Ecosystem scale trade-off in nitrogen acquisition pathways

Abstract

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Impact of climatic factors and NRE on litter Nmin.
Fig. 2: Correlation between litter Nmin and foliar nutrient traits.
Fig. 3: Distribution of soil F:B ratio and its relationship to NRE and Nmin.
Fig. 4: Schematic showing how the N cycle links aboveground N resorption and belowground N mineralization during litter decomposition in various ecosystems.

Data availability

The data supporting the findings of this study can be obtained in Supplementary Dataset 1 and Dataset 2.

References

  1. 1.

    Chapin, F. S., Matson, P. A. & Mooney, H. A. Principles of Terrestrial Ecosystem Ecology (Springer, New York, 2011).

  2. 2.

    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).

    Article  PubMed  Google Scholar 

  3. 3.

    Wardle, D. A. et al. Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633 (2004).

    Article  CAS  Google Scholar 

  4. 4.

    Thamdrup, B. New pathways and processes in the global nitrogen cycle. Annu. Rev. Ecol. Evol. Syst. 43, 407–428 (2012).

    Article  Google Scholar 

  5. 5.

    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).

    Article  Google Scholar 

  6. 6.

    Fischer, A. M. in Annual Plant Reviews Volume 26: Senescence Processes in Plants (ed. Gan, S.) 87–107 (Blackwell, Oxford, 2007).

  7. 7.

    Sinsabaugh, R. L. & Shah, J. J. F. Ecoenzymatic stoichiometry and ecological theory. Annu. Rev. Ecol. Evol. Syst. 43, 313–343 (2012).

    Article  Google Scholar 

  8. 8.

    Lim, P. O., Kim, H. J. & Nam, H. G. Leaf senescence. Annu. Rev. Plant. Biol. 58, 115–136 (2007).

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Parton, W. et al. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315, 361–364 (2007).

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Fridley, J. D. Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485, 359–362 (2012).

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    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).

    Article  Google Scholar 

  13. 13.

    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).

    Article  Google Scholar 

  14. 14.

    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).

    Article  Google Scholar 

  15. 15.

    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).

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    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).

    Article  Google Scholar 

  17. 17.

    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).

    Article  Google Scholar 

  18. 18.

    Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).

    Article  CAS  Google Scholar 

  19. 19.

    Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ. Press, Princeton, 2002).

  20. 20.

    Zhou, J. et al. Microbial mediation of carbon-cycle feedbacks to climate warming. Nat. Clim. Change 2, 106–110 (2012).

    Article  CAS  Google Scholar 

  21. 21.

    Hobbie, S. E. Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends. Ecol. Evol. 30, 357–363 (2015).

    Article  PubMed  Google Scholar 

  22. 22.

    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).

    Article  PubMed  Google Scholar 

  23. 23.

    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).

    Article  PubMed  Google Scholar 

  24. 24.

    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).

    Article  Google Scholar 

  25. 25.

    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).

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    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).

    Article  CAS  PubMed  Google Scholar 

  27. 27.

    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).

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    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).

    Article  PubMed  Google Scholar 

  29. 29.

    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).

    Article  CAS  Google Scholar 

  30. 30.

    Austin, A. T. Has water limited our imagination for aridland biogeochemistry?. Trends Ecol. Evol. 26, 229–235 (2011).

    Article  PubMed  Google Scholar 

  31. 31.

    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).

    Article  Google Scholar 

  32. 32.

    Van der Putten, W. H. Climate change, aboveground-belowground interactions, and species’ range shifts. Annu. Rev. Ecol. Evol. Syst. 43, 365–383 (2012).

    Article  Google Scholar 

  33. 33.

    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).

    Article  CAS  PubMed  Google Scholar 

  34. 34.

    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).

    Article  CAS  PubMed  Google Scholar 

  35. 35.

    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).

    Article  CAS  PubMed  Google Scholar 

  36. 36.

    Yu, Q. et al. Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol. Lett. 13, 1390–1399 (2010).

    Article  PubMed  Google Scholar 

  37. 37.

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

    Article  CAS  PubMed  Google Scholar 

  38. 38.

    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).

    Article  CAS  PubMed  Google Scholar 

  39. 39.

    Fierer, N., Strickland, M. S., Liptzin, D., Bradford, M. A. & Cleveland, C. C. Global patterns in belowground communities. Ecol. Lett. 12, 1238–1249 (2009).

    Article  PubMed  Google Scholar 

  40. 40.

    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).

    Article  PubMed  Google Scholar 

  41. 41.

    Vitousek, P. M. & Farrington, H. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37, 63–75 (1997).

    Article  CAS  Google Scholar 

  42. 42.

    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).

    Article  Google Scholar 

  43. 43.

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. Proc. Natl Acad. Sci. USA 111, 6341–6346 (2014).

    Article  CAS  Google Scholar 

  45. 45.

    Kaiser, C., Franklin, O., Dieckmann, U. & Richter, A. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol. Lett. 17, 680–690 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Zechmeister-Boltenstern, S. et al. The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol. Monogr. 85, 133–155 (2015).

    Article  Google Scholar 

  47. 47.

    Gallinat, A. S., Primack, R. B. & Wagner, D. L. Autumn, the neglected season in climate change research. Trends. Ecol. Evol. 30, 169–176 (2015).

    Article  PubMed  Google Scholar 

  48. 48.

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    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).

    Article  CAS  Google Scholar 

  50. 50.

    Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    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).

    Article  CAS  Google Scholar 

  52. 52.

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    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).

    Article  PubMed  Google Scholar 

  54. 54.

    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).

    Article  CAS  Google Scholar 

  55. 55.

    Allison, S. D. & Vitousek, P. M. Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 141, 612–619 (2004).

    Article  PubMed  Google Scholar 

  56. 56.

    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).

    Article  Google Scholar 

  57. 57.

    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).

    Article  CAS  Google Scholar 

  58. 58.

    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).

    Google Scholar 

  59. 59.

    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).

    Article  Google Scholar 

  60. 60.

    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).

    Article  CAS  Google Scholar 

  61. 61.

    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).

    Google Scholar 

  62. 62.

    Fioretto, A., Papa, S. & Fuggi, A. Litter-fall and litter decomposition in a low Mediterranean shrubland. Biol. Fert. Soils 39, 37–44 (2003).

    Article  CAS  Google Scholar 

  63. 63.

    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).

    Article  Google Scholar 

  64. 64.

    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).

    Article  Google Scholar 

  65. 65.

    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).

    Article  CAS  Google Scholar 

  66. 66.

    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).

    Article  Google Scholar 

  67. 67.

    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).

    Article  Google Scholar 

  68. 68.

    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).

    Article  Google Scholar 

  69. 69.

    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).

    Article  Google Scholar 

  70. 70.

    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).

    Article  CAS  Google Scholar 

  71. 71.

    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).

    Article  Google Scholar 

  72. 72.

    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).

    Article  CAS  Google Scholar 

  73. 73.

    Kozovits, A. R. et al. Nutrient resorption and patterns of litter production and decomposition in a Neotropical savanna. Funct. Ecol. 21, 1034–1043 (2007).

    Article  Google Scholar 

  74. 74.

    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).

    Article  Google Scholar 

  75. 75.

    Quested, H. M. et al. Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecology 84, 3209–3221 (2003).

    Article  Google Scholar 

  76. 76.

    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).

  77. 77.

    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).

    Article  CAS  Google Scholar 

  78. 78.

    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).

    Article  CAS  Google Scholar 

  79. 79.

    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).

    Article  Google Scholar 

  80. 80.

    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).

    Article  Google Scholar 

  81. 81.

    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).

    Article  CAS  Google Scholar 

  82. 82.

    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).

    Article  Google Scholar 

  83. 83.

    Vitousek, P. M. Foliar and litter nutrients, nutrient resorption, and decomposition in Hawaiian Metrosideros polymorpha. Ecosystems 1, 401–407 (1998).

    Article  CAS  Google Scholar 

  84. 84.

    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).

    Article  CAS  Google Scholar 

  85. 85.

    Weerakkody, J. & Parkinson, D. Leaf litter decomposition in an upper montane rainforest in Sri Lanka. Pedobiologia 50, 387–395 (2006).

    Article  CAS  Google Scholar 

  86. 86.

    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).

    Article  CAS  Google Scholar 

  87. 87.

    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).

    Article  Google Scholar 

  88. 88.

    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).

    Article  Google Scholar 

  89. 89.

    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).

    Article  Google Scholar 

  90. 90.

    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).

    Article  Google Scholar 

  91. 91.

    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).

    Article  PubMed  Google Scholar 

  92. 92.

    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).

    Article  CAS  Google Scholar 

  93. 93.

    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).

    Article  PubMed  Google Scholar 

  94. 94.

    O’Lear, H. A. & Seastedt, T. R. Landscape patterns of litter decomposition in alpine tundra. Oecologia 99, 95–101 (1994).

    Article  PubMed  Google Scholar 

  95. 95.

    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).

    CAS  PubMed  Google Scholar 

  96. 96.

    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).

    Article  Google Scholar 

  97. 97.

    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).

    Article  CAS  Google Scholar 

  98. 98.

    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).

    Article  CAS  Google Scholar 

  99. 99.

    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).

    Article  Google Scholar 

  100. 100.

    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).

    Article  Google Scholar 

  101. 101.

    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).

    Article  CAS  PubMed  Google Scholar 

  102. 102.

    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).

    Article  Google Scholar 

  103. 103.

    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).

    Article  PubMed  Google Scholar 

  104. 104.

    Hobbie, S. E. & Gough, L. Litter decomposition in moist acidic and non-acidic tundra with different glacial histories. Oecologia 140, 113–124 (2004).

    Article  PubMed  Google Scholar 

  105. 105.

    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).

    Article  CAS  Google Scholar 

  106. 106.

    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).

    Article  PubMed  Google Scholar 

  107. 107.

    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).

    Article  Google Scholar 

  108. 108.

    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).

    Article  CAS  Google Scholar 

  109. 109.

    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).

    Article  Google Scholar 

  110. 110.

    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).

    Article  Google Scholar 

  111. 111.

    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).

    Article  Google Scholar 

  112. 112.

    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).

    Article  Google Scholar 

  113. 113.

    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).

    Article  Google Scholar 

  114. 114.

    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).

    Article  Google Scholar 

  115. 115.

    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).

    Article  CAS  Google Scholar 

  116. 116.

    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).

    Article  Google Scholar 

  117. 117.

    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).

    Article  CAS  Google Scholar 

  118. 118.

    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).

    Article  CAS  Google Scholar 

  119. 119.

    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).

    Article  CAS  PubMed  Google Scholar 

  120. 120.

    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).

    Article  CAS  Google Scholar 

  121. 121.

    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).

    Article  CAS  Google Scholar 

  122. 122.

    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).

    Article  Google Scholar 

  123. 123.

    Magill, A. H. et al. Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecol. Appl. 7, 402–415 (1997).

    Article  Google Scholar 

  124. 124.

    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).

    Article  CAS  Google Scholar 

  125. 125.

    Martínez-Sánchez, J. L. Nitrogen and phosphorus resorption in trees of a neotropical rain forest. J. Trop. Ecol. 19, 465–468 (2003).

    Article  Google Scholar 

  126. 126.

    Alvarez-Sánchez, J. & Enríquez, R. B. Leaf decomposition in a Mexican tropical rain forest. Biotropica 28, 657–667 (1996).

    Article  Google Scholar 

  127. 127.

    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).

    CAS  Google Scholar 

  128. 128.

    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).

    Google Scholar 

  129. 129.

    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).

    Article  CAS  Google Scholar 

  130. 130.

    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).

    Google Scholar 

  131. 131.

    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).

    Article  CAS  Google Scholar 

  132. 132.

    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).

    Article  CAS  Google Scholar 

  133. 133.

    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).

    Article  CAS  Google Scholar 

  134. 134.

    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).

    Article  CAS  Google Scholar 

  135. 135.

    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).

    Article  PubMed  Google Scholar 

  136. 136.

    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).

    Article  CAS  Google Scholar 

  137. 137.

    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).

    Article  Google Scholar 

  138. 138.

    Sariyildiz, T. & Anderson, J. M. Interactions between litter quality, decomposition and soil fertility: a laboratory study. Soil Biol. Biochem. 35, 391–399 (2003).

    Article  CAS  Google Scholar 

  139. 139.

    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).

    Article  PubMed  Google Scholar 

  140. 140.

    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).

    Article  CAS  Google Scholar 

  141. 141.

    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).

    Google Scholar 

  142. 142.

    Wang, X., Huang, J. & Yan, E. Leaf litter decomposition of commen trees in Tiantong. Acta Phytoecol. Sin. 28, 457–467 (2004).

    Google Scholar 

  143. 143.

    Austin, A. T. & Vitousek, P. M. Nutrient dynamics on a precipitation gradient in Hawai’i. Oecologia 113, 519–529 (1998).

    Article  PubMed  Google Scholar 

  144. 144.

    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).

    Article  Google Scholar 

  145. 145.

    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).

    Article  Google Scholar 

  146. 146.

    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).

    Article  CAS  Google Scholar 

  147. 147.

    Diehl, P. et al. Nutrient conservation strategies in native Andean-Patagonian forests. J. Veg. Sci. 14, 63–70 (2003).

    Article  Google Scholar 

  148. 148.

    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).

    Article  CAS  Google Scholar 

  149. 149.

    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).

    Article  CAS  Google Scholar 

  150. 150.

    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).

    Article  Google Scholar 

  151. 151.

    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).

    CAS  Google Scholar 

  152. 152.

    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).

    Google Scholar 

  153. 153.

    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).

    Google Scholar 

  154. 154.

    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).

    Google Scholar 

  155. 155.

    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).

    Article  CAS  Google Scholar 

  156. 156.

    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).

    Article  Google Scholar 

  157. 157.

    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).

    Article  CAS  Google Scholar 

  158. 158.

    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).

    Article  CAS  Google Scholar 

  159. 159.

    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).

    Article  Google Scholar 

  160. 160.

    Birgander, J., Rousk, J. & Olsson, P. A. Comparison of fertility and seasonal effects on grassland microbial communities. Soil Biol. Biochem. 76, 80–89 (2014).

    Article  CAS  Google Scholar 

  161. 161.

    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).

    Article  CAS  Google Scholar 

  162. 162.

    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).

    Article  CAS  Google Scholar 

  163. 163.

    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).

    Article  PubMed  Google Scholar 

  164. 164.

    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).

    Article  Google Scholar 

  165. 165.

    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).

    Article  Google Scholar 

  166. 166.

    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).

    Article  Google Scholar 

  167. 167.

    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).

    Article  CAS  PubMed  Google Scholar 

  168. 168.

    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).

    Article  CAS  Google Scholar 

  169. 169.

    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).

    Article  CAS  Google Scholar 

  170. 170.

    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).

    Article  PubMed  Google Scholar 

  171. 171.

    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).

    Article  Google Scholar 

  172. 172.

    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).

    Article  CAS  Google Scholar 

  173. 173.

    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).

    Article  Google Scholar 

  174. 174.

    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).

    Article  Google Scholar 

  175. 175.

    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).

    Article  CAS  Google Scholar 

  176. 176.

    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).

    Article  Google Scholar 

  177. 177.

    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).

    Article  CAS  Google Scholar 

  178. 178.

    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).

    Article  CAS  Google Scholar 

  179. 179.

    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).

    Article  CAS  Google Scholar 

  180. 180.

    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).

    Article  CAS  Google Scholar 

  181. 181.

    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).

    Article  CAS  Google Scholar 

  182. 182.

    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).

    PubMed  Google Scholar 

  183. 183.

    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).

    Article  CAS  Google Scholar 

  184. 184.

    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).

    Article  CAS  Google Scholar 

  185. 185.

    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).

    Article  Google Scholar 

  186. 186.

    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).

    Article  CAS  Google Scholar 

  187. 187.

    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).

    Article  CAS  Google Scholar 

  188. 188.

    Kulmatiski, A. Changing soils to manage plant communities: activated carbon as a restoration tool in ex-arable fields. Restor. Ecol. 19, 102–110 (2011).

    Article  Google Scholar 

  189. 189.

    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).

  190. 190.

    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).

    Article  CAS  Google Scholar 

  191. 191.

    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).

    Article  CAS  Google Scholar 

  192. 192.

    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).

    Article  CAS  Google Scholar 

  193. 193.

    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).

    Article  CAS  Google Scholar 

  194. 194.

    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).

    Article  Google Scholar 

  195. 195.

    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).

    Article  CAS  PubMed  Google Scholar 

  196. 196.

    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).

    Article  CAS  Google Scholar 

  197. 197.

    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).

    Article  CAS  Google Scholar 

  198. 198.

    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).

    Article  Google Scholar 

  199. 199.

    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).

    Article  CAS  Google Scholar 

  200. 200.

    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).

    Article  Google Scholar 

  201. 201.

    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).

    Article  PubMed  Google Scholar 

  202. 202.

    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).

    Article  CAS  Google Scholar 

  203. 203.

    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).

    Article  CAS  Google Scholar 

  204. 204.

    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).

    Article  CAS  Google Scholar 

  205. 205.

    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).

    Article  PubMed  Google Scholar 

  206. 206.

    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).

    Article  Google Scholar 

  207. 207.

    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).

  208. 208.

    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).

    Article  CAS  Google Scholar 

  209. 209.

    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).

    Article  Google Scholar 

  210. 210.

    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).

    Article  CAS  PubMed  Google Scholar 

  211. 211.

    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).

    Article  Google Scholar 

  212. 212.

    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).

    Article  CAS  Google Scholar 

  213. 213.

    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).

    Article  PubMed  Google Scholar 

  214. 214.

    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).

    Article  CAS  Google Scholar 

  215. 215.

    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).

    Article  CAS  Google Scholar 

  216. 216.

    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).

    Article  CAS  Google Scholar 

  217. 217.

    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).

    Article  CAS  Google Scholar 

  218. 218.

    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).

    Article  CAS  Google Scholar 

  219. 219.

    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).

    Article  CAS  Google Scholar 

  220. 220.

    Wardle, D. A. & Jonsson, M. Long-term resilience of above- and belowground ecosystem components among contrasting ecosystems. Ecology 95, 1836–1849 (2014).

    Article  PubMed  Google Scholar 

  221. 221.

    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).

    Article  CAS  Google Scholar 

  222. 222.

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. 223.

    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).

    Article  Google Scholar 

  224. 224.

    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).

    Article  CAS  Google Scholar 

  225. 225.

    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).

    Article  Google Scholar 

  226. 226.

    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).

    Article  Google Scholar 

  227. 227.

    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).

    Article  CAS  PubMed  Google Scholar 

  228. 228.

    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).

    Article  CAS  Google Scholar 

  229. 229.

    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).

    Article  CAS  Google Scholar 

  230. 230.

    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).

    Article  CAS  Google Scholar 

  231. 231.

    Zhang, W. et al. Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob. Change Biol. 11, 266–277 (2011).

    Article  CAS  Google Scholar 

  232. 232.

    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).

    Article  CAS  Google Scholar 

  233. 233.

    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).

    Article  CAS  Google Scholar 

  234. 234.

    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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  235. 235.

    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).

    Article  CAS  PubMed  Google Scholar 

  236. 236.

    Burnham, K. P. & Anderson, D. R. Understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004)..

Download references

Acknowledgements

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.

Author information

Affiliations

Authors

Contributions

L.L. and M.D. designed the experiment. M.D. and L.L. collected and analysed the data. M.D., L.L. and L.J. wrote the manuscript. W.L., X.W., S.L., S.Y. and B.W. commented on the details of the manuscript drafts.

Corresponding author

Correspondence to Lingli Liu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figures 1–7, Supplementary Tables 1–11

Reporting Summary

Supplementary Dataset 1

N resorption efficiency and N mineralization rate data during litter decomposition

Supplementary Dataset 1

Soil bacteria to fungi ratio data

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

Further reading