forests. Biogeochemistry, 109(1-3), 189-202. https://doi.org/10.1007/s10533-011-9619-6
Delarue, F., Buttler, A., Bragazza, L., Grasset, L., Jassey, V. E. J., Gogo, S., & Laggoun-Défarge, F. (2015). Experimental warming differentially affects microbial structure and activity in two contrasted moisture sites in a Sphagnum-dominated peatland. Science of the Total Environment, 511, 576-583. https://doi.org/10.1016/j.scitotenv.2014.12.095
Delarue, F., Laggoun-Défarge, F., Buttler, A., Gogo, S., Jassey, V. E. J., & Disnar, J. R. (2011). Effects of short-term ecosystem experimental warming on water-extractable organic matter in an ombrotrophic Sphagnum peatland (Le Forbonnet, France). Organic Geochemistry, 42(9), 1016-1024. https://doi.org/10.1016/j.orggeochem.2011.07.005
Deng, Q., Hui, D., Luo, Y., Elser, J., Wang, Y., Loladze, I., Zhang, Q., & Dennis, S. (2015). Down-regulation of tissue N:P ratios in terrestrial plants by elevated CO2. Ecology, 96(12), 3354-3362. https://doi.org/10.1890/15-0217.1
Dieleman, W. I., Vicca, S., Dijkstra, F. A., Hagedorn, F., Hovenden, M. J., Larsen, K. S., Morgan, J., Volder, A., Beier, C., Dukes, J., King, J., Leuzinger, S., Linder, S., Luo, Y., Oren, R., de Angelis, P., Tingey, D., Hoosbeek, M. R., & Janssens, I. A. (2012). Simple additive effects are rare: A quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Global Change Biology, 18(9), 2681-2693. https://doi.org/10.1111/j.1365-2486.2012.02745.x
Doughty, C. E., Metcalfe, D. B., Girardin, C. A. J., Amézquita, F. F., Cabrera, D. G., Huasco, W. H., Silva-Espejo, J. E., Araujo-Murakami, A., da Costa, M. C., Rocha, W., Feldpausch, T. R., Mendoza, A. L. M., da Costa, A. C. L., Meir, P., Phillips, O. L., & Malhi, Y. (2015). Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature, 519(7541), 78-82. https://doi.org/10.1038/nature14213
Ebersberger, D., Niklaus, P. A., & Kandeler, E. (2003). Long term CO2 enrichment stimulates N-mineralisation and enzyme activities in calcareous grassland. Soil Biology and Biochemistry, 35, 965-972. https://doi.org/10.1016/S0038-0717(03)00156-1
Engel, V. C., Griffin, K. L., Murthy, R., Patterson, L., Klimas, C., & Potosnak, M. (2004). Growth CO2 concentration modifies the transpiration response of Populus deltoides to drought and vapor pressure deficit. Tree Physiology, 24(10), 1137-1145. https://doi.org/10.1093/treephys/24.10.1137
Finzi, A. C., Sinsabaugh, R. L., Long, T. M., & Osgood, M. P. (2006). Microbial community responses to atmospheric carbon dioxide enrichment in a warm-temperate forest. Ecosystems, 9(2), 215-226. https://doi.org/10.1007/s10021-005-0078-6
Fleischer, K., Rammig, A., De Kauwe, M. G., Walker, A. P., Domingues, T. F., Fuchslueger, L., Garcia, S., Goll, D. S., Grandis, A., Jiang, M., Haverd, V., Hofhansl, F., Holm, J. A., Kruijt, B., Leung, F., Medlyn, B. E., Mercado, L. M., Norby, R. J., Pak, B., … Lapola, D. M. (2019). Amazon forest response to CO2 fertilization dependent on plant phosphorus acquisition. Nature Geoscience, 12(9), 736-741. https://doi.org/10.1038/s41561-019-0404-9
Franco-Andreu, L., Gómez, I., Parrado, J., García, C., Hernández, T., & Tejada, M. (2016). Behavior of two pesticides in a soil subjected to severe drought. Effects on soil biology. Applied Soil Ecology, 105(May), 17-24. https://doi.org/10.1016/j.apsoil.2016.04.001
Freeman, C., Liska, G., Ostle, N. J., Lock, M. A., Reynolds, B., & Hudson, J. (1996). Microbial activity and enzymic decomposition processes following peatland water table drawdown. Plant and Soil, 180(1), 121-127. https://doi.org/10.1007/BF00015418
Goll, D. S., Vuichard, N., Maignan, F., Jornet-Puig, A., Sardans, J., Violette, A., Peng, S., Sun, Y., Kvakic, M., Guimberteau, M., Guenet, B., Zaehle, S., Penuelas, J., Janssens, I., & Ciais, P. (2017). A representation of the phosphorus cycle for ORCHIDEE (revision 4520). Geoscientific Model Development, 10(10), 3745-3770. https://doi.org/10.5194/gmd-10-3745-2017
Groffman, P. M., & Fisk, M. C. (2011). Phosphate additions have no effect on microbial biomass and activity in a northern hardwood forest. Soil Biology and Biochemistry, 43(12), 2441-2449. https://doi.org/10.1016/j.soilbio.2011.08.011
Gutknecht, J. L. M., Henry, H. A. L., & Balser, T. C. (2010). Pedobiologia Inter-annual variation in soil extra-cellular enzyme activity in response to simulated global change and fire disturbance. Pedobiologia, 53(5), 283-293. https://doi.org/10.1016/j.pedobi.2010.02.001
Harris, I., Jones, P. D., Osborn, T. J., & Lister, D. H. (2014). Updated high-resolution grids of monthly climatic observations - The CRU TS3.10 Dataset. International Journal of Climatology, 34(3), 623-642. https://doi.org/10.1002/joc.3711
Harris, I., Osborn, T. J., Jones, P., & Lister, D. (2020). Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Scientific Data, 7(1), 1-18. https://doi.org/10.1038/s41597-020-0453-3
Henry, H. A. L., Juarez, J. D., Field, C. B., & Vitousek, P. M. (2005). Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Global Change Biology, 11(10), 1808-1815. https://doi.org/10.1111/j.1365-2486.2005.001007.x
Hinojosa, M. B., Parra, A., Ramírez, D. A., Carreira, J. A., García-Ruiz, R., & Moreno, J. M. (2012). Effects of drought on soil phosphorus availability and fluxes in a burned Mediterranean shrubland. Geoderma, 191, 61-69. https://doi.org/10.1016/j.geoderma.2012.01.015
Huang, J., Ji, M., Xie, Y., Wang, S., He, Y., & Ran, J. (2016). Global semi-arid climate change over last 60 years. Climate Dynamics, 46(3-4), 1131-1150. https://doi.org/10.1007/s00382-015-2636-8
Huang, W., Liu, J., Zhou, G., Zhang, D., & Deng, Q. (2011). Effects of precipitation on soil acid phosphatase activity in three successional forests in southern China. Biogeosciences, 8(7), 1901-1910. https://doi.org/10.5194/bg-8-1901-2011
Hubau, W., Lewis, S. L., Phillips, O. L., Affum-Baffoe, K., Beeckman, H., Cuní-Sanchez, A., Daniels, A. K., Ewango, C. E. N., Fauset, S., Mukinzi, J. M., Sheil, D., Sonké, B., Sullivan, M. J. P., Sunderland, T. C. H., Taedoumg, H., Thomas, S. C., White, L. J. T., Abernethy, K. A., Adu-Bredu, S., … Zemagho, L. (2020). Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature, 579(7797), 80-87. https://doi.org/10.1038/s41586-020-2035-0
Janssens, I. A., Dieleman, W., Luyssaert, S., Subke, J. A., Reichstein, M., Ceulemans, R., Ciais, P., Dolman, A. J., Grace, J., Matteucci, G., Papale, D., Piao, S. L., Shulze, E.-D., Tang, J., & Law, B. E. (2010). Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience, 3(5), 315-322. https://doi.org/10.1038/ngeo844
Jassey, V. E., Chiapusio, G., Binet, P., Buttler, A., Laggoun-Défarge, F., Delarue, F., Bernard, N., Mitchell, E. A. D., Toussaint, M.-L., & Francez, A.-J. & Gilbert, D. (2013). Above- and belowground linkages in Sphagnum peatland: Climate warming affects plant-microbial interactions. Global Change Biology, 19(3), 811-823. https://doi.org/10.1111/gcb.12075
Kandeler, E., Mosier, A. R., Morgan, J. A., Milchunas, D. G., King, J. Y., Rudolph, S., & Tscherko, D. (2006). Response of soil microbial biomass and enzyme activities to the transient elevation of carbon dioxide in a semi-arid grassland. Soil Biology and Biochemistry, 38(8), 2448-2460. https://doi.org/10.1016/j.soilbio.2006.02.021
Kim, S. Y., & Kang, H. (2008). Effects of elevated CO2 on below-ground processes in temperate marsh microcosms. Hydrobiologia, 605(1), 123-130. https://doi.org/10.1007/s10750-008-9325-0
Krämer, S., & Green, D. M. (2000). Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biology and Biochemistry, 32(2), 179-188. https://doi.org/10.1016/S0038-0717(99)00140-6
Lagomarsino, A., Moscatelli, M. C., Hoosbeek, M. R., De Angelis, P., & Grego, S. (2008). Assessment of soil nitrogen and phosphorous availability under elevated CO2 and N-fertilization in a short rotation poplar plantation. Plant and Soil, 308(1-2), 131-147. https://doi.org/10.1007/s11104-008-9614-4
Liang, Q., Chen, H., Gong, Y., Yang, H., Fan, M., & Kuzyakov, Y. (2014). Effects of 15 years of manure and mineral fertilizers on enzyme activities in particle-size fractions in a North China Plain soil. European Journal of Soil Biology, 60(3), 112-119. https://doi.org/10.1016/j.ejsobi.2013.11.009
Llorens, L., Peñuelas, J., & Estiarte, M. (2003). Ecophysiological responses of two Mediterranean shrubs, Erica multiflora and Globularia alypum, to experimentally drier and warmer conditions. Physiologia Plantarum, 119(2), 231-243. https://doi.org/10.1034/j.1399-3054.2003.00174.x
Llorens, L., Peñuelas, J., Estiarte, M., & Bruna, P. (2004). Contrasting growth changes in two dominant species of a mediterranean shrubland submitted to experimental drought and warming. Annals of Botany, 94(6), 843-853. https://doi.org/10.1093/aob/mch211
Luo, Y., Su, B., Currie, W. S., Dukes, J. S., Finzi, A., Hartwig, U., Hungate, B., McMurtrie, R. E., Oren, R. A., Parton, W. J., & Field, C. B. (2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience, 54(8), 731-739. https://doi.org/10.1641/0006-3568(2004)054[0731:PNLOER]2.0.CO;2
Margalef, O., Sardans, J., Fernández-Martínez, M., Molowny-Horas, R., Janssens, I. A., Ciais, P., Goll, D., Richter, A., Oberstainer, M., Asensio, D., & Peñuelas, J. (2017). Global patterns of phosphatase activity in natural soils. Scientific Reports, 7(1). https://doi.org/10.1038/s41598-017-01418-8
Marklein, A. R., & Houlton, B. Z. (2012). Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist, 193(3), 696-704. https://doi.org/10.1111/j.1469-8137.2011.03967.x
Meisner, A., Boer, W. D., Verhoeven, K. J. F., Boschker, H. T. S., & Van Der Putten, W. H. (2011). Comparison of nutrient acquisition in exotic plant species and congeneric natives. Journal of Ecology, 99, 1308-1315. https://doi.org/10.1111/j.1365-2745.2011.01858.x
Menge, D. N. L., & Field, C. B. (2007). Simulated global changes alter phosphorus demand in annual grassland. Global Change Biology, 13(12), 2582-2591. https://doi.org/10.1111/j.1365-2486.2007.01456.x
Morgan, J. A., LeCain, D. R., Read, J. J., Hunt, H. W., & Knight, W. G. (1998). Photosynthetic pathway and ontogeny affect water relations and the impact of CO2 on Bouteloua gracilis (C4) and Pascopyrum smithii (C3). Oecologia, 114(4), 483-493. https://doi.org/10.1007/s004420050472
Moscatelli, M. C., Lagomarsino, A., De Angelis, P., & Grego, S. (2005). Seasonality of soil biological properties in a poplar plantation growing under elevated atmospheric CO2. Applied Soil Ecology, 30(3), 162-173. https://doi.org/10.1016/j.apsoil.2005.02.008
Nannipieri, P., Giagnoni, L., Landi, L., & Renella, G. (2011). Role of phosphatase enzymes in soil. In E. K. Bünemann, A. Oberson, & E. Frossard (Eds.), Phosphorus in action (pp. 215-243). https://doi.org/10.1007/978-3-642-15271-9
Niklaus, P. A., Alphei, J., Kampichler, C., Kandeler, E., Körner, C., Tscherko, D., & Wohlfender, M. (2007). Interactive effects of plant species diversity and elevated CO2 on soil biota and nutrient cycling. Ecology, 88(12), 3153-3163. https://doi.org/10.1890/06-2100.1
Olander, L. P., & Vitousek, P. M. (2000). Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry, 49(2), 175-190. https://doi.org/10.1023/A:1006316117817
Ostertag, R. (2001). Fine-root dynamics in Hawaiian montane forests. Ecology, 82(2), 485-499.
Peñuelas, J., Ciais, P., Canadell, J. G., Janssens, I. A., Fernández-Martínez, M., Carnicer, J., Obersteiner, M., Piao, S., Vautard, R., & Sardans, J. (2017). Shifting from a fertilization-dominated to a warming-dominated period. Nature Ecology and Evolution, 1(10), 1438-1445. https://doi.org/10.1038/s41559-017-0274-8
Penuelas, J., Janssens, I. A., Ciais, P., Obersteiner, M., & Sardans, J. (2020). Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human health. Global Change Biology, 26(4), 1962-1985. https://doi.org/10.1111/gcb.14981
Peñuelas, J., Poulter, B., Sardans, J., Ciais, P., van der Velde, M., Bopp, L., Boucher, O., Godderis, Y., Hinsinger, P., Llusia, J., Nardin, E., Vicca, S., Obersteiner, M., & Janssens, I. A. (2013). Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4. https://doi.org/10.1038/ncomms3934
Pold, G., Grandy, A. S., Melillo, J. M., & DeAngelis, K. M. (2017). Changes in substrate availability drive carbon cycle response to chronic warming. Soil Biology and Biochemistry, 110, 68-78. https://doi.org/10.1016/j.soilbio.2017.03.002
R Core Team. (2020). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Rodgers, V. L., Stinson, K. A., & Finzi, A. C. (2008). Ready or not, garlic mustard is moving in: Alliaria petiolata as a member of Eastern North American forests. BioScience, 58(5), 426-436. https://doi.org/10.1641/B580510
Rothstein, D. E., Vitousek, P. M., & Simmons, B. L. (2004). An exotic tree alters decomposition and nutrient cycling in a Hawaiian montane forest. Ecosystems, 8, 805-814. https://doi.org/10.1007/s10021-004-0009-y
Ryan, M. H., Tibbett, M., Edmonds-Tibbett, T., Suriyagoda, L. D. B., Lambers, H., Cawthray, G. R., & Pang, J. (2012). Carbon trading for phosphorus gain: The balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant, Cell and Environment, 35(12), 2170-2180. https://doi.org/10.1111/j.1365-3040.2012.02547.x
Sardans, J., Bartrons, M., Margalef, O., Gargallo-Garriga, A., Janssens, I. A., Ciais, P., Obersteiner, M., Sigurdsson, B. D., Chen, H. Y. H., & Peñuelas, J. (2017). Plant invasion is associated with higher plant-soil nutrient concentrations in nutrient-poor environments. Global Change Biology, 23(3), 1282-1291. https://doi.org/10.1111/gcb.13384
Sardans, J., Grau, O., Chen, H. Y. H., Janssens, I. A., Ciais, P., Piao, S., & Peñuelas, J. (2017). Changes in nutrient concentrations of leaves and roots in response to global change factors. Global Change Biology, 23(9), 3849-3856. https://doi.org/10.1111/gcb.13721
Sardans, J., & Peñuelas, J. (2005). Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biology and Biochemistry, 37(3), 455-461. https://doi.org/10.1016/j.soilbio.2004.08.004
Sardans, J., & Peñuelas, J. (2010). Soil enzyme activity in a Mediterranean forest after six years of drought. Soil Science Society of America Journal, 74(3), 838-851. https://doi.org/10.2136/sssaj2009.0225
Sardans, J., & Peñuelas, J. (2012). The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiology, 160(4), 1741-1761. https://doi.org/10.1104/pp.112.208785
Sardans, J., Peñuelas, J., & Estiarte, M. (2006). Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland. Plant and Soil, 289(1-2), 227-238. https://doi.org/10.1007/s11104-006-9131-2
Sardans, J., Peñuelas, J., & Estiarte, M. (2007). Seasonal patterns of root-surface phosphatase activities in a Mediterranean shrubland. Responses to experimental warming and drought. Biology and Fertility of Soils, 43(6), 779-786. https://doi.org/10.1007/s00374-007-0166-1
Sardans, J., Peñuelas, J., & Ogaya, R. (2008). Experimental drought reduced acid and alkaline phosphatase activity and increased organic extractable P in soil in a Quercus ilex Mediterranean forest. European Journal of Soil Biology, 44(5-6), 509-520. https://doi.org/10.1016/j.ejsobi.2008.09.011
Schimel, D., Stephens, B. B., & Fisher, J. B. (2015). Effect of increasing CO2 on the terrestrial carbon cycle. Proceedings of the National Academy of Sciences of the United States of America, 112(2), 436-441. https://doi.org/10.1073/pnas.1407302112
Shangguan, W., Dai, Y., Duan, Q., Liu, B., & Yuan, H. (2014). A global soil data set for earth system modeling. Journal of Advances in Modeling Earth Systems, 6, 249-263. https://doi.org/10.1002/2013MS000293
Souza, R. C., Solly, E. F., Dawes, M. A., Graf, F., Hagedorn, F., Egli, S., Clement, C. R., Nagy, L., Rixen, C., & Peter, M. (2017). Responses of soil extracellular enzyme activities to experimental warming and CO2 enrichment at the alpine treeline. Plant and Soil, 416(1-2), 527-537. https://doi.org/10.1007/s11104-017-3235-8
Souza-Alonso, P., Novoa, A., & González, L. (2014). Soil biology and biochemistry soil biochemical alterations and microbial community responses under Acacia dealbata link invasion. Soil Biology and Biochemistry Journal, 79, 100-108. https://doi.org/10.1016/j.soilbio.2014.09.008
Spohn, M., & Kuzyakov, Y. (2013). Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation - Coupling soil zymography with 14C imaging. Soil Biology and Biochemistry, 67, 106-113. https://doi.org/10.1016/j.soilbio.2013.08.015
Steinauer, K., Tilman, D., Wragg, P. D., Cesarz, S., Cowles, J. M., Pritsch, K., Reich, P. B., Weisser, W. W., & Eisenhauer, N. (2015). Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology, 96(1), 99-112. https://doi.org/10.1890/14-0088.1
Sun, Y., Goll, D. S., Ciais, P., Peng, S., Margalef, O., Asensio, D., Sardans, J., & Peñuelas, J. (2020). Spatial pattern and environmental drivers of acid phosphatase activity in Europe. Frontiers in Big Data, 2, 51. https://doi.org/10.3389/fdata.2019.00051
Sun, Y., Peng, S., Goll, D. S., Ciais, P., Guenet, B., Guimberteau, M., Hinsinger, P., Janssens, I. A., Peñuelas, J., Piao, S., Poulter, B., Violette, A., Yang, X., Yin, Y. I., & Zeng, H. (2017). Diagnosing phosphorus limitations in natural terrestrial ecosystems in carbon cycle models. Earth's Future, 5(7), 730-749. https://doi.org/10.1002/2016EF000472
Suriyagoda, L., Lambers, H., Ryan, M. R., & Renton, M. (2010). Effects of leaf development and phosphorus supply on the photosynthetic characteristics of perennial legume species with pasture potential: Modelling photosynthesis with leaf development. Functional Plant Biology, 37(8), 713-725. https://doi.org/10.1071/FP09284
Suriyagoda, L. D. B., Ryan, M. H., Renton, M., & Lambers, H. (2014). Plant responses to limited moisture and phosphorus availability: A meta-analysis. Advances in Agronomy, 124, 143-200. https://doi.org/10.1016/B978-0-12-800138-7.00004-8
Treseder, K. K. (2008). Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecology Letters, 11(10), 1111-1120. https://doi.org/10.1111/j.1461-0248.2008.01230.x
Turner, B. L., Condron, L. M., Wells, A., & Andersen, K. M. (2012). Soil nutrient dynamics during podzol development under lowland temperate rain forest in New Zealand. Catena, 97, 50-62. https://doi.org/10.1016/j.catena.2012.05.007
Turner, B. L., & Wright, J. S. (2014). The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry, 117(1), 115-130. https://doi.org/10.1007/s10533-013-9848-y
van der Schrier, G., Barichivich, J., Briffa, K. R., & Jones, P. D. (2013). A scPDSI-based global data set of dry and wet spells for 1901-2009. Journal of Geophysical Research: Atmospheres, 118, 4025-4048. https://doi.org/10.1002/jgrd.50355
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3), 1-48. https://www.jstatsoft.org/v36/i03/
Vitousek, P. M., & Farrington, H. (1997). Nutrient limitation and soil development: Experimental test of a biogeochemical theory. Biogeochemistry, 37(1), 63-75. https://doi.org/10.1023/A:1005757218475
Vitousek, P. M., Porder, S., Houlton, B. Z., & Chadwick, O. A. (2010). Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications, 20(1), 5-15. https://doi.org/10.1007/s00216-012-6370-3
Vo, N. X. Q., & Kang, H. (2013). Regulation of soil enzyme activities in constructed wetlands under a short-term drying period. Chemistry and Ecology, 29(2), 146-165. https://doi.org/10.1080/02757540.2012.711323
Walker, T. W., & Syers, J. K. (1976). The fate of phosphorus during pedogenesis. Geoderma, 15(1), 1-19. https://doi.org/10.1016/0016-7061(76)90066-5
Wallenstein, M. D., Mcmahon, S. K., & Schimel, J. P. (2009). Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Change Biology, 15(7), 1631-1639. https://doi.org/10.1111/j.1365-2486.2008.01819.x
Wang, R., Filley, T. R., Xu, Z., Wang, X., Li, M.-H., Zhang, Y., Luo, W., & Jiang, Y. (2014). Coupled response of soil carbon and nitrogen pools and enzyme activities to nitrogen and water addition in a semi-arid grassland of Inner Mongolia. Plant and Soil, 381(1-2), 323-336. https://doi.org/10.1007/s11104-014-2129-2
Wang, R., Goll, D., Balkanski, Y., Hauglustaine, D., Boucher, O., Ciais, P., Janssens, I., Penuelas, J., Guenet, B., Sardans, J., Bopp, L., Vuichard, N., Zhou, F., Li, B., Piao, S., Peng, S., Huang, Y. E., & Tao, S. (2017). Global forest carbon uptake due to nitrogen and phosphorus deposition from 1850 to 2100. Global Change Biology, 23(11), 4854-4872. https://doi.org/10.1111/gcb.13766
Wang, S., Zhang, Y., Ju, W., Chen, J. M., Ciais, P., Cescatti, A., Sardans, J., Janssens, I. A., Wu, M., Berry, J. A., Campbell, E., Fernández-Martínez, M., Alkama, R., Sitch, S., Friedlingstein, P., Smith, W. K., Yuan, W., He, W., Lombardozzi, D., … Peñuelas, J. (2020). Recent global decline of CO2 fertilization effects on vegetation photosynthesis. Science, 370(6522), 1295-1300. https://doi.org/10.1126/science.abb7772
Wang, X., Dong, S., Gao, Q., Zhou, H., Liu, S., Su, X., & Li, Y. (2014). Effects of short-term and long-term warming on soil nutrients, microbial biomass and enzyme activities in an alpine meadow on the Qinghai-Tibet Plateau of China. Soil Biology and Biochemistry, 76(May), 140-142. https://doi.org/10.1016/j.soilbio.2014.05.014
Wang, Y., Ciais, P., Goll, D., Huang, Y., Luo, Y., Wang, Y.-P., Bloom, A. A., Broquet, G., Hartmann, J., Peng, S., Penuelas, J., Piao, S., Sardans, J., Stocker, B. D., Wang, R., Zaehle, S., & Zechmeister-Boltenstern, S. (2018). GOLUM-CNP v1.0: A data-driven modeling of carbon, nitrogen and phosphorus cycles in major terrestrial biomes. Geoscientific Model Development, 11(9), 3903-3928. https://doi.org/10.5194/gmd-11-3903-2018
Wang, Y. P., Houlton, B. Z., & Field, C. B. (2007). A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production. Global Biogeochemical Cycles, 21(1), 1-15. https://doi.org/10.1029/2006GB002797
Williams, C. J., Shingara, E. A., & Yavitt, J. B. (2000). Phenol oxidase activity in peatlands in New York state: Response to summer drought and peat type. Wetlands, 20(2), 416-421. https://doi.org/10.1672/0277-5212(2000)020%5B0416:POAIPI%5D2.0.CO;2
Xu, S., Sardans, J., Zhang, J., & Peñuelas, J. (2020). Variations in foliar carbon:nitrogen and nitrogen:phosphorus ratios under global change: A meta-analysis of experimental field studies. Scientific Reports, 10(1), 1-11. https://doi.org/10.1038/s41598-020-68487-0
Yang, K., & Zhu, J. (2015). The effects of N and P additions on soil microbial properties in paired stands of temperate secondary forests and adjacent larch plantations in Northeast China. Soil Biology and Biochemistry, 90, 80-86. https://doi.org/10.1016/j.soilbio.2015.08.002
Yang, K., Zhu, J., Gu, J., Yu, L., & Wang, Z. (2015). Changes in soil phosphorus fractions after 9 years of continuous nitrogen addition in a Larix gmelinii plantation. Annals of Forest Science, 72(4), 435-442. https://doi.org/10.1007/s13595-014-0444-7
Yang, X., Thornton, P. E., Ricciuto, D. M., & Hoffman, F. M. (2016). Phosphorus feedbacks constraining tropical ecosystem responses to changes in atmospheric CO2 and climate. Geophysical Research Letters, 43(13), 7205-7214, https://doi.org/10.1002/2016GL069241
Yavitt, J. B., Wright, S. J., & Wieder, R. K. (2004). Seasonal drought and dry-season irrigation influence leaf-litter nutrients and soil enzymes in a moist, lowland forest in Panama. Austral Ecology, 29(2), 177-188. https://doi.org/10.1111/j.1442-9993.2004.01334.x
Zechmeister-Boltenstern, S., Keiblinger, K. M., Mooshammer, M., Peñuelas, J., Richter, A., Sardans, J., & Wanek, W. (2015). The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecological Monographs, 85(2), 133-155. https://doi.org/10.1890/14-0777.1
Zeglin, L. H., Stursova, M., Sinsabaugh, R. L., & Collins, S. L. (2007). Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia, 154(2), 349-359. https://doi.org/10.1007/s00442-007-0836-6
Zhang, N., Guo, R., Song, P., Guo, J., & Gao, Y. (2013). Effects of warming and nitrogen deposition on the coupling mechanism between soil nitrogen and phosphorus in Songnen Meadow Steppe, northeastern China. Soil Biology and Biochemistry, 65, 96-104. https://doi.org/10.1016/j.soilbio.2013.05.015
Zhang, Z. J., Li, H. Y., Hu, J., Li, X., He, Q., Tian, G. M., Wang, H., Wang, S. Y., & Wang, B. (2015). Do microorganism stoichiometric alterations affect carbon sequestration in paddy soil subjected to phosphorus input? Ecological Applications, 25(3), 866-879. https://doi.org/10.1890/14-0189.1
Zheng, J.-Q., Han, S.-J., Zhou, Y.-M., Ren, F.-R., Xin, L.-H., & Zhang, Y. (2010). Microbial activity in a temperate forest soil as affected by elevated atmospheric CO2. Pedosphere, 20(4), 427-435. https://doi.org/10.1016/S1002-0160(10)60032-X
Zheng, M., Huang, J., Chen, H., Wang, H., & Mo, J. (2015). Responses of soil acid phosphatase and beta-glucosidase to nitrogen and phosphorus addition in two subtropical forests in southern China. European Journal of Soil Biology, 68, 77-84. https://doi.org/10.1016/j.ejsobi.2015.03.010
Zhou, S., Williams, A. P., Berg, A. M., Cook, B. I., Zhang, Y., Hagemann, S., Lorenz, R., Seneviratne, S. I., & Gentine, P. (2019). Land-atmosphere feedbacks exacerbate concurrent soil drought and atmospheric aridity. Proceedings of the National Academy of Sciences of the United States of America, 116(38), 18848-18853. https://doi.org/10.1073/pnas.1904955116
Zhu, F., Yoh, M., Gilliam, F. S., Lu, X., & Mo, J. (2013). Nutrient limitation in three lowland tropical forests in southern China receiving high nitrogen deposition: Insights from fine root responses to nutrient additions. PLoS One, 8(12), 1-8. https://doi.org/10.1371/journal.pone.0082661
Zhu, Q., Riley, W. J., Tang, J., Collier, N., Hoffman, F. M., Yang, X., & Bisht, G. (2019). Representing nitrogen, phosphorus, and carbon interactions in the E3SM Land Model: Development and global benchmarking. Journal of Advances in Modeling Earth Systems, 11(7), 2238-2258. https://doi.org/10.1029/2018MS001571
Zhu, Z., Piao, S., Myneni, R. B., Huang, M., Zeng, Z., Canadell, J. G., Ciais, P., Sitch, S., Friedlingstein, P., Arneth, A., Cao, C., Cheng, L., Kato, E., Koven, C., Li, Y., Lian, X. U., Liu, Y., Liu, R., Mao, J., … Zeng, N. (2016). Greening of the Earth and its drivers. Nature Climate Change, 6(8), 791-795. https://doi.org/10.1038/nclimate3004