Skip to main content

Advertisement

SpringerLink
Log in

Future challenges in coupled C–N–P cycle models for terrestrial ecosystems under global change: a review

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Climate change has consequences for terrestrial functioning, but predictions of plant responses remain uncertain because of the gaps in the representation of nutrient cycles and C–N–P interactions in ecosystem models. Here, we review the processes that are included in ecosystem models, but focus on coupled C–N–P cycle models. We highlight important plant adjustments to climate change, elevated atmospheric CO2, and/or nutrient limitations that are currently not—or only partially—incorporated in ecosystem models by reviewing experimental studies and compiling data. Plant adjustments concern C:N:P stoichiometry, photosynthetic capacity, nutrient resorption rates, allocation patterns, symbiotic N2 fixation and root exudation (phosphatases, carboxylates) and the effect of root exudation on nutrient mobilization in the soil rhizosphere (P solubilization, biochemical mineralization of organic P and priming effect). We showed that several plant adjustments could be formulated and calibrated using existing experimental data in the literature. Finally, we proposed a roadmap for future research because improving ecosystem models necessitate specific data and collaborations between modelers and empiricists.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aber JD, Ollinger SV, Driscoll CT (1997) Modeling nitrogen saturation in forest ecosystems in response to land use and atmospheric deposition. Ecol Model 101:61–78

    Article  Google Scholar 

  • Abrahao A, Lambers H, Sawaya ACHF, Mazzafera P, Oliveira RS (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176:345–355

    Article  Google Scholar 

  • Achat DL, Bakker MR, Morel C (2009) Process-based assessment of phosphorus availability in a low phosphorus sorbing forest soil using isotopic dilution methods. Soil Sci Soc Am J 73:2131–2142

    Article  Google Scholar 

  • Achat DL, Bakker MR, Zeller B, Pellerin S, Bienaime S, Morel C (2010) Long term organic phosphorus mineralization in Spodosols under forests and its relation to carbon and nitrogen mineralization. Soil Biol Biochem 42:1479–1490

    Article  Google Scholar 

  • Achat DL, Augusto L, Bakker MR, Gallet-Budynek A, Morel C (2012) Microbial processes controlling P availability in forest Spodosols as affected by soil depth and soil properties. Soil Biol Biochem 44:39–48

    Article  Google Scholar 

  • Achat DL, Pousse N, Nicolas M, Brédoire F, Augusto L (2016) Soil properties controlling inorganic phosphorus availability: general results from a national forest network and a global compilation of the literature. Biogeochemistry 127:255–272

    Article  Google Scholar 

  • Ågren GI, Wetterstedt JÅ, Billberger MF (2012) Nutrient limitation on terrestrial plant growth–modeling the interaction between nitrogen and phosphorus. New Phytol 194:953–960

    Article  Google Scholar 

  • Ali MA, Louche J, Legname E, Duchemin M, Plassard C (2009) Pinus pinaster seedlings and their fungal symbionts show high plasticity in phosphorus acquisition in acidic soils. Tree Physiol 29:1587–1597

    Article  Google Scholar 

  • Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. PNAS 105:11512–11519

    Article  Google Scholar 

  • Almeida JPF, Lüscher A, Frehner M, Oberson A, Nösberger J (1999) Partitioning of P and the activity of root acid phosphatase in white clover (Trifolium repens L.) are modified by increased atmospheric CO2 and P fertilization. Plant Soil 210:159–166

    Article  Google Scholar 

  • Annaheim KE, Doolette AL, Smernik RJ, Mayer J, Oberson A, Frossard E, Bünemann EK (2015) Long-term addition of organic fertilizers has little effect on soil organic phosphorus as characterized by 31P NMR spectroscopy and enzyme additions. Geoderma 257–258:67–77

    Article  Google Scholar 

  • Arain MA, Yuan F, Black TA (2006) Soil–plant nitrogen cycling modulated carbon exchanges in a western temperate conifer forest in Canada. Agric For Meteorol 140:171–192

    Article  Google Scholar 

  • Arróniz-Crespo M, Leake JR, Horton P, Phoenix GK (2008) Bryophyte physiological responses to, and recovery from, long-term nitrogen deposition and phosphorus fertilisation in acidic grassland. New Phytol 180:864–874

    Article  Google Scholar 

  • Asner GP, Knapp DE, Anderson CB, Martin RE, Vaughn N (2016) Large-scale climatic and geophysical controls on the leaf economics spectrum. PNAS 113:E4043–E4051

    Article  Google Scholar 

  • Augusto L, Delerue F, Gallet-Budynek A, Achat DL (2013) Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Glob Biogeochem Cycles 27:804–815

    Article  Google Scholar 

  • Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr 12:547–561

    Article  Google Scholar 

  • Barrow NJ (2008) The description of sorption curves. Eur J Soil Sci 59:900–910

    Article  Google Scholar 

  • Batterman SA, Wurzburger N, Hedin LO (2013) Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J Ecol 101:1400–1408

    Article  Google Scholar 

  • Bloom AJ, Chapin FS, Mooney HA (1985) Resource limitation in plants—an economic analogy. Ann Rev Ecol Syst 16:363–392

    Article  Google Scholar 

  • Bown HE, Watt MS, Clinton PW, Mason EG, Richardson B (2007) Partititioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiate. Tree Physiol 27:335–344

    Article  Google Scholar 

  • Bunemann EK (2008) Enzyme additions as a tool to assess the potential bioavailability of organically bound nutrients. Soil Biol Biochem 40:2116–2129

    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

    Article  Google Scholar 

  • Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95

    Article  Google Scholar 

  • Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20:3646–3659

    Article  Google Scholar 

  • Cameron DR et al (2013) Environmental change impacts on the C- and N-cycle of European forests: a model comparison study. Biogeosciences 10:1751–1773

    Article  Google Scholar 

  • Canham CD, Berkowitz AR, Kelly VR, Lovett GM, Ollinger SV, Schnurr J (1996) Biomass allocation and multiple resource limitation in tree seedlings. Can J For Res 26:1521–1530

    Article  Google Scholar 

  • Carswell FE, Grace J, Lucas ME, Jarvis PG (2000) Interaction of nutrient limitation and elevated CO2 concentration on carbon assimilation of a tropical tree seedling (Cedrela odorata). Tree Physiol 20:977–986

    Article  Google Scholar 

  • Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development. Nature 397:491–497

    Article  Google Scholar 

  • Churkina G, Brovkin V, von Bloh W, Trusilova K, Jung M, Dentener F (2009) Synergy of rising nitrogen depositions and atmospheric CO2 on land carbon uptake moderately offsets global warming. Glob Biogeochem Cycle 23:GB4027

    Article  Google Scholar 

  • Condit R, Engelbrecht BMJ, Pino D, Perez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. PNAS 110:5064–5068

    Article  Google Scholar 

  • Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation: applications to the biogeochemical cycle of soil phosphorus in natural ecosystems. Geoderma 64:197–214

    Article  Google Scholar 

  • CSIRO, Commonwealth Scientific and Industrial Research Organisation (1997) Plant analysis: an interpretation manual. In: Reuter DJ, Robinson JB (ed), CSIRO Publishing, Collingwood

  • Cumming JR (1993) Growth and nutrition of nonmycorrhizal and mycorrhizal pitch pine (Pinus rigida) seedlings under phosphorus limitation. Tree Physiol 13:173–187

    Article  Google Scholar 

  • Davies JAC, Tipping E, Rowe EC, Boyle JF, Pannatier EG, Martinsen V (2016) Long-term P weathering and recent N deposition control contemporary plant-soil C, N and P. Glob Biogeochem Cycle. doi:10.1002/2015GB005167

    Google Scholar 

  • De Kauwe MG et al (2014) Where does the carbon go? A model–data intercomparison of vegetation carbon allocation and turnover processes at two temperate forest free-air CO2 enrichment sites. New Phytol 203:883–899

    Article  Google Scholar 

  • Delgado D, Zúñiga-Feest A, Alvear M, Borie F (2013) The effect of phosphorus on cluster-root formation and functioning of Embothrium coccineum (R. et J. Forst.). Plant Soil 373:765–773

    Article  Google Scholar 

  • Devau N, Le Cadre E, Hinsinger P, Jaillard B, Gerard F (2009) Soil pH controls the environmental availability of phosphorus: experimental and mechanistic modelling approaches. Appl Geochem 24:2163–2174

    Article  Google Scholar 

  • Devau N, Hinsinger P, Le Cadre E, Gérard F (2011) Root-induced processes controlling phosphate availability in soils with contrasted P-fertilized treatments. Plant Soil 348:203–218

    Article  Google Scholar 

  • Drake JE et al (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357

    Article  Google Scholar 

  • Duputel M, Devau N, Brossard M, Jaillard B, Jones DL, Hinsinger P, Gérard F (2013) Citrate adsorption can decrease soluble phosphate concentration in soils: results of theoretical modeling. Appl Geochem 35:120–131

    Article  Google Scholar 

  • Egle K, Romer W, Keller H (2003) Exudation of low molecular weight organic acids by Lupinus albus L., Lupinus angustifolius L. and Lupinus luteus L. as affected by phosphorus supply. Agronomie 23:511–518

    Article  Google Scholar 

  • Ellsworth DS, Crous KY, Lambers H, Cooke J (2015) Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species. Plant Cell Environ 38:1142–1156

    Article  Google Scholar 

  • Elser J, Bracken M, Cleland E, Gruner D, Harpole W, Hillebrand H, Ngai J, Seabloom E, Shurin J, Smith J (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  Google Scholar 

  • Esser G, Kattge J, Sakalli A (2011) Feedback of carbon and nitrogen cycles enhances carbon sequestration in the terrestrial biosphere. Glob Chang Biol 17:819–842

    Article  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  Google Scholar 

  • Finzi AC, Cole JJ, Doney SC, Holland EA, Jackson RB (2011) Research frontiers in the analysis of coupled biogeochemical cycles. Front Ecol Environ 9:74–80

    Article  Google Scholar 

  • Finzi AC et al (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094

    Article  Google Scholar 

  • Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  Google Scholar 

  • Fox TR, Comerford NB (1992) Rhizosphere phosphatase activity and phosphatase hyrolyzable organic phosphorus in two forested spodosols. Soil Biol Biochem 24:579–583

    Article  Google Scholar 

  • Fung IY, Doney SC, Lindsay K, John J (2005) Evolution of carbon sinks in a changing climate. PNAS 102:11201–11206

    Article  Google Scholar 

  • Galloway JN et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  Google Scholar 

  • Garcia-Palacios P, Vandegehuchte ML, Shaw EA, Dam M, Post KH, Ramirez KS, Sylvain ZA, de Tomasel CM, Wall DH (2015) Are there links between responses of soil microbes and ecosystem functioning to elevated CO2, N deposition and warming? A global perspective. Glob Chang Biol 21:1590–1600

    Article  Google Scholar 

  • Gardner LB (1990) The role of rock weathering in the phosphorus budget of terrestrial watersheds. Biogeochemistry 11:97–110

    Article  Google Scholar 

  • Gaume A, Mächler F, De Leon C, Narro L, Frossard E (2001) Low-P tolerance by maize (Zea mays L.) genotypes: Significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil 228:253–264

    Article  Google Scholar 

  • Gerard F (2016) Clay minerals, iron/aluminum oxides, and their contribution to phosphate sorption in soils—a myth revisited. Geoderma 262:213–226

    Article  Google Scholar 

  • Gerber S, Hedin LO, Oppenheimer M, Pacala SW, Shevliakova E (2010) Nitrogen cycling and feedbacks in a global dynamic land model. Global Biogeochem Cycle 24:GB1001

    Google Scholar 

  • Gerke J (2015) The acquisition of phosphate by higher plants: Effect of carboxylate release by the roots. A critical review. J Plant Nutr Soil Sci 178:351–364

    Article  Google Scholar 

  • Ghannoum O, Paul MJ, Ward JL, Beale MH, Corol DI, Conroy JP (2008) The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses. Funct Plant Biol 35:213–221

    Article  Google Scholar 

  • Gifford RM, Lutze JL, Barrett D (1996) Global atmospheric change effects on terrestrial carbon sequestration: Exploration with a global C- and N-cycle model (CQUESTN). Plant Soil 187:369–387

    Article  Google Scholar 

  • Gilhespy SL et al (2014) First 20 years of DNDC (denitrification decomposition): Model evolution. Ecol Model 292:51–62

    Article  Google Scholar 

  • Goll DS, Brovkin V, Parida BR, Reick CH, Kattge J, Reich PB, van Bodegom PM, Niinemets U (2012) Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences 9:3547–3569

    Article  Google Scholar 

  • Grant RF (1991) A technique for estimating denitrification rates at different soil temperatures, water contents, and nitrate concentrations. Soil Sci 152:41–52

    Article  Google Scholar 

  • Grant RF, Nyborg M, Laidlaw J (1993a) Evolution of nitrous oxide from soil: 1. Model development. Soil Sci 156:259–265

    Article  Google Scholar 

  • Grant RF, Nyborg M, Laidlaw J (1993b) Evolution of nitrous oxide from soil: II. Experimental results and model testing. Soil Sci 156:266–277

    Article  Google Scholar 

  • Grant RF et al (1999) Diurnal and annual exchanges of mass and energy between an aspen-hazelnut forest and the atmosphere: Testing the mathematical model Ecosys with data from the BOREAS experiment. J Geophys Res 104:27699–27717

    Article  Google Scholar 

  • Grant RF et al (2001) Controls on carbon and energy exchange by a black spruce-moss ecosystem: testing the mathematical model Ecosys with data from the BOREAS experiment. Global Biogeochem Cycle 15:129–147

    Article  Google Scholar 

  • Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296

    Article  Google Scholar 

  • Güsewell S, Gessner MO (2009) N: P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219

    Article  Google Scholar 

  • Han W, Tang L, Chen Y, Fang J (2013) Relationship between the relative limitation and resorption efficiency of nitrogen vs phosphorus in woody plants. PLoS ONE 8:e83366

    Article  Google Scholar 

  • Hanson PJ et al (2004) Oak forest carbon and water simulations: model intercomparisons and evaluations against independent data. Ecol Monogr 74:443–489

    Article  Google Scholar 

  • Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862

    Article  Google Scholar 

  • Hedin LO, Vitousek PM, Matson PA (2003) Nutrient losses over four million years of tropical forest development. Ecology 84:2231–2255

    Article  Google Scholar 

  • Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292

    Article  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  Google Scholar 

  • Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129

    Article  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195

    Article  Google Scholar 

  • Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330

    Article  Google Scholar 

  • Hungate BA, Dukes JS, Shaw MR, Luo Y, Field CB (2003) Nitrogen and climate change. Science 302:1512–1513

    Article  Google Scholar 

  • Hunt ER Jr, Lavigne MB, Franklin SE (1999) Factors controlling the decline of net primary production with stand age for balsam fir in Newfoundland assessed using an ecosystem simulation model. Ecol Model 122:151–164

    Article  Google Scholar 

  • Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytol 186:346–357

    Article  Google Scholar 

  • Jansson PE, Karlberg L (2001) Coupled heat and mass transfer model for soil-plant-atmosphere systems. Royal Institute of Technology, Department of Civil and Environmental Engineering, Stockholm. (ftp://www.lwr.kth.se/CoupModel/CoupModel.pdf), p 321

  • Jarosch KA, Doolette AL, Smernik RJ, Tamburini F, Frossard E, Bünemann EK (2015) Characterisation of soil organic phosphorus in NaOH-EDTA extracts: a comparison of 31P NMR spectroscopy and enzyme addition assays. Soil Biol Biochem 91:298–309

    Article  Google Scholar 

  • Jin J, Tang C, Salte P (2015) The impact of elevated carbon dioxide on the phosphorus nutrition of plants: a review. Ann Bot 116:987–999

    Article  Google Scholar 

  • Johnson D, Leake JR, Lee JA (1999) The effects of quantity and duration of simulated pollutant nitrogen deposition on root-surface phosphatase activities in calcareous and acid grasslands: a bioassay approach. New Phytol 141:433–442

    Article  Google Scholar 

  • Kamh M, Abdou M, Chude V, Wiesler F, Horst WJ (2002) Mobilization of phosphorus contributes to positive rotational effects of leguminous cover crops on maize grown on soils from northern Nigeria. J Plant Nutr Soil Sci 165:566–572

    Article  Google Scholar 

  • Karam SL, Weisberg PJ, Scheller RM, Johnson DW, Miller WW (2013) Development and evaluation of a nutrient cycling extension for the LANDIS-II landscape simulation model. Ecol Model 250:45–57

    Article  Google Scholar 

  • Keller M, Oberson A, Annaheim KE, Tamburini F, Mäder P, Mayer J, Frossard E, Bünemann EK (2012) Phosphorus forms and enzymatic hydrolyzability of organic phosphorus in soils after 30 years of organic and conventional farming. J Plant Nutr Soil Sci 175:385–393

    Article  Google Scholar 

  • Kimmins JP, Mailly D, Seely B (1999) Modelling forest ecosystem net primary production: the hybrid simulation approach used in FORECAST. Ecol Model 122:195–224

    Article  Google Scholar 

  • Kirschbaum MUF (1999) CenW, a forest growth model with linked carbon, energy, nutrient and water cycles. Ecol Model 118:17–59

    Article  Google Scholar 

  • Kirschbaum MUF, Paul KI (2002) Modelling carbon and nitrogen dynamics in forest soils with a modified version of the CENTURY model. Soil Biol Biochem 34:341–354

    Article  Google Scholar 

  • Kohler IH, MacDonald A, Schnyder H (2012) Nutrient supply enhanced the increase in intrinsic water use efficiency of a temperate semi natural grassland in the last century. Glob Chang Biol 18:3367–3376

    Article  Google Scholar 

  • Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713

    Article  Google Scholar 

  • Leff JW et al (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. PNAS 112:10967–10972

    Article  Google Scholar 

  • Lewis DR, McGechan MB (2002) A review of field scale phosphorus dynamics models. Biosyst Eng 82:359–380

    Article  Google Scholar 

  • Li C, Frolking S, Frolking TA (1992) A model of nitrous oxide evolution from soil driven by rainfall events: 1. Model structure and sensitivity. J Geophys Res 97:9759–9776

    Article  Google Scholar 

  • Li M, Osaki M, Rao IM, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant Soil 195:161–169

    Article  Google Scholar 

  • Liebig J (1842) Animal chemistry, or organic chemistry in its application to physiology and pathology. Johnson Reprint Corporation, New York

    Google Scholar 

  • Liu S, Munson R, Johnson DW, Gherini S, Summers K, Hudson R, Wilkinson K, Pitelka LF (1991) Application of a nutrient cycling model (NuCM) to northern mixed hardwood and southern coniferous forests. Tree Physiol 9:173–182

    Article  Google Scholar 

  • Liu Y, Mi G, Chen F, Zhang J, Zhang F (2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci 167:217–223

    Article  Google Scholar 

  • Loustau D, Brahim MB, Gaudillere JP, Dreyer E (1999) Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings. Tree Physiol 19:707–715

    Article  Google Scholar 

  • Lü XT, Reed SC, Yu Q, Han XG (2016) Nutrient resorption helps drive intra-specific coupling of foliar nitrogen and phosphorus under nutrient-enriched conditions. Plant Soil 398:111–120

    Article  Google Scholar 

  • Luo Y et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  Google Scholar 

  • Marklein AR et al (2015) Mineralization ratios of nitrogen and phosphorus from decomposing litter in temperate versus tropical forests. Glob Ecol Biogeogr 25:335–346

    Article  Google Scholar 

  • Matear RJ, Wang YP, Lenton A (2010) Land and ocean nutrient and carbon cycle interactions. Curr Opin Environ Sustain 2:258–263

    Article  Google Scholar 

  • McGechan MB (2002) Sorption of phosphorus by soil, Part 2: measurement methods, results and model parameter values. Biosyst Eng 82:115–130

    Article  Google Scholar 

  • McGechan MB, Lewis DR (2002) Sorption of phosphorus by soil, Part 1: principles, equations and models. Biosyst Eng 82:1–24

    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

    Article  Google Scholar 

  • McMurtrie RE, Dewar RC, Medlyn BE, Jeffreys MP (2000) Effects of elevated [CO2] on forest growth and carbon storage: a modelling analysis of the consequences of changes in litter quality/quantity and root exudation. Plant Soil 224:135–152

    Article  Google Scholar 

  • Medlyn BE, Duursma RA, Zeppel MJB (2011) Forest productivity under climate change: a checklist for evaluating model studies. Wiley Interdiscip Rev-Clim Chang 2:332–355

    Article  Google Scholar 

  • Menge DN, Lichstein JW, Ángeles-Pérez G (2014) Nitrogen fixation strategies can explain the latitudinal shift in nitrogen-fixing tree abundance. Ecology 95:2236–2245

    Article  Google Scholar 

  • Menge DN, Wolf AA, Funk JL (2015) Diversity of nitrogen fixation strategies in Mediterranean legumes. Nature Plants 1:1–5

    Article  Google Scholar 

  • Metherell AK, Harding LA, Cole CV, Parton WJ (1993) CENTURY soil organic matter model environment. Technical documentation. Agroecosystem Version 4.0. Great Plains System Research Unit. Technical Report No. 4. USDA-ARS, Fort Collins. https://www.nrel.colostate.edu/projects/century/

  • Meunier CL, Gundale MJ, Sanchez IS, Liess A (2016) Impact of nitrogen deposition on forest and lake food webs in nitrogen-limited environments. Glob Chang Biol 22:164–179

    Article  Google Scholar 

  • Meyerholt J, Zaehle S (2015) The role of stoichiometric flexibility in modelling forest ecosystem responses to nitrogen fertilization. New Phytol 208:1042–1055

    Article  Google Scholar 

  • Montzka SA, Dlugokencky EJ, Butler JH (2011) Non-CO2 greenhouse gases and climate change. Nature 476:43–50

    Article  Google Scholar 

  • Morel C, Ziadi N, Messiga A, Belanger G, Denoroy P, Jeangros B, Jouany C, Fardeau JC, Mollier A, Parent LE, Proix N, Rabeharisoa L, Sinaj S (2014) Modeling of phosphorus dynamics in contrasting agroecosystems using long-term field experiments. Can J Soil Sci 94:377–387

    Article  Google Scholar 

  • Negrin MA, Gonzalez-Carcedo S, Hernandez-Moreno JM (1995) P fractionation in sodium bicarbonate extracts of andic soils. Soil Biol Biochem 21:761–766

    Article  Google Scholar 

  • Newman EI (1995) Phosphorus inputs to terrestrial ecosystems. J Ecol 83:713–726

    Article  Google Scholar 

  • Noormets A, Epron D, Domec JC, McNulty SG, Fox T, Sun G, King JS (2015) Effects of forest management on productivity and carbon sequestration: a review and hypothesis. For Ecol Manage 355:124–140

    Article  Google Scholar 

  • Norby RJ et al (2016) Model-data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments. New Phytol 209:17–28

    Article  Google Scholar 

  • O’Hara GW (2001) Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: a review. Aust J Exp Agr 41:417–433

    Article  Google Scholar 

  • Oburger E, Jones DL, Wenzel WW (2011) Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil. Plant Soil 341:363–382

    Article  Google Scholar 

  • Oehl F, Oberson A, Sinaj S, Frossard E (2001) Organic phosphorus mineralization studies using isotopic dilution techniques. Soil Sci Soc Am J 65:780–787

    Article  Google Scholar 

  • Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675

    Article  Google Scholar 

  • Olander L, Vitousek P (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–191

    Article  Google Scholar 

  • Otani T, Ae N (1999) Extraction of organic phosphorus in Andosols by various methods. Soil Sci Plant Nutr 45:151–161

    Article  Google Scholar 

  • Pant HK, Warman PR (2000) Enzymatic hydrolysis of soil organic phosphorus by immobilized phosphatases. Biol Fertil Soils 30:306–311

    Article  Google Scholar 

  • Parton WJ, Schimel DJ, Cole CV, Ojima DS (1987) Analysis of factors controlling soil organic matter levels in great plains grasslands. Soil Sci Soc Am J 51:1173–1179

    Article  Google Scholar 

  • Parton WJ, Stewart JWB, Cole CV (1988) Dynamics of C, N, P and S in grassland soils: a model. Biogeochemistry 5:109–131

    Article  Google Scholar 

  • Parton WJ, Hartman M, Ojima D, Schimel D (1998) DAYCENT and its land surface submodel: description and testing. Glob Planet Chang 19:35–48

    Article  Google Scholar 

  • Parton WJ, Hanson PJ, Swanston C, Torn M, Trumbore SE, Riley W, Kelly R (2010) ForCent model development and testing using the enriched background isotope study experiment. J Geophys Res 115:G04001

    Article  Google Scholar 

  • Penuelas J et al (2013) Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934

    Google Scholar 

  • Persson J, Nasholm T (2002) Regulation of amino acid uptake in conifers by exogenous and endogenous nitrogen. Planta 215:639–644

    Article  Google Scholar 

  • Phillips RP, Bernhardt ES, Schlesinger WH (2009) Elevated CO2 increases root exudation from loblolly pine (Pinus taeda) seedlings as an N-mediated response. Tree Physiol 29:1513–1523

    Article  Google Scholar 

  • Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194

    Article  Google Scholar 

  • Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2003) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289

    Article  Google Scholar 

  • Phuyal M, Artz RRE, Sheppard L, Leith ID, Johnson D (2008) Long-term nitrogen deposition increases phosphorus limitation of bryophytes in an ombrotrophic bog. Plant Ecol 196:111–121

    Article  Google Scholar 

  • Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139

    Article  Google Scholar 

  • Playsted CWS, Johnston ME, Ramage CM, Edwards DG, Cawthray GR, Lambers H (2006) Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytol 170:491–500

    Article  Google Scholar 

  • Porté A, Loustau D (1998) Variability of the photosynthetic characteristics of mature needles within the crown of a 25-year-old Pinus pinaster. Tree Physiol 18:223–232

    Article  Google Scholar 

  • Qualls RG, Richardson CJ (2003) Factors controlling concentration, export, and decomposition of dissolved organic nutrients in the Everglades of Florida. Biogeochemistry 62:197–229

    Article  Google Scholar 

  • Rasse DP (2002) Nitrogen deposition and atmospheric CO2 interactions on fine root dynamics in temperate forests: a theoretical model analysis. Glob Chang Biol 8:486–503

    Article  Google Scholar 

  • Rastetter EB (2011) Modeling coupled biogeochemical cycles. Front Ecol Environ 9:68–73

    Article  Google Scholar 

  • Reddell P, Yun Y, Shipton WA (1997) Do Casuarina cunninghamiana seedlings dependent on symbiotic N2 fixation have higher phosphorus requirements than those supplied with adequate fertilizer nitrogen? Plant Soil 189:213–219

    Article  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: A contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512

    Article  Google Scholar 

  • Reed SC, Yang X, Thornton PE (2015) Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor. New Phytol 208:324–329

    Article  Google Scholar 

  • Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160:207–212

    Article  Google Scholar 

  • Rejmankova E, Snyder JM (2008) Emergent macrophytes in phosphorus limited marshes: do phosphorus usage strategies change after nutrient addition? Plant Soil 313:141–153

    Article  Google Scholar 

  • Requejo MI, Eichler-Lobermann B (2014) Organic and inorganic phosphorus forms in soil as affected by long-term application of organic amendments. Nutr Cycl Agroecosyst 100:245–255

    Article  Google Scholar 

  • Ribet J, Drevon JJ (1996) The phosphorus requirement of N2-fixing and urea-fed Acacia mangium. New Phytol 132:383–390

    Article  Google Scholar 

  • Robson AD, Ohara GW, Abbott LK (1981) Involvement of phosphorus in nitrogen-fixation by subterranean clover (Trifolium subterraneum L). Aust J Plant Physiol 8:427–436

    Article  Google Scholar 

  • Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ 24:891–903

    Article  Google Scholar 

  • Rousk J, Brookes PC, Baath E (2011) Fungal and bacterial growth responses to N fertilization and pH in the150-year ‘Park Grass’ UK grassland experiment. FEMS Microbiol Ecol 76:89–99

    Article  Google Scholar 

  • Runing SW, Coulghan JC (1988) A general model of forest ecosystem processes for regional applications. I. Hydrologic balance, canopy gas exchange and primary production processes. Ecol Model 42:125–154

    Article  Google Scholar 

  • Sardans J et al (2016) Foliar and soil concentrations and stoichiometry of nitrogen and phosphorus across European Pinus sylvestris forests: relationships with climate, N deposition and tree growth. Funct Ecol. doi:10.1111/1365-2435.12541

    Google Scholar 

  • Scheller RM, Mladenoff DJ (2004) A forest growth and biomass module for a landscape simulation model, LANDIS: design, validation, and application. Ecol Model 180:211–229

    Article  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant–soil feedbacks in a northern hardwood forest. Ecology 96:2488–2498

    Article  Google Scholar 

  • Seeling B, Jungk A (1996) Utilization of organic phosphorus in calcium chloride extracts of soil by barley plants and hydrolysis by acid and alkaline phosphatases. Plant Soil 178:179–184

    Article  Google Scholar 

  • Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, Fontaine S (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155

    Article  Google Scholar 

  • Shane MW, de Vos M, de Roock S, Cawthray GR, Lambers H (2003) Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R. Br. Plant Soil 248:209–219

    Article  Google Scholar 

  • Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Sci 168:837–845

    Article  Google Scholar 

  • Smaill SJ, Clinton PW, Hock BK (2011) A nutrient balance model (NuBalM) to predict biomass and nitrogen pools in Pinus radiata forests. For Ecol Manag 262:270–277

    Article  Google Scholar 

  • Smith B, Warlind D, Arneth A, Hickler T, Leadley P, Siltberg J, Zaehle S (2014) Implications of incorporating N cycling and N limitations on primary production in an individual-based dynamic vegetation model. Biogeosciences 11:2027–2054

    Article  Google Scholar 

  • Sokolov AP et al (2008) Consequences of considering carbon–nitrogen interactions on the feedbacks between climate and the terrestrial carbon cycle. J Clim 21:3776–3796

    Article  Google Scholar 

  • Soussana JF, Tallec T (2010) Can we understand and predict the regulation of biological N2 fixation in grassland ecosystems? Nutr Cycl Agroecosys 88:197–213

    Article  Google Scholar 

  • Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic phosphorus mineralization can be stimulated by root exudates—A 33P isotopic dilution study. Soil Biol Biochem 65:254–263

    Article  Google Scholar 

  • Sulman BN, Phillips RP, Oishi AC, Shevliakova E, Pacala SW (2014) Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nat Clim Chang 4:1099–1102

    Article  Google Scholar 

  • Tadano T, Sakai H (1991) Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions. Soil Sci Plant Nutr 37:129–140

    Article  Google Scholar 

  • Tang JY, Riley WJ (2013) A total quasi-steady-state formulation of substrate uptake kinetics in complex networks and an example application to microbial litter decomposition. Biogeosciences 10:8329–8351

    Article  Google Scholar 

  • Tang JY, Riley WJ (2014) Weaker soil carbon-climate feedbacks resulting from microbial and abiotic interactions. Nat Clim Chang 5:56–60

    Article  Google Scholar 

  • Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environ Exp Bot 67:228–234

    Article  Google Scholar 

  • Tang HL, Shen JB, Zhang FS, Rengel Z (2013) Interactive effects of phosphorus deficiency and exogenous auxin on root morphological and physiological traits in white lupin (Lupinus albus L.). Sci China Life Sci 56:313–323

    Article  Google Scholar 

  • Thomas RQ, Brookshire ENJ, Gerber S (2015) Nitrogen limitation on land: how can it occur in Earth system models? Glob Chang Biol 21:1777–1793

    Article  Google Scholar 

  • Thornton PE, Lamarque JF, Rosenbloom NA, Mahowald NM (2007) Influence of carbon-nitrogen cycle coupling on land model response to CO2 fertilization and climate variability. Global Biogeochem Cycle 21:GB4018

    Article  Google Scholar 

  • Thornton PE, Doney SC, Lindsay K, Moore JK, Mahowald N, Randerson JT, Fung I, Lamarque JF, Feddema JJ, Lee YH (2009) Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model. Biogeosciences 6:2099–2120

    Article  Google Scholar 

  • Tipping E, Rowe E, Evans C, Mills R, Emmett B, Chaplow J, Hall J (2012) N14C: a plant–soil nitrogen and carbon cycling model to simulate terrestrial ecosystem responses to atmospheric nitrogen deposition. Ecol Model 247:11–26

    Article  Google Scholar 

  • Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD (2012) A framework for representing microbial decomposition in coupled climate models. Biogeochemistry 109:19–33

    Article  Google Scholar 

  • Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118

    Article  Google Scholar 

  • Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9:9–17

    Article  Google Scholar 

  • Treseder K, Vitousek P (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82:946–954

    Article  Google Scholar 

  • Treseder KK et al (2012) Integrating microbial ecology into ecosystem models: challenges and priorities. Biogeochemistry 109:7–18

    Article  Google Scholar 

  • Turner BL (2005) Storage-induced changes in phosphorus solubility of air-dried soils. Soil Sci Soc Am J 69:630–633

    Article  Google Scholar 

  • Turner BL, McKelvie ID, Haygarth PM (2002) Characterisation of water-extractable soil organic phosphorus by phosphatase hydrolysis. Soil Biol Biochem 34:27–35

    Article  Google Scholar 

  • Ushio M, Fujiki Y, Hidaka A, Kitayama K (2015) Linkage of root physiology and morphology as an adaptation to soil phosphorus impoverishment in tropical montane forests. Funct Ecol 29:1235–1245

    Article  Google Scholar 

  • van Groenigen KJ, Six J, Hungate BA, de Graaff MA, van Breemen N, van Kessel C (2006) Element interactions limit soil carbon storage. PNAS 103:6571–6574

    Article  Google Scholar 

  • Vargas R, Carbone MS, Reichstein M, Baldocchi DD (2011) Frontiers and challenges in soil respiration research: from measurements to model-data integration. Biogeochemistry 102:1–13

    Article  Google Scholar 

  • Verburg PSJ, Johnson DW (2001) A spreadsheet-based biogeochemical model to simulate nutrient cycling processes in forest ecosystems. Ecol Model 141:185–200

    Article  Google Scholar 

  • Vergutz L et al (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45

    Article  Google Scholar 

  • Vitousek PM, Menge DN, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Philos Trans R Soc B 368:20130119

    Article  Google Scholar 

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  Google Scholar 

  • Walker AP et al (2014a) The relationship of leaf photosynthetic traits—Vcmax and Jmax—to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecol Evol 4:3218–3235

    Article  Google Scholar 

  • Walker AP et al (2014b) Comprehensive ecosystem model-data synthesis using multiple data sets at two temperate forest free-air CO2 enrichment experiments: model performance at ambient CO2 concentration. J Geophys Res Biogeosci 119(5):937–964

    Article  Google Scholar 

  • Wang YP, Houlton BZ, Field CB (2007) A model of biogeochemical cycles of carbon, nitrogen and phosphorus including symbiotic nitrogen fixation and phosphatase production. Glob Biogeochem Cycle 21:GB1018

    Article  Google Scholar 

  • Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7:2261–2282

    Article  Google Scholar 

  • Wang F et al (2014) Multimodel simulations of forest harvesting effects on long-term productivity and CN cycling in aspen forests. Ecol Appl 24:1374–1389

    Article  Google Scholar 

  • Wassen MJ, de Boer HJ, Fleischer K, Rebel KT, Dekker SC (2013) Vegetation-mediated feedback in water, carbon, nitrogen and phosphorus cycles. Landsc Ecol 28:599–614

    Article  Google Scholar 

  • Wei L, Chen C, Xu Z (2010) Citric acid enhances the mobilization of organic phosphorus in subtropical and tropical forest soils. Biol Fertil Soils 46:765–769

    Article  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

    Article  Google Scholar 

  • Wilson KB, Baldocchi DD, Hanson PJ (2000) Spatial and seasonal variability of photosynthetic parameters and their relationship to leaf nitrogen in a deciduous forest. Tree Physiol 20:565–578

    Article  Google Scholar 

  • Wyngaard N, Cabrera ML, Jarosch KA, Bünemann EK (2016) Phosphorus in the coarse soil fraction is related to soil organic phosphorus mineralization measured by isotopic dilution. Soil Biol Biochem 96:107–118

    Article  Google Scholar 

  • Xu-Ri, Prentice IC (2008) Terrestrial nitrogen cycle simulation with a dynamic global vegetation model. Glob Chang Biol 14:1745–1764

    Article  Google Scholar 

  • Yang X, Wittig V, Jain AK, Post W (2009) Integration of nitrogen cycle dynamics into the Integrated Science Assessment Model for the study of terrestrial ecosystem responses to global change. Glob Biogeochem Cycle 23:GB4029

    Article  Google Scholar 

  • Yang X, Post WM, Thornton PE, Jain A (2013) The distribution of soil phosphorus for global biogeochemical modeling. Biogeosciences 10:2525–2537

    Article  Google Scholar 

  • Yang X, Thornton PE, Ricciuto DM, Post WM (2014) The role of phosphorus dynamics in tropical forests—a modeling study using CLM-CNP. Biogeosciences 11:1667–1681

    Article  Google Scholar 

  • Zaehle S, Dalmonech D (2011) Carbon–nitrogen interactions on land at global scales: current understanding in modelling climate biosphere feedbacks. Curr Opin Environ Sustain 3:311–320

    Article  Google Scholar 

  • Zaehle S, Friend AD (2010) Carbon and nitrogen cycle dynamics in the O-CN land surface model: 1. Model description, site-scale evaluation, and sensitivity to parameter estimates. Global Biogeochem Cycle 24:GB1005

    Google Scholar 

  • Zaehle S, Friedlingstein P, Friend AD (2010a) Terrestrial nitrogen feedbacks may accelerate future climate change. Geophys Res Lett 37:L01401

    Article  Google Scholar 

  • Zaehle S, Friend AD, Friedlingstein P, Dentener F, Peylin P, Schulz M (2010b) Carbon and nitrogen cycle dynamics in the O-CN land surface model: 2. Role of the nitrogen cycle in the historical terrestrial carbon balance. Global Biogeochem Cycle 24:GB1006

    Google Scholar 

  • Zaehle S et al (2014) Evaluation of 11 terrestrial carbon–nitrogen cycle models against observations from two temperate Free-Air CO2 Enrichment studies. New Phytol 202:803–822

    Article  Google Scholar 

  • Zhang Q, Wang YP, Pitman AJ, Dai YJ (2011) Limitations of nitrogen and phosphorous on the terrestrial carbon uptake in the 20th century. Geophys Res Lett 38:L22701

    Google Scholar 

  • Zhang Q, Pitman AJ, Wang YP, Dai YJ, Lawrence PJ (2013a) The impact of nitrogen and phosphorous limitation on the estimated terrestrial carbon balance and warming of land use change over the last 156 yr. Earth Syst Dyn 4:333–345

    Article  Google Scholar 

  • Zhang Y, Zhou Z, Yang Q (2013b) Nitrogen (N) deposition impacts seedling growth of Pinus massoniana via N:P ratio effects and the modulation of adaptive responses to low P (phosphorus). PLoS ONE 8:e79229

    Article  Google Scholar 

  • Zhang S, Jiang H, Zhao H, Korpelainen H, Li C (2014) Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies. Tree Physiol 34:343–354

    Article  Google Scholar 

  • Zhu Z, Arp PA, Meng F, Bourque CPA, Foster NW (2003) A forest nutrient cycling and biomass model (ForNBM) based on year-round, monthly weather conditions, part I: assumption, structure and processing. Ecol Model 169:347–360

    Article  Google Scholar 

  • Zhu Q, Riley WJ, Tang J, Koven CD (2016) Multiple soil nutrient competition between plants, microbes, and mineral surfaces: model development, parameterization, and example applications in several tropical forests. Biogeosciences 13:341–363

    Article  Google Scholar 

  • Zhu-Barker X, Cavazos AR, Ostrom NE, Horwath WR, Glass JB (2015) The importance of abiotic reactions for nitrous oxide production. Biogeochemistry 126:251–267

    Article  Google Scholar 

  • Zou X, Binkley D, Caldwell BA (1995) Effects of dinitrogen-fixing trees on phosphorus biogeochemical cycling in contrasting forests. Soil Sci Soc Am J 59:1452–1458

    Article  Google Scholar 

Download references

Acknowledgements

This review was made in the framework of the David Achat’s research project, and the EVAFORA and MACACC projects supported by the French agency for energy and environment (ADEME) and the French National Research Agency (ANR), respectively. We thank Bruno Ringeval, Delphine Picard, Simon Martel and Sébastien Lafont for useful discussions. Finally, we thank editors Stephen Porder and Sharon Billings and two anonymous reviewers for improving the study.

Author information

Authors and Affiliations

  1. INRA, Bordeaux Sciences Agro, UMR 1391 ISPA, 33140, Villenave d’Ornon, France

    David L. Achat, Laurent Augusto, Anne Gallet-Budynek & Denis Loustau

Authors
  1. David L. Achat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laurent Augusto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anne Gallet-Budynek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denis Loustau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David L. Achat.

Additional information

Responsible Editor: Stephen Porder.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 182 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Achat, D.L., Augusto, L., Gallet-Budynek, A. et al. Future challenges in coupled C–N–P cycle models for terrestrial ecosystems under global change: a review. Biogeochemistry 131, 173–202 (2016). https://doi.org/10.1007/s10533-016-0274-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-016-0274-9

Keywords

Search

Navigation