The nitrogen (N) cycle in terrestrial ecosystems is strongly influenced by resorption before litter fall and by mineralization after litter fall. Although both resorption and mineralization make N available to plants and are influenced by climate, their linkage in a changing environment remains largely unknown. Here, our synthesis study shows that, at the global scale, increasing N-resorption efficiency negatively affects the N-mineralization rate. As temperature and precipitation increase, the increasing rates of N cycling closely correspond to a shift from the more conservative resorption pathway to the mineralization pathway. Furthermore, ecosystems with faster N-cycle rates support plant species that have higher foliar N:P ratios and microbial communities with lower fungi:bacteria ratios. Our study shows an ecosystem scale trade-off in N-acquisition pathways. We propose that incorporating the dynamic interaction between N resorption and N mineralization into Earth system models will improve the simulation of nutrient constraints on ecosystem productivity.
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Chapin, F. S., Matson, P. A. & Mooney, H. A. Principles of Terrestrial Ecosystem Ecology (Springer, New York, 2011).
Cleveland, C. C. et al. Patterns of new versus recycled primary production in the terrestrial biosphere. Proc. Natl Acad. Sci. USA 110, 12733–12737 (2013).
Wardle, D. A. et al. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633 (2004).
Thamdrup, B. New pathways and processes in the global nitrogen cycle. Annu. Rev. Ecol. Evol. Syst. 43, 407–428 (2012).
Aerts, R., Verhoeven, J. T. A. & Whigham, D. F. Plant-mediated controls on nutrient cycling in temperate fens and bogs. Ecology 80, 2170–2181 (1999).
Fischer, A. M. in Annual Plant Reviews Volume 26: Senescence Processes in Plants (ed. Gan, S.) 87–107 (Blackwell, Oxford, 2007).
Sinsabaugh, R. L. & Shah, J. J. F. Ecoenzymatic stoichiometry and ecological theory. Annu. Rev. Ecol. Evol. Syst. 43, 313–343 (2012).
Lim, P. O., Kim, H. J. & Nam, H. G. Leaf senescence. Annu. Rev. Plant. Biol. 58, 115–136 (2007).
Parton, W. et al. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315, 361–364 (2007).
Fridley, J. D. Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485, 359–362 (2012).
Díaz, C. et al. Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol. 147, 1437–1449 (2008).
Estiarte, M. & Peñuelas, J. Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob. Change Biol. 21, 1005–1017 (2015).
Yuan, Z. Y. & Chen, H. Y. H. Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Glob. Ecol. Biogeogr. 18, 11–18 (2009).
Vergutz, L., Manzoni, S., Porporato, A., Novais, R. F. & Jackson, R. B. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol. Monogr. 82, 205–220 (2012).
Reed, S. C., Townsend, A. R., Davidson, E. A. & Cleveland, C. C. Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol. 196, 173–180 (2012).
Hedin, L. O., Brookshire, E. N. J., Menge, D. N. L. & Barron, A. R. The nitrogen paradox in tropical forest ecosystems. Annu. Rev. Ecol. Evol. Syst. 40, 613–635 (2009).
Reed, S. C., Cleveland, C. C. & Townsend, A. R. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu. Rev. Ecol. Evol. Syst. 42, 489–512 (2011).
Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).
Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ. Press, Princeton, 2002).
Zhou, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Change 2, 106–110 (2012).
Hobbie, S. E. Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends. Ecol. Evol. 30, 357–363 (2015).
van der Heijden, M. G. A., Bardgett, R. D. & van Straalen, N. M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008).
Cornwell, W. K. et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065–1071 (2008).
Zhang, D., Hui, D., Luo, Y. & Zhou, G. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J. Plant Ecol. 1, 85–93 (2008).
García-Palacios, P., Maestre, F. T., Kattge, J. & Wall, D. H. Climate and litter quality differently modulate the effects of soil fauna on litter decomposition across biomes. Ecol. Lett. 16, 1045–1053 (2013).
Fife, D. N., Nambiar, E. K. S. & Saur, E. Retranslocation of foliar nutrients in evergreen tree species planted in a Mediterranean environment. Tree Physiol. 28, 187–196 (2008).
Brookshire, E. N. J., Gerber, S., Menge, D. N. L. & Hedin, L. O. Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecol. Lett. 15, 9–16 (2012).
Gill, A. L., Finzi, A. C. & Penuelas, J. Belowground carbon flux links biogeochemical cycles and resource-use efficiency at the global scale. Ecol. Lett. 19, 1419–1428 (2016).
Soper, F. M. et al. Modest gaseous nitrogen losses point to conservative nitrogen cycling in a lowland tropical forest watershed. Ecosystems 21, 901–912 (2018).
Austin, A. T. Has water limited our imagination for aridland biogeochemistry?. Trends Ecol. Evol. 26, 229–235 (2011).
Wang, J., Liu, L., Wang, X. & Chen, Y. The interaction between abiotic photodegradation and microbial decomposition under ultraviolet radiation. Glob. Change Biol. 21, 2095–2104 (2015).
Van der Putten, W. H. Climate change, aboveground-belowground interactions, and species’ range shifts. Annu. Rev. Ecol. Evol. Syst. 43, 365–383 (2012).
Elser, J. J., Fagan, W. F., Kerkhoff, A. J., Swenson, N. G. & Enquist, B. J. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol. 186, 593–608 (2010).
Reich, P. B. & Oleksyn, J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc. Natl Acad. Sci. USA 101, 11001–11006 (2004).
Lovelock, C. E., Feller, I. C., Ball, M. C., Ellis, J. & Sorrell, B. Testing the growth rate vs. geochemical hypothesis for latitudinal variation in plant nutrients. Ecol. Lett. 10, 1154–1163 (2007).
Yu, Q. et al. Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol. Lett. 13, 1390–1399 (2010).
Peñuelas, J. et al. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nat. Commun. 4, 2934 (2013).
Deng, M. et al. Increased phosphate uptake but not resorption alleviates phosphorus deficiency induced by nitrogen deposition in temperate Larix principis-rupprechtii plantations. New Phytol. 212, 1019–1029 (2016).
Fierer, N., Strickland, M. S., Liptzin, D., Bradford, M. A. & Cleveland, C. C. Global patterns in belowground communities. Ecol. Lett. 12, 1238–1249 (2009).
Waring, B. G., Averill, C. & Hawkes, C. V. Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecol. Lett. 16, 887–894 (2013).
Vitousek, P. M. & Farrington, H. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37, 63–75 (1997).
Güesewell, S. & Gessner, M. O. N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct. Ecol. 23, 211–219 (2009).
Schneider, T. et al. Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J. 6, 1749–1762 (2012).
Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. Proc. Natl Acad. Sci. USA 111, 6341–6346 (2014).
Kaiser, C., Franklin, O., Dieckmann, U. & Richter, A. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol. Lett. 17, 680–690 (2014).
Zechmeister-Boltenstern, S. et al. The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol. Monogr. 85, 133–155 (2015).
Gallinat, A. S., Primack, R. B. & Wagner, D. L. Autumn, the neglected season in climate change research. Trends. Ecol. Evol. 30, 169–176 (2015).
Diaz, C. et al. Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol. 147, 1437–1449 (2008).
Campbell, E. E. et al. Using litter chemistry controls on microbial processes to partition litter carbon fluxes with the Litter Decomposition and Leaching (LIDEL) model. Soil Biol. Biochem. 100, 160–174 (2016).
Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).
Bååth, E. & Anderson, T. H. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol. Biochem. 35, 955–963 (2003).
Kaiser, C., Frank, A., Wild, B., Koranda, M. & Richter, A. Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biol. Biochem. 42, 1650–1652 (2010).
Kampichler, C. & Bruckner, A. The role of microarthropods in terrestrial decomposition: a meta-analysis of 40 years of litterbag studies. Biol. Rev. 84, 375–389 (2009).
Wieder, W. R., Bonan, G. B. & Allison, S. D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change 3, 909–912 (2013).
Allison, S. D. & Vitousek, P. M. Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141, 612–619 (2004).
Cárdenas, I. & Campo, J. Foliar nitrogen and phosphorus resorption and decomposition in the nitrogen-fixing tree Lysiloma microphyllum in primary and secondary seasonally tropical dry forests in Mexico. J. Trop. Ecol. 23, 107–113 (2007).
Das, C. & Mondal, N. K. Litterfall, decomposition and nutrient release of Shorea robusta and Tectona grandis in a sub-tropical forest of West Bengal, eastern India. J. For. Res. 27, 1055–1065 (2016).
Demessie, A., Singh, B. R., Lal, R. & Strand, L. T. Leaf litter fall and litter decomposition under Eucalyptus and coniferous plantations in Gambo District, southern Ethiopia. Acta Agric. Scand. B Soil Plant Sci. 62, 467–476 (2012).
Feller, I. C., Whigham, D. F., O’Neill, J. P. & McKee, K. L. Effects of nutrient enrichment on within-stand cycling in a mangrove forest. Ecology 80, 2193–2205 (1999).
Feller, I. C., McKee, K. L., Whigham, D. F. & O’Neill, J. P. Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62, 145–175 (2003).
Finzi, A. C., Allen, A. S., DeLucia, E. H., Ellsworth, D. S. & Schlesinger, W. H. Forest litter production, chemistry, and decomposition following two years of free-air CO2 enrichment. Ecology 82, 470–484 (2001).
Fioretto, A., Papa, S. & Fuggi, A. Litter-fall and litter decomposition in a low Mediterranean shrubland. Biol. Fert. Soils 39, 37–44 (2003).
Fonte, S. J. & Schowalter, T. D. Decomposition of greenfall vs. senescent foliage in a tropical forest ecosystem in Puerto Rico. Biotropica 36, 474–482 (2004).
Forey, E., Trap, J. & Aubert, M. Liming impacts Fagus sylvatica leaf traits and litter decomposition 25 years after amendment. For. Ecol. Manage. 353, 67–76 (2015).
Fornara, D. A. & Du Toit, J. T. Browsing-induced effects on leaf litter quality and decomposition in a southern African savanna. Ecosystems 11, 238–249 (2008).
Funk, J. L. Hedychium gardnerianum invasion into Hawaiian montane rainforest: interactions among litter quality, decomposition rate, and soil nitrogen availability. Biogeochemistry 76, 441–451 (2005).
Girisha, G. K., Condron, L. M., Clinton, P. W. & Davis, M. R. Decomposition and nutrient dynamics of green and freshly fallen radiata pine (Pinus radiata) needles. For. Ecol. Manage. 179, 169–181 (2003).
Hobbie, S. E. et al. Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment. Ecol. Monogr. 82, 389–405 (2012).
Huang, J. J., Wang, X. H. & Yan, E. R. Leaf nutrient concentration, nutrient resorption and litter decomposition in an evergreen broad-leaved forest in eastern China. For. Ecol. Manage. 239, 150–158 (2007).
Kasurinen, A., Riikonen, J., Oksanen, E., Vapaavuori, E. & Holopainen, T. Chemical composition and decomposition of silver birch leaf litter produced under elevated CO2 and O3. Plant Soil 282, 261–280 (2006).
Kiser, L. C., Fox, T. R. & Carlson, C. A. Foliage and litter chemistry, decomposition, and nutrient release in Pinus taeda. Forests 4, 595–612 (2013).
Kitayama, K., Aiba, S. I., Takyu, M., Majalap, N. & Wagai, R. Soil phosphorus fractionation and phosphorus-use efficiency of a Bornean tropical montane rain forest during soil aging with podozolization. Ecosystems 7, 259–274 (2004).
Kozovits, A. R. et al. Nutrient resorption and patterns of litter production and decomposition in a Neotropical savanna. Funct. Ecol. 21, 1034–1043 (2007).
Pandey, R. R., Sharma, G., Tripathi, S. K. & Singh, A. K. Litterfall, litter decomposition and nutrient dynamics in a subtropical natural oak forest and managed plantation in northeastern India. For. Ecol. Manage. 240, 96–104 (2007).
Quested, H. M. et al. Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecology 84, 3209–3221 (2003).
Santiago, L.S. Leaf Traits of Canopy Trees on a Precipitation Gradient in Panama: Integrating Plant Physiological Ecology and Ecosystem Science. PhD thesis, Univ. Florida (2003).
Schlesinger, W. H. & Hasey, M. M. Decomposition of chaparral shrub foliage-losses of organic and inorganic constituents from deciduous and evergreen leaves. Ecology 62, 762–774 (1981).
Schmidt, M., Veldkamp, E. & Corre, M. D. Tree-microbial biomass competition for nutrients in a temperate deciduous forest, central Germany. Plant Soil 408, 227–242 (2016).
Smith, K., Gholz, H. L. & Oliveira, F. D. Litterfall and nitrogen-use efficiency of plantations and primary forest in the eastern Brazilian Amazon.For. Ecol. Manage 109, 209–220 (1998).
Soudzilovskaia, N. A., Onipchenko, V. G., Cornelissen, J. H. C. & Aerts, R. Effects of fertilisation and irrigation on ‘foliar afterlife’ in alpine tundra. J. Veg. Sci 18, 755–766 (2007).
Steltzer, H. & Bowman, W. D. Litter N retention over winter for a low and a high phenolic species in the alpine tundra. Plant Soil 275, 361–370 (2005).
Uselman, S. M., Snyder, K. A. & Blank, R. R. Insect biological control accelerates leaf litter decomposition and alters short-term nutrient dynamics in a Tamarix-invaded riparian ecosystem. Oikos 120, 409–417 (2011).
Vitousek, P. M. Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1, 401–407 (1998).
Wang, J., You, Y. M., Tang, Z. X., Sun, X. L. & Sun, O. J. A comparison of decomposition dynamics among green tree leaves, partially decomposed tree leaf litter and their mixture in a warm temperate forest ecosystem. J. For. Res. 27, 1037–1045 (2016).
Weerakkody, J. & Parkinson, D. Leaf litter decomposition in an upper montane rainforest in Sri Lanka. Pedobiologia 50, 387–395 (2006).
Yang, Q. P. et al. Effects of freeze damage on litter production, quality and decomposition in a loblolly pine forest in central China. Plant Soil 374, 449–458 (2014).
Aerts, R. & Decaluwe, H. Above-ground productivity and nutrient turnover of Molinia caerulea along and experimental gradient of nutrient availability. Oikos 54, 320–324 (1989).
Van vuuren, M. M. I., Berendse, F. & Devisser, W. Species and site differences in the decomposition of litter and roots from wet heathlands. Can. J. Bot. 71, 167–173 (1993).
Billings, S. A. et al. Effects of elevated carbon dioxide on green leaf tissue and leaf litter quality in an intact Mojave Desert ecosystem. Glob. Change Biol. 9, 729–735 (2003).
Weatherly, H. E., Zitzer, S. F., Coleman, J. S. & Arnone, J. A. In situ litter decomposition and litter quality in a Mojave Desert ecosystem: effects of elevated atmospheric CO2 and interannual climate variability. Glob. Change Biol. 9, 1223–1233 (2003).
Blanco, J. A., Imbert, J. B. & Castillo, F. J. Thinning affects nutrient resorption and nutrient-use efficiency in two Pinus sylvestris stands in the Pyrenees. Ecol. Appl. 19, 682–698 (2009).
Blanco, J. A., Bosco Imbert, J. & Castillo, F. J. Thinning affects Pinus sylvestris needle decomposition rates and chemistry differently depending on site conditions. Biogeochemistry 106, 397–414 (2011).
Bowman, W. D., Theodose, T. A. & Fisk, M. C. Physiological and production responses of plant-growth forms to increases in limiting resources in alpine tundra: implications for differential community response to environmental change. Oecologia 101, 217–227 (1995).
O’Lear, H. A. & Seastedt, T. R. Landscape patterns of litter decomposition in alpine tundra. Oecologia 99, 95–101 (1994).
Cheng, X.-B. et al. Nutrient dynamics in Quercus mongolica leaves at different canopy positions. Ying Yong Sheng Tai Xue Bao 22, 2272–2278 (2011).
Zheng, J. Q., Han, S. J., Wang, Y., Zhang, C. G. & Li, M. H. Composition and function of microbial communities during the early decomposition stages of foliar litter exposed to elevated CO2 concentrations. Eur. J. Soil Sci. 61, 914–925 (2010).
Chuyong, G. B., Newbery, D. M. & Songwe, N. C. Litter nutrients and retranslocation in a central African rain forest dominated by ectomycorrhizal trees. New Phytol. 148, 493–510 (2000).
Chuyong, G. B., Newbery, D. M. & Songwe, N. C. Litter breakdown and mineralization in a central African rain forest dominated by ectomycorrhizal trees. Biogeochemistry 61, 73–94 (2002).
Distel, R. A., Moretto, A. S. & Didone, N. G. Nutrient resorption from senescing leaves in two Stipa species native to central Argentina. Austral Ecol. 28, 210–215 (2003).
Moretto, A. S. & Distel, R. A. Decomposition of and nutrient dynamics in leaf litter and roots of Poa ligularis and Stipa gyneriodes. J. Arid Environ. 55, 503–514 (2003).
Freschet, G. T., Cornelissen, J. H., van Logtestijn, R. S. & Aerts, R. Substantial nutrient resorption from leaves, stems and roots in a subarctic flora: what is the link with other resource economics traits? New Phytol. 186, 879–889 (2010).
Freschet, G. T., Aerts, R. & Cornelissen, J. H. C. Multiple mechanisms for trait effects on litter decomposition: moving beyond home-field advantage with a new hypothesis. J. Ecol. 100, 619–630 (2012).
Hobbie, S. E. & Gough, L. Foliar and soil nutrients in tundra on glacial landscapes of contrasting ages in northern Alaska. Oecologia 131, 453–462 (2002).
Hobbie, S. E. & Gough, L. Litter decomposition in moist acidic and non-acidic tundra with different glacial histories. Oecologia 140, 113–124 (2004).
Huang, J. Y. et al. Nutrient resorption based on different estimations of five perennial herbaceous species from the grassland in inner Mongolia, China. J. Arid Environ. 76, 1–8 (2012).
Liu, P., Huang, J., Sun, O. J. & Han, X. Litter decomposition and nutrient release as affected by soil nitrogen availability and litter quality in a semiarid grassland ecosystem. Oecologia 162, 771–780 (2010).
Jiang, C. et al. Nutrient resorption of coexistence species in alpine meadow of the Qinghai-Tibetan Plateau explains plant adaptation to nutrient-poor environment. Ecol. Eng. 44, 1–9 (2012).
Duan, J. et al. Non-additive effect of species diversity and temperature sensitivity of mixed litter decomposition in the alpine meadow on Tibetan Plateau. Soil Biol. Biochem. 57, 841–847 (2013).
Keenan, R. J., Prescott, C. E. & Kimmins, J. P. H. Litter production and nutrient resorption in western red cedar and western hemlock forests on northern Vancouver Island, British Columbia. Can. J. For. Res. 25, 1850–1857 (1995).
Keenan, R. J., Prescott, C. E., Kimmins, J. P., Pastor, J. & Dewey, B. Litter decomposition in western red cedar and western hemlock forests on northern Vancouver Island, British Columbia. Can. J. Bot. 74, 1626–1634 (1996).
Killingbeck, K. T. & Whitford, W. G. High foliar nitrogen in desert shrubs: an important ecosystem trait or defective desert doctrine?. Ecology 77, 1728–1737 (1996).
Kemp, P. R., Reynolds, J. F., Virginia, R. A. & Whitford, W. G. Decomposition of leaf and root litter of Chihuahuan desert shrubs: effects of three years of summer drought. J. Arid Environ. 53, 21–39 (2003).
Kumar, B. M., George, S. J., Jamaludheen, V. & Suresh, T. K. Comparison of biomass production, tree allometry and nutrient use efficiency of multipurpose trees grown in woodlot and silvopastoral experiments in Kerala, India. For. Ecol. Manage. 112, 145–163 (1998).
Jamaludheen, V. & Kumar, B. M. Litter of multipurpose trees in Kerala, India: variations in the amount, quality, decay rates and release of nutrients. For. Ecol. Manage. 115, 1–11 (1999).
Lagerström, A., Nilsson, M.-C. & Wardle, D. A. Decoupled responses of tree and shrub leaf and litter trait values to ecosystem retrogression across an island area gradient. Plant Soil 367, 183–197 (2013).
Dearden, F. M., Dehlin, H., Wardle, D. A. & Nilsson, M.-C. Changes in the ratio of twig to foliage in litterfall with species composition, and consequences for decomposition across a long term chronosequence. Oikos 115, 453–462 (2006).
Li, X., Zheng, X., Han, S., Zheng, J. & Li, T. Effects of nitrogen additions on nitrogen resorption and use efficiencies and foliar litterfall of six tree species in a mixed birch and poplar forest, northeastern China. Can. J. For. Res. 40, 2256–2261 (2010).
Li, X., Han, S. & Zhang, Y. Foliar decomposition in a broadleaf-mixed Korean pine (Pinus koraiensis Sieb. Et Zucc) plantation forest: the impact of initial litter quality and the decomposition of three kinds of organic matter fraction on mass loss and nutrient release rates. Plant Soil 295, 151–167 (2007).
Lindroth, R. L. et al. Consequences of elevated carbons dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environ. Pollut. 115, 395–404 (2001).
Parsons, W. F. J., Bockheim, J. G. & Lindroth, R. L. Independent, interactive, and species-specific responses of leaf litter decomposition to elevated CO2 and O3 in a northern hardwood forest. Ecosystems 11, 505–519 (2008).
Lindsay, E. A. & French, K. Litterfall and nitrogen cycling following invasion by Chrysanthemoides monilifera ssp. rotundata in coastal Australia. J. Appl. Ecol. 42, 556–566 (2005).
Lindsay, E. A. & French, K. Chrysanthemoides monilifera ssp. rotundata invasion alters decomposition rates in coastal areas of south-eastern Australia. For. Ecol. Manage. 198, 387–399 (2004).
Magill, A. H. et al. Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecol. Appl. 7, 402–415 (1997).
Magill, A. H. & Aber, J. D. Long-term effects of experimental nitrogen additions on foliar litter decay and humus formation in forest ecosystems. Plant Soil 203, 301–311 (1998).
Martínez-Sánchez, J. L. Nitrogen and phosphorus resorption in trees of a neotropical rain forest. J. Trop. Ecol. 19, 465–468 (2003).
Alvarez-Sánchez, J. & Enríquez, R. B. Leaf decomposition in a Mexican tropical rain forest. Biotropica 28, 657–667 (1996).
Mo, J., Zhang, D., Huang, Z., Yu, Q. & Kong, G. Distribution pattern of nutrient elements in plants of Dinghushan lower subtropical evergreen broad-leaved forest. J. Trop. Subtrop. Bot. 8, 198–206 (2000).
Li, Z., Wang, B., Wong, H., Tu, M. & Yao, W. Nutrient dynamics of litterfall in lower subtropical monsoon evergreen broad-leaved forest of Dinghushan. J. Trop. Subtrop. Bot. 6, 209–215 (1998).
Mo, J., Brown, S., Xue, J., Fang, Y. & Li, Z. Response of litter decomposition to simulated N deposition in disturbed, rehabilitated and mature forests in subtropical China. Plant Soil 282, 135–151 (2006).
Liang, G. et al. Response of leaf litter decomposition of two dominant trees to simulated acid rain in southern China. Acta Ecol. Sin. 34, 5728–5735 (2014).
Norris, M. D. & Reich, P. B. Modest enhancement of nitrogen conservation via retranslocation in response to gradients in N supply and leaf N status. Plant Soil 316, 193–204 (2009).
Norris, M. D., Avis, P. G., Reich, P. B. & Hobbie, S. E. Positive feedbacks between decomposition and soil nitrogen availability along fertility gradients. Plant Soil 367, 347–361 (2013).
Owensby, C. E., Coyne, P. I. & Auen, L. M. Nitrogen and phosphorus dynamics of a tallgrass prairie ecosystem exposed to elevated carbon dioxide. Plant Cell Environ. 16, 843–850 (1993).
Kemp, P. R., Waldecker, D. G., Owensby, C. E., Reynolds, J. F. & Virginia, R. A. Effects of elevated CO2 and nitrogen fertilization pretreatments on decomposition on tallgrass prairie leaf litter. Plant Soil 165, 115–127 (1994).
Quested, H. M., Press, M. C., Callaghan, T. V. & Cornelissen, J. H. C. The hemiparasitic angiosperm Bartsia alpina has the potential to accelerate decomposition in sub-arctic communities. Oecologia 130, 88–95 (2002).
Quested, H. M., Callaghan, T. V., Cornelissen, J. H. C. & Press, M. C. The impact of hemiparasitic plant litter on decomposition: direct, seasonal and litter mixing effects. J. Ecol. 93, 87–98 (2005).
Sariyildiz, T. & Anderson, J. M. Variation in the chemical composition of green leaves and leaf litters from three deciduous tree species growing on different soil types. For. Ecol. Manage. 210, 303–319 (2005).
Sariyildiz, T. & Anderson, J. M. Interactions between litter quality, decomposition and soil fertility: a laboratory study. Soil Biol. Biochem. 35, 391–399 (2003).
See, C. R. et al. Soil nitrogen affects phosphorus recycling: foliar resorption and plant–soil feedbacks in a northern hardwood forest. Ecology 96, 2488–2498 (2015).
Lovett, G. M., Arthur, M. A. & Crowley, K. F. Effects of calcium on the rate and extent of litter decomposition in a northern hardwood forest. Ecosystems 19, 87–97 (2015).
Yan, E., Wang, X., Guo, M., Zhong, Q. & Zhou, W. C:N:P stoichiometry across evergreen broad-leaved forests, evergreen coniferous forests and deciduous broad-leaved forests in the Tiantong region, Zhejiang Province, eastern China. Chin. J. Plant Ecol. 34, 48–57 (2010).
Wang, X., Huang, J. & Yan, E. Leaf litter decomposition of commen trees in Tiantong. Acta Phytoecol. Sin. 28, 457–467 (2004).
Austin, A. T. & Vitousek, P. M. Nutrient dynamics on a precipitation gradient in Hawai’i. Oecologia 113, 519–529 (1998).
Austin, A. T. & Vitousek, P. M. Precipitation, decomposition and litter decomposability of Metrosideros polymorpha in native forests on Hawai’i. J. Ecol. 88, 129–138 (2000).
Xu, X. N., Hirata, E. & Shibata, H. Effect of typhoon disturbance on fine litterfall and related nutrient input in a subtropical forest on Okinawa Island, Japan. Basic Appl. Ecol. 5, 271–282 (2004).
Xu, X. N. & Hirata, E. J. Decomposition patterns of leaf litter of seven common canopy species in a subtropical forest: N and P dynamics. Plant Soil 273, 279–289 (2005).
Diehl, P. et al. Nutrient conservation strategies in native Andean-Patagonian forests. J. Veg. Sci. 14, 63–70 (2003).
Vivanco, L. & Austin, A. T. Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J. Ecol. 96, 727–736 (2008).
Lee, D. W., O’Keefe, J., Holbrook, N. M. & Feild, T. S. Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecol. Res. 18, 677–694 (2003).
Boerner, R. E. J. & Rebbeck, J. Decomposition and nitrogen release from leaves of three hardwood species grown under elevated O3 and/or CO2. Plant Soil 170, 147–157 (1995).
Zhao, Q., Liu, X., Hu, Y. & Zeng, D. Effects of nitrogen addition on nutrient allocation and nutrient resorption efficiency in Larix gmelinii. Sci. Silvae Sin. 46, 14–19 (2010).
Zhang, D., Mao, Z., Zhu, S. & Zhou, B. Litter falls of 6 major forest stands in Maoershan Mountain of Heilongjiang Province. Bull. Bot. Res. 28, 104–108 (2008).
Sun, S. & Chen, L. Leaf nutrient dynamics and resorption efficiency of Quercus liaotungensis in the Donglingshan Mountain region. Acta Phytoecol. Sin. 25, 76–82 (2001).
Wang, J. & Huang, J. Comparison of major nutrient release patterns in leaf litter decomposition in warm temperate zone of China. Acta Phytoecol. Sin. 25, 375–380 (2001).
Bach, L. H., Frostegård, A. & Ohlson, M. Variation in soil microbial communities across a boreal spruce forest landscape. Can. J. For. Res. 38, 1504–1516 (2008).
Bardgett, R. D. & McAlister, E. The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol. Fert. Soils 29, 282–290 (1999).
Bardgett, R. D. & Walker, L. R. Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biol. Biochem. 36, 555–559 (2004).
Bardgett, R. D., Lovell, R. D., Hobbs, P. J. & Jarvis, S. C. Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol. Biochem. 31, 1021–1030 (1999).
Bi, J., Zhang, N., Liang, Y., Yang, H. & Ma, K. Interactive effects of water and nitrogen addition on soil microbial communities in a semiarid steppe. J. Plant Ecol. 5, 320–329 (2012).
Birgander, J., Rousk, J. & Olsson, P. A. Comparison of fertility and seasonal effects on grassland microbial communities. Soil Biol. Biochem. 76, 80–89 (2014).
Boot, C. M., Hall, E. K., Denef, K. & Baron, J. S. Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem. Soil Biol. Biochem. 92, 211–220 (2016).
Boyle, S. A., Yarwood, R. R., Bottomley, P. J. & Myrold, D. D. Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biol. Biochem. 40, 443–451 (2008).
Carrasco, L. et al. Estimation by PLFA of microbial community structure associated with the rhizosphere of Lygeum spartum and Piptatherum miliaceum growing in semiarid mine tailings. Microb. Ecol. 60, 265–271 (2010).
Chang, E. H. & Chiu, C. Y. Changes in soil microbial community structure and activity in a cedar plantation invaded by moso bamboo. Appl. Soil Ecol. 91, 1–7 (2015).
Chang, E. H., Chen, T. H., Tian, G. l., Hsu, C. K. & Chiu, C.Y. Effect of 40 and 80 years of conifer regrowth on soil microbial activities and community structure in subtropical low mountain forests. Forests 7, 244 (2016).
Chen, F. et al. Changes in soil microbial community structure and metabolic activity following conversion from native Pinus massoniana plantations to exotic Eucalyptus plantations. For. Ecol. Manage. 291, 65–72 (2013).
Deng, Q. et al. Soil microbial community and its interaction with soil carbon and nitrogen dynamics following afforestation in central China. Sci. Total Environ. 541, 230–237 (2016).
Djukic, I., Zehetner, F., Mentler, A. & Gerzabek, M. H. Microbial community composition and activity in different alpine vegetation zones. Soil Biol. Biochem. 42, 155–161 (2010).
Ebersberger, D., Werrnbter, N., Niklaus, P. A. & Kandeler, E. Effects of long term CO2 enrichment on microbial community structure in calcareous grassland. Plant Soil 264, 313–323 (2004).
Eskelinen, A., Stark, S. & Männistö, M. Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia 161, 113–123 (2009).
Fang, X. et al. Forest-type shift and subsequent intensive management affected soil organic carbon and microbial community in southeastern China. Eur. J. For. Res. 136, 689–697 (2017).
Fanin, N., Häettenschwiler, S. & Fromin, N. Litter fingerprint on microbial biomass, activity, and community structure in the underlying soil. Plant Soil 379, 79–91 (2014).
Feng, X., Simpson, A. J., Schlesinger, W. H. & Simpson, M. J. Altered microbial community structure and organic matter composition under elevated CO2 and N fertilization in the duke forest. Glob. Change Biol 16, 2104–2116 (2010).
Ford, H., Rousk, J., Garbutt, A., Jones, L. & Jones, D. L. Grazing effects on microbial community composition, growth and nutrient cycling in salt marsh and sand dune grasslands. Biol. Fert. Soils 49, 89–98 (2013).
Frey, S. D., Drijber, R., Smith, H. & Melillo, J. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol. Biochem. 40, 2904–2907 (2008).
Frostegård, A. & Bååth, E. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol. Fert. Soils 22, 59–65 (1996).
Fritze, H., Pietikainen, J. & Pennanen, T. Distribution of microbial biomass and phospholipid fatty acids in Podzol profiles under coniferous forest. Eur. J. Soil Sci. 51, 565–573 (2000).
Gavazov, K., Mills, R., Spiegelberger, T., Lenglet, J. & Buttler, A. Biotic and abiotic constraints on the decomposition of Fagus sylvatica leaf litter along an altitudinal gradient in contrasting land-use types. Ecosystems 17, 1326–1337 (2014).
Gordon, H., Haygarth, P. M. & Bardgett, R. D. Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biol. Biochem. 40, 302–311 (2008).
Guenet, B. et al. The impact of long-term CO2 enrichment and moisture levels on soil microbial community structure and enzyme activities. Geoderma 170, 331–336 (2012).
Hopkins, F. M. et al. Increased belowground carbon inputs and warming promote loss of soil organic carbon through complementary microbial responses. Soil Biol. Biochem. 76, 57–69 (2014).
Huang, G., Cao, Y. F., Wang, B. & Li, Y. Effects of nitrogen addition on soil microbes and their implications for soil C emission in the Gurbantunggut Desert, center of the Eurasian continent. Sci. Total Environ. 515, 215–224 (2015).
Huang, G., Li, Y. & Su, Y. G. Divergent responses of soil microbial communities to water and nitrogen addition in a temperate desert. Geoderma 251, 55–64 (2015).
Huang, Z. et al. Soil microbial biomass, community composition and soil nitrogen cycling in relation to tree species in subtropical China. Soil Biol. Biochem. 62, 68–75 (2013).
Jin, V. L. & Evans, R. D. Microbial 13C utilization patterns via stable isotope probing of phospholipid biomarkers in Mojave Desert soils exposed to ambient and elevated atmospheric CO2. Glob. Change Biol 16, 2334–2344 (2010).
Kanerva, T., Palojärvi, A., Rämö, K. & Manninen, S. Changes in soil microbial community structure under elevated tropospheric O3 and CO2. Soil Biol. Biochem. 40, 2502–2510 (2008).
Korkama, T., Fritze, H., Kiikkilä, O. & Pennanen, T. Do same-aged but different height Norway spruce (Picea abies) clones affect soil microbial community? Soil Biol. Biochem. 39, 2420–2423 (2007).
Kulmatiski, A. Changing soils to manage plant communities: activated carbon as a restoration tool in ex-arable fields. Restor. Ecol. 19, 102–110 (2011).
Lange, M. et al. Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoS ONE 9, e96182 (2014).
Lemanski, K. & Scheu, S. Incorporation of 13C labelled glucose into soil microorganisms of grassland: effects of fertilizer addition and plant functional group composition. Soil Biol. Biochem. 69, 38–45 (2014).
Lemanski, K. & Scheu, S. The influence of fertilizer addition, cutting frequency and herbicide application on soil organisms in grassland. Biol. Fert. Soils 51, 197–205 (2015).
Li, J. et al. Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol. Fert. Soils 51, 207–215 (2015).
Li, M. et al. Effects of flue gas desulfurization gypsum by-products on microbial biomass and community structure in alkaline-saline soils. J. Soils Sediments 12, 1040–1053 (2012).
Liu, Y., Li, X., Xing, Z., Zhao, X. & Pan, Y. Responses of soil microbial biomass and community composition to biological soil crusts in the revegetated areas of the Tengger Desert. Appl. Soil Ecol. 65, 52–59 (2013).
Long, X. E., Wang, J., Huang, Y. & Yao, H. Microbial community structures and metabolic profiles response differently to physiochemical properties between three landfill cover soils. Environ. Sci. Pollut. Res. Int. 23, 15483–15494 (2016).
Lucas-Borja, M. E. et al. Soil microbial community structure and activity in monospecific and mixed forest stands, under Mediterranean humid conditions. Plant Soil 354, 359–370 (2012).
Macdonald, L. M., Paterson, E., Dawson, L. A. & McDonald, A. J. S. Defoliation and fertiliser influences on the soil microbial community associated with two contrasting Lolium perenne cullivars. Soil Biol. Biochem. 38, 674–682 (2006).
Marhan, S., Kandeler, E. & Scheu, S. Phospholipid fatty acid profiles and xylanase activity in particle size fractions of forest soil and casts of Lumbricus terrestris L. (Oligochaeta, Lumbricidae). Appl. Soil Ecol. 35, 412–422 (2007).
Mitchell, R. J., Campbell, C. D., Chapman, S. J. & Cameron, C. M. The ecological engineering impact of a single tree species on the soil microbial community. J. Ecol. 98, 50–61 (2010).
Montecchia, M. S. et al. Multivariate approach to characterizing soil microbial communities in pristine and agricultural sites in northwest Argentina. Appl. Soil Ecol. 47, 176–183 (2011).
Moore-Kucera, J. & Dick, R. P. PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb. Ecol. 55, 500–511 (2008).
Mutabaruka, R., Hairiah, K. & Cadisch, G. Microbial degradation of hydrolysable and condensed tannin polyphenol-protein complexes in soils from different land-use histories. Soil Biol. Biochem. 39, 1479–1492 (2007).
Nkongolo, K. K. et al. Assessing biological impacts of land reclamation in a mining region in canada: effects of dolomitic lime applications on forest ecosystems and microbial phospholipid fatty acid signatures. Water Air Soil Pollut. 227, 104 (2016).
Nottingham, A. T., Turner, B. L., Chamberlain, P. M., Stott, A. W. & Tanner, E. V. J. Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry 111, 219–237 (2012).
Ohtonen, R., Fritze, H., Pennanen, T., Jumpponen, A. & Trappe, J. Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119, 239–246 (1999).
Papatheodorou, E. M. et al. Differential responses of structural and functional aspects of soil microbes and nematodes to abiotic and biotic modifications of the soil environment. Appl. Soil Ecol. 61, 26–33 (2012).
Paz-Ferreiro, J., Liang, C., Fu, S., Mendez, A. & Gasco, G. The Effect of biochar and its interaction with the earthworm Pontoscolex corethrurus on soil microbial community structure in tropical soils. PLoS ONE 10, e0124891(2015).
Potthast, K., Hamer, U. & Makeschin, F. Land-use change in a tropical mountain rainforest region of southern Ecuador affects soil microorganisms and nutrient cycling. Biogeochemistry 111, 151–167 (2012).
Rinnan, R., Michelsen, A., Bååth, E. & Jonasson, S. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob. Change Biol. 13, 28–39 (2007).
Rousk, J., Brookes, P. C. & Bååth, E. Fungal and bacterial growth responses to N fertilization and pH in the 150-year ‘Park Grass’ UK grassland experiment. FEMS Microbiol. Ecol. 76, 89–99 (2011).
Rousk, J., Smith, A. R. & Jones, D. L. Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems. Glob. Change Biol. 19, 3872–3884 (2013).
Sun, Y. et al. Responses of soil microbial communities to prescribed burning in two paired vegetation sites in southern China. Ecol. Res. 26, 669–677 (2011).
Throckmorton, H. M., Bird, J. A., Dane, L., Firestone, M. K. & Horwath, W. R. The source of microbial C has little impact on soil organic matter stabilisation in forest ecosystems. Ecol. Lett. 15, 1257–1265 (2012).
Ushio, M., Balser, T. C. & Kitayama, K. Effects of condensed tannins in conifer leaves on the composition and activity of the soil microbial community in a tropical montane forest. Plant Soil 365, 157–170 (2013).
van Diepen, L. T. A., Lilleskov, E. A., Pregitzer, K. S. & Miller, R. M. Simulated nitrogen deposition causes a decline of intra- and extraradical abundance of arbuscular mycorrhizal fungi and changes in microbial community structure in northern hardwood forests. Ecosystems 13, 683–695 (2010).
Wang, F. et al. Species-dependent responses of soil microbial properties to fresh leaf inputs in a subtropical forest soil in South China. J. Plant Ecol. 7, 86–96 (2014).
Wang, H. et al. Soil microbial community composition rather than litter quality is linked with soil organic carbon chemical composition in plantations in subtropical China. J. Soils Sediments 15, 1094–1103 (2015).
Wang, M., Xue, J., Horswell, J., Kimberley, M. O. & Huang, Z. Long-term biosolids application alters the composition of soil microbial groups and nutrient status in a pine plantation. Biol. Fert. Soils 53, 799–809 (2017).
Wang, Q., Wang, S., He, T., Liu, L. & Wu, J. Response of organic carbon mineralization and microbial community to leaf litter and nutrient additions in subtropical forest soils. Soil Biol. Biochem. 71, 13–20 (2014).
Wardle, D. A. & Jonsson, M. Long-term resilience of above- and belowground ecosystem components among contrasting ecosystems. Ecology 95, 1836–1849 (2014).
Weber, P. & Bardgett, R. D. Influence of single trees on spatial and temporal patterns of belowground properties in native pine forest. Soil Biol. Biochem. 43, 1372–1378 (2011).
Whitaker, J. et al. Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient. J. Ecol. 102, 1058–1071 (2014).
Wu, L. et al. Assessment of shifts in microbial community structure and catabolic diversity in response to Rehmannia glutinosa monoculture. Appl. Soil Ecol. 67, 1–9 (2013).
Xing, S. H. et al. Genotype and slope position control on the availability of soil soluble organic nitrogen in tea plantations. Biogeochemistry 103, 245–261 (2011).
Xu, M. et al. Soil microbial community structure and activity along a montane elevational gradient on the Tibetan Plateau. Eur. J. Soil Biol. 64, 6–14 (2014).
Xu, Z. et al. The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of Changbai Mountain. Appl. Soil Ecol. 86, 19–29 (2015).
Yang, Q. et al. Structure and function of soil microbial community in artificially planted Sonneratia apetala and S. caseolaris forests at different stand ages in Shenzhen Bay, China. Mar. Pollut. Bull. 85, 754–763 (2014).
Yannikos, N. et al. Impact of Populus trees on the composition of organic matter and the soil microbial community in Orthic Gray Luvisols in Saskatchewan (Canada). Soil Biol. Biochem. 70, 5–11 (2014).
Yoshitake, S. et al. Successional changes in the soil microbial community along a vegetation development sequence in a subalpine volcanic desert on Mount Fuji, Japan. Plant Soil 364, 261–272 (2013).
Zhang, C. et al. Contrasting effects of ammonium and nitrate additions on the biomass of soil microbial communities and enzyme activities in subtropical China. Biogeosciences 14, 4815–4827 (2017).
Zhang, W. et al. Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob. Change Biol. 11, 266–277 (2011).
Zhao, J., Wang, X., Shao, Y., Xu, G. & Fu, S. Effects of vegetation removal on soil properties and decomposer organisms. Soil Biol. Biochem. 43, 954–960 (2011).
Zhou, Y., Clark, M., Su, J. & Xiao, C. Litter decomposition and soil microbial community composition in three Korean pine (Pinus koraiensis) forests along an altitudinal gradient. Plant Soil 386, 171–183 (2015).
Zornoza, R. et al. Changes in soil microbial community structure following the abandonment of agricultural terraces in mountainous areas of eastern Spain. Appl. Soil Ecol. 42, 315–323 (2009).
Grueber, C. E., Nakagawa, S., Laws, R. J. & Jamieson, I. G. Multimodel inference in ecology and evolution: challenges and solutions. J. Evol. Biol. 24, 699–711 (2011).
Burnham, K. P. & Anderson, D. R. Understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004)..
We thank B. Schmid for his advice on statistical analyses. This study was financially supported by the Chinese National Key Development Program for Basic Research (2017YFC0503902, 2014CB954003) and the National Natural Science Foundation of China (31522011, 31670478, and 31700420). L.J. was supported by US National Science Foundation, grant no. DEB-1342754.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Deng, M., Liu, L., Jiang, L. et al. Ecosystem scale trade-off in nitrogen acquisition pathways. Nat Ecol Evol 2, 1724–1734 (2018). https://doi.org/10.1038/s41559-018-0677-1
Floresta e Ambiente (2021)
Global Change Biology (2020)
Soil Biology and Biochemistry (2020)
Environmental Pollution (2020)
Herbivore Assemblage as an Important Factor Modulating Grazing Effects on Ecosystem Carbon Fluxes in a Meadow Steppe in Northeast China
Journal of Geophysical Research: Biogeosciences (2020)