Isotopic evidence for oligotrophication of terrestrial ecosystems

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Matters Arising to this article was published on 22 July 2019

Abstract

Human societies depend on an Earth system that operates within a constrained range of nutrient availability, yet the recent trajectory of terrestrial nitrogen (N) availability is uncertain. Examining patterns of foliar N concentrations and isotope ratios (δ15N) from more than 43,000 samples acquired over 37 years, here we show that foliar N concentration declined by 9% and foliar δ15N declined by 0.6–1.6‰. Examining patterns across different climate spaces, foliar δ15N declined across the entire range of mean annual temperature and mean annual precipitation tested. These results suggest declines in N supply relative to plant demand at the global scale. In all, there are now multiple lines of evidence of declining N availability in many unfertilized terrestrial ecosystems, including declines in δ15N of tree rings and leaves from herbarium samples over the past 75–150 years. These patterns are consistent with the proposed consequences of elevated atmospheric carbon dioxide and longer growing seasons. These declines will limit future terrestrial carbon uptake and increase nutritional stress for herbivores.

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Fig. 1: Relationships between residual foliar δ15N of non-N2-fixing species and predictors.
Fig. 2: Results of the regressions of residual foliar δ15N and residual log-transformed foliar [N].
Fig. 3: Conceptual diagram summarizing N availability bifurcation hypothesis for global terrestrial ecosystems.

Data availability

The data sets generated during and/or analysed during the current study are available in the Dryad repository (https://doi.org/10.5061/dryad.v2k2607). All codes used for statistical analyses and figure generation are available on Dryad (https://doi.org/10.5061/dryad.v2k2607).

References

  1. 1.

    Rockström, J. et al. A safe operating space for humanity. Nature 461, 472–475 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Fowler, D. et al. The global nitrogen cycle in the twenty-first century. Philo Trans. R. Soc. B 368, 20130164 (2013).

    Article  CAS  Google Scholar 

  4. 4.

    Clark, C. M., Morefield, P. E., Gilliam, F. S. & Pardo, L. H. Estimated losses of plant biodiversity in the United States from historical N deposition (1985–2010). Ecology 94, 1441–1448 (2013).

    Article  PubMed  Google Scholar 

  5. 5.

    de Vries, W., Kros, J., Kroeze, C. & Seitzinger, S. P. Assessing planetary and regional nitrogen boundaries related to food security and adverse environmental impacts. Curr. Opin. Environ. Sustain. 5, 392–402 (2013).

    Article  Google Scholar 

  6. 6.

    Sinha, E., Michalak, A. & Balaji, V. Eutrophication will increase during the 21st century as a result of precipitation changes. Science 357, 405–408 (2017).

    Article  CAS  PubMed  Google Scholar 

  7. 7.

    Vitousek, P. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).

    Article  CAS  Google Scholar 

  8. 8.

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

    Article  Google Scholar 

  9. 9.

    Gill, R. A. et al. Nonlinear grassland responses to past and future atmospheric CO2. Nature 417, 279–282 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Norby, R. J., Warren, J. M., Iversen, C. M., Medlyn, B. E. & McMurtrie, R. E. CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc. Natl Acad. Sci. USA 107, 19368–19373 (2010).

    Article  PubMed  Google Scholar 

  11. 11.

    Feng, Z. et al. Constraints to nitrogen acquisition of terrestrial plants under elevated CO2. Glob. Change Biol. 21, 3152–3168 (2015).

    Article  Google Scholar 

  12. 12.

    Elmore, A. J., Nelson, D. M. & Craine, J. M. Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests. Nat. Plants 2, 16133 (2016).

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Smith, B. et al. Implications of incorporating N cycling and N limitations on primary production in an individual-based dynamic vegetation model. Biogeosciences 11, 2027–2054 (2014).

    Article  Google Scholar 

  14. 14.

    Bobbink, R. et al. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30–59 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Craine, J. M., Elmore, A. & Angerer, J. P. Long-term declines in dietary nutritional quality for North American cattle. Environ. Res. Lett. 12, 044019 (2017).

    Article  CAS  Google Scholar 

  16. 16.

    Stiling, P. & Cornelissen, T. How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob. Change Biol. 13, 1823–1842 (2007).

    Article  Google Scholar 

  17. 17.

    Craine, J. M. et al. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol. 183, 980–992 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. 18.

    Craine, J. M. et al. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 1, 1–26 (2015).

    Article  CAS  Google Scholar 

  19. 19.

    Garten, C. T. Variation in foliar 15N abundance and the availability of soil-nitrogen on Walker Branch watershed. Ecology 74, 2098–2113 (1993).

    Article  Google Scholar 

  20. 20.

    Werner, G. D., Cornwell, W. K., Sprent, J. I., Kattge, J. & Kiers, E. T. A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat. Commun. 5, 4087 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009).

    Article  CAS  Google Scholar 

  22. 22.

    Craine, J. M. et al. Convergence of soil nitrogen isotopes across global climate gradients. Sci. Rep. 5, 8280 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Hietz, P. et al. Long-term change in the nitrogen cycle of tropical forests. Science 334, 664–666 (2011).

    Article  CAS  PubMed  Google Scholar 

  24. 24.

    Decina, S. M., Templer, P. H., Hutyra, L. R., Gately, C. K. & Rao, P. Variability, drivers, and effects of atmospheric nitrogen inputs across an urban area: emerging patterns among human activities, the atmosphere, and soils. Sci. Total Environ. 609, 1524–1534 (2017).

    Article  CAS  PubMed  Google Scholar 

  25. 25.

    McLauchlan, K. K. et al. Centennial-scale reductions in nitrogen availability in temperate forests of the United States. Sci. Rep. 7, 7856 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Jonard, M. et al. Tree mineral nutrition is deteriorating in Europe. Glob. Change Biol. 21, 418–430 (2015).

    Article  Google Scholar 

  27. 27.

    McLauchlan, K. K., Ferguson, C. J., Wilson, I. E., Ocheltree, T. W. & Craine, J. M. Thirteen decades of foliar isotopes indicate declining nitrogen availability in central North American grasslands. New Phytol. 187, 1135–1145 (2010).

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    Ziska, L. H. et al. Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proc. Biol. Sci. 283, 20160414 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Gruneberg, E., Ziche, D. & Wellbrock, N. Organic carbon stocks and sequestration rates of forest soils in Germany. Glob. Change Biol. 20, 2644–2662 (2014).

    Article  Google Scholar 

  30. 30.

    Durán, J. et al. Climate change decreases nitrogen pools and mineralization rates in northern hardwood forests. Ecosphere 7, e01251 (2016).

    Article  Google Scholar 

  31. 31.

    Eshleman, K. N., Sabo, R. D. & Kline, K. M. Surface water quality is improving due to declining atmospheric N deposition. Environ. Sci. Technol. 47, 12193–12200 (2013).

    Article  CAS  PubMed  Google Scholar 

  32. 32.

    Sabo, R. D. et al. Watershed-scale changes in terrestrial nitrogen cycling during a period of decreased atmospheric nitrate and sulfur deposition. Atmos. Environ. 146, 271–279 (2016).

    Article  CAS  Google Scholar 

  33. 33.

    Lucas, R. W. et al. Long‐term declines in stream and river inorganic nitrogen (N) export correspond to forest change. Ecol. Appl. 26, 545–556 (2016).

    Article  PubMed  Google Scholar 

  34. 34.

    Bernal, S., Hedin, L. O., Likens, G. E., Gerber, S. & Buso, D. C. Complex response of the forest nitrogen cycle to climate change. Proc. Natl Acad. Sci. USA 109, 3406–3411 (2012).

    Article  PubMed  Google Scholar 

  35. 35.

    Nordhaus, T., Shellenberger, M. & Blomqvist, L. The Planetary Boundaries Hypothesis. A Review of the Evidence (Breakthrough Institute, Oakland, 2012).

  36. 36.

    Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer L. A.) (IPCC, 2014).

  38. 38.

    New, M., Lister, D., Hulme, M. & Makin, I. A high-resolution data set of surface climate over global land areas.Clim. Res. 21, 1–25 (2002).

    Article  Google Scholar 

  39. 39.

    Rosseel, Y. lavaan: an R package for structural equation modeling. J. Stat. Softw. 48, 1–36 (2012).

    Article  Google Scholar 

  40. 40.

    Grace, J. B. Structural Equation Modeling and Natural Systems (Cambridge Univ. Press, Cambridge, 2006).

  41. 41.

    Eldridge, D. J., Wang, L. & Ruiz-Colmenero, M. Shrub encroachment alters the spatial patterns of infiltration. Ecohydrology 8, 83–93 (2015).

    Article  Google Scholar 

  42. 42.

    Lu, X., Wang, L. & McCabe, M. F. Elevated CO2 as a driver of global dryland greening. Sci. Rep. 6, 20716 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Anderson, J. T. & Gezon, Z. J. Plasticity in functional traits in the context of climate change: a case study of the subalpine forb Boechera stricta (Brassicaceae). Glob. Change Biol. 21, 1689–1703 (2015).

    Article  Google Scholar 

  44. 44.

    Aranibar, J. N., Goiran, S. B., Guevara, A. & Villagra, P. E. Carbon and nitrogen dynamics in a sandy groundwater-coupled ecosystem in the Monte Desert, indicated by plant stable isotopes. J. Arid Environ. 102, 58–67 (2014).

    Article  Google Scholar 

  45. 45.

    Averill, C. & Finzi, A. C. Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δ15N. Ecology 92, 883–891 (2011).

    Article  PubMed  Google Scholar 

  46. 46.

    Bai, E., Boutton, T. W., Liu, F., Ben Wu, X. & Archer, S. R. Variation in woody plant δ13C along a topoedaphic gradient in a subtropical savanna parkland. Oecologia 156, 479–489 (2008).

    Article  PubMed  Google Scholar 

  47. 47.

    Bai, E. et al. Spatial variation of the stable nitrogen isotope ratio of woody plants along a topoedaphic gradient in a subtropical savanna. Oecologia 159, 493–503 (2009).

    Article  PubMed  Google Scholar 

  48. 48.

    Bai, S. H., Sun, F., Xu, Z. & Blumfield, T. J. Ecophysiological status of different growth stage of understorey Acacia leiocalyx and Acacia disparrima in an Australian dry sclerophyll forest subjected to prescribed burning. J. Soils Sediments 13, 1378–1385 (2013).

    Article  Google Scholar 

  49. 49.

    Bansal, S., Nilsson, M.-C. & Wardle, D. A. Response of photosynthetic carbon gain to ecosystem retrogression of vascular plants and mosses in the boreal forest. Oecologia 169, 661–672 (2012).

    Article  PubMed  Google Scholar 

  50. 50.

    Baptist, F. et al. 13C and 15N allocations of two alpine species from early and late snowmelt locations reflect their different growth strategies. J. Exp. Bot. 60, 2725–2735 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Baraloto, C. et al. Decoupled leaf and stem economics in rain forest trees. Ecol. Lett. 13, 1338–1347 (2010).

    Article  PubMed  Google Scholar 

  52. 52.

    Bauer, G. A. et al. in Carbon and Nitrogen Cycling in European Forest Ecosystems (ed. Schulze, E.-D.) 189–214 (Springer, Berlin, 2000).

  53. 53.

    Bauters, M. et al. Parallel functional and stoichiometric trait shifts in South-American and African forest communities with elevation. Biogeosci. Discuss. 2017, 1–27 (2017).

    Article  Google Scholar 

  54. 54.

    Bazot, S., Fresneau, C., Damesin, C. & Barthes, L. Contribution of previous year’s leaf N and soil N uptake to current year’s leaf growth in sessile oak. Biogeosciences 13, 3475–3484 (2016).

    Article  Google Scholar 

  55. 55.

    Beyschlag, W., Hanisch, S., Friedrich, S., Jentsch, A. & Werner, C. 15N natural abundance during early and late succession in a middle-European dry acidic grassland. Plant Biol. 11, 713–724 (2009).

    Article  CAS  PubMed  Google Scholar 

  56. 56.

    Blonder, B., Baldwin, B. G., Enquist, B. J. & Robichaux, R. H. Variation and macroevolution in leaf functional traits in the Hawaiian silversword alliance (Asteraceae). J. Ecol. 104, 219–228 (2016).

    Article  Google Scholar 

  57. 57.

    Blumenthal, S. A., Chritz, K. L., Rothman, J. M. & Cerling, T. E. Detecting intraannual dietary variability in wild mountain gorillas by stable isotope analysis of feces. Proc. Natl Acad. Sci. USA 109, 21277–21282 (2012).

    Article  PubMed  Google Scholar 

  58. 58.

    Blumenthal, S. A., Rothman, J. M., Chritz, K. L. & Cerling, T. E. Stable isotopic variation in tropical forest plants for applications in primatology. Am. J. Primatol. 78, 92 (2016).

  59. 59.

    Boeckx, P., Paulino, L., Oyarzun, C., van Cleemput, O. & Godoy, R. Soil δ15N patterns in old-growth forests of southern Chile as integrator for N-cycling. Isotopes Environ. Health Stud. 41, 249–259 (2005).

    Article  CAS  PubMed  Google Scholar 

  60. 60.

    Brearley, F. Q. Nitrogen stable isotopes indicate differences in nitrogen cycling between two contrasting Jamaican montane forests. Plant Soil 367, 465–476 (2013).

    Article  CAS  Google Scholar 

  61. 61.

    Brearley, F. Q., Fine, P. V. A. & Perreijn, K. Does nitrogen availability have greater control over the formation of tropical heath forests than water stress? A hypothesis based on nitrogen isotope ratios. Acta Amazon. 41, 589–592 (2011).

    Article  CAS  Google Scholar 

  62. 62.

    Burton, J. I., Perakis, S. S., McKenzie, S. C., Lawrence, C. E. & Puettmann, K. J. Intraspecific variability and reaction norms of forest understory plant species traits. Funct. Ecol. 31, 1881–1893 (2017).

    Article  Google Scholar 

  63. 63.

    Cardon, Z. G., Stark, J. M., Herron, P. M. & Rasmussen, J. A. Sagebrush carrying out hydraulic lift enhances surface soil nitrogen cycling and nitrogen uptake into inflorescences. Proc. Natl Acad. Sci. USA 110, 18988–18993 (2013).

    Article  CAS  PubMed  Google Scholar 

  64. 64.

    Carr, A. S., Chase, B. M., Boom, A. & Medina-Sanchez, J. Stable isotope analyses of rock hyrax faecal pellets, hyraceum and associated vegetation in southern Africa: implications for dietary ecology and palaeoenvironmental reconstructions. J. Arid Environ. 134, 33–48 (2016).

    Article  Google Scholar 

  65. 65.

    Chen, C., Li, J., Wang, G. & Shi, M. Accounting for the effect of temperature in clarifying the response of foliar nitrogen isotope ratios to atmospheric nitrogen deposition. Sci. Total Environ. 609, 1295–1302 (2017).

    Article  CAS  PubMed  Google Scholar 

  66. 66.

    Compton, J. E., Hooker, T. D. & Perakis, S. S. Ecosystem N distribution and δ15N during a century of forest regrowth after agricultural abandonment. Ecosystems 10, 1197–1208 (2007).

    Article  CAS  Google Scholar 

  67. 67.

    Correa, S. B., Winemiller, K. & Cardenas, D. Isotopic variation among Amazonian floodplain woody plants and implications for food-web research. Biota Neotrop. 16, e20150078 (2016).

    Article  Google Scholar 

  68. 68.

    Courty, P.-E. et al. Carbon and nitrogen metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis. Plant Physiol. 156, 952–961 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Couto-Vazquez, A. & Gonzalez-Prieto, S. J. Effects of biotic and abiotic factors on δ15N in young Pinus radiata. Eur. J. For. Res. 133, 631–637 (2014).

    Article  CAS  Google Scholar 

  70. 70.

    Couto-Vázquez, A. & González-Prieto, S. J. Effects of climate, tree age, dominance and growth on δ15N in young pinewoods. Trees 24, 507–514 (2010).

    Article  Google Scholar 

  71. 71.

    Craine, J. M. et al. Grazing and landscape controls on nitrogen availability across 330 South African savanna sites. Austral Ecol. 34, 731–740 (2009).

    Article  Google Scholar 

  72. 72.

    Craine, J. M., Towne, E. G., Ocheltree, T. W. & Nippert, J. B. Community traitscape of foliar nitrogen isotopes reveals N availability patterns in a tallgrass prairie. Plant Soil 356, 395–403 (2012).

    Article  CAS  Google Scholar 

  73. 73.

    Crowley, B. E., McGoogan, K. C. & Lehman, S. M. Edge effects on foliar stable isotope values in a Madagascan tropical dry forest. PLoS ONE 7, e44538 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Crowley, B. E., Rasoazanabary, E. & Godfrey, L. R. Stable isotopes complement focal individual observations and confirm dietary variability in reddish-gray mouse lemurs (Microcebus griseorufus) from southwestern Madagascar. Am. J. Phys. Anthropol. 155, 77–90 (2014).

    Article  PubMed  Google Scholar 

  75. 75.

    Crowley, B. E. et al. Explaining geographical variation in the isotope composition of mouse lemurs (Microcebus). J. Biogeogr. 38, 2106–2121 (2011).

    Article  Google Scholar 

  76. 76.

    Dahlin, K. M., Asner, G. P. & Field, C. B. Environmental and community controls on plant canopy chemistry in a Mediterranean-type ecosystem. Proc. Natl Acad. Sci. USA 110, 6895–6900 (2013).

    Article  PubMed  Google Scholar 

  77. 77.

    Dawes, M. A., Schleppi, P., Hattenschwiler, S., Rixen, C. & Hagedorn, F. Soil warming opens the nitrogen cycle at the alpine treeline. Glob. Change Biol. 23, 421–434 (2017).

    Article  Google Scholar 

  78. 78.

    Diaz, F. P., Frugone, M., Gutierrez, R. A. & Latorre, C. Nitrogen cycling in an extreme hyperarid environment inferred from δ15N analyses of plants, soils and herbivore diet. Sci. Rep. 6, 22226 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Domingues, T. F., Martinelli, L. A. & Ehleringer, J. R. Ecophysiological traits of plant functional groups in forest and pasture ecosystems from eastern Amazonia, Brazil. Plant Ecol. 193, 101–112 (2007).

    Article  Google Scholar 

  80. 80.

    Dominguez, M. T. et al. Relationships between leaf morphological traits, nutrient concentrations and isotopic signatures for Mediterranean woody plant species and communities. Plant Soil 357, 407–424 (2012).

    Article  CAS  Google Scholar 

  81. 81.

    Elmore, A. J., Craine, J. M., Nelson, D. M . & Guinn, S. M. Continental scale variability of foliar nitrogen and carbon isotopes in Populus balsamifera and their relationships with climate. Sci. Rep. 7, 7759 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Ens, E., Hutley, L. B., Rossiter-Rachor, N. A., Douglas, M. M. & Setterfield, S. A. Resource-use efficiency explains grassy weed invasion in a low-resource savanna in north Australia. Front. Plant Sci. 6, 560 (2015).

    Google Scholar 

  83. 83.

    Evaristo, J. & McDonnell, J. J. Carbon, nitrogen, and water stable isotopes in plant tissue and soils across a moisture gradient in Puerto Rico. Hydrol. Process. 31, 1558–1559 (2017).

    Article  CAS  Google Scholar 

  84. 84.

    Fajardo, A. & Gundale, M. J. Combined effects of anthropogenic fires and land-use change on soil properties and processes in Patagonia, Chile. For. Ecol. Manage. 357, 60–67 (2015).

    Article  Google Scholar 

  85. 85.

    Falxa-Raymond, N., Palmer, M. I., McPhearson, T. & Griffin, K. L. Foliar nitrogen characteristics of four tree species planted in New York City forest restoration sites. Urban Ecosyst. 17, 807–824 (2014).

    Article  Google Scholar 

  86. 86.

    Falxa-Raymond, N., Patterson, A. E., Schuster, W. S. F. & Griffin, K. L. Oak loss increases foliar nitrogen, δ15N and growth rates of Betula lenta in a northern temperate deciduous forest. Tree Physiol. 32, 1092–1101 (2012).

    Article  CAS  PubMed  Google Scholar 

  87. 87.

    Fang, Y. et al. Nitrogen deposition and forest nitrogen cycling along an urban-rural transect in southern China. Glob. Change Biol. 17, 872–885 (2011).

    Article  Google Scholar 

  88. 88.

    Feng, Z., Brumme, R., Xu, Y. J. & Lamersdorf, N. Tracing the fate of mineral N compounds under high ambient N deposition in a Norway spruce forest at Solling/Germany. For. Ecol. Manage. 255, 2061–2073 (2008).

    Article  Google Scholar 

  89. 89.

    Finger, R. A. et al. Effects of permafrost thaw on nitrogen availability and plant-soil interactions in a boreal Alaskan lowland. J. Ecol. 104, 1542–1554 (2016).

    Article  Google Scholar 

  90. 90.

    Frenette‐Dussault, C., Shipley, B., Léger, J. F., Meziane, D. & Hingrat, Y. Functional structure of an arid steppe plant community reveals similarities with Grime’s C‐S‐R theory. J. Veg. Sci. 23, 208–222 (2012).

    Article  Google Scholar 

  91. 91.

    Fujiyoshi, L. et al. Spatial variations in larch needle and soil 15N at a forest-grassland boundary in northern Mongolia. Isotopes Environ. Health Stud. 53, 54–69 (2017).

    Article  CAS  PubMed  Google Scholar 

  92. 92.

    Gao, J., Zhao, P., Shen, W., Rao, X. & Hu, Y. Physiological homeostasis and morphological plasticity of two tree species subjected to precipitation seasonal distribution changes. Perspect. Plant Ecol. Evol. Syst. 25, 1–19 (2017).

    Article  Google Scholar 

  93. 93.

    Gao, J. et al. Suppression of nighttime sap flux with lower stem photosynthesis in Eucalyptus trees. Int. J. Biometeorol. 60, 545–556 (2016).

    Article  PubMed  Google Scholar 

  94. 94.

    Godfrey, L. R. et al. What did Hadropithecus eat, and why should paleoanthropologists care? Am. J. Primatol. 78, 1098–1112 (2016).

    Article  CAS  PubMed  Google Scholar 

  95. 95.

    Golluscio, R., Faigon, A. & Tanke, M. Spatial distribution of roots and nodules, and δ15N evidence of nitrogen fixation in Adesmia volckmanni, a Patagonian leguminous shrub. J. Arid Environ. 67, 328–335 (2006).

    Article  Google Scholar 

  96. 96.

    Gos, P. et al. Relative contribution of soil, management and traits to co-variations of multiple ecosystem properties in grasslands. Oecologia 180, 1001–1013 (2016).

    Article  PubMed  Google Scholar 

  97. 97.

    Gray, A. et al. Does geographic origin dictate ecological strategies in Acacia senegal (L.) Willd.? Evidence from carbon and nitrogen stable isotopes. Plant Soil 369, 479–496 (2013).

    Article  CAS  Google Scholar 

  98. 98.

    Große‐Stoltenberg, A., Hellmann, C., Thiele, J., Oldeland, J. & Werner, C. Invasive acacias differ from native dune species in the hyperspectral/biochemical trait space. J. Veg. Sci. 29, 325–335 (2018).

    Article  Google Scholar 

  99. 99.

    Guerrieri, R., Lepine, L., Asbjornsen, H., Xiao, J. & Ollinger, S. V. Evapotranspiration and water use efficiency in relation to climate and canopy nitrogen in US forests. J. Geophys. Res. Biogeosci. 121, 2610–2629 (2016).

    Article  CAS  Google Scholar 

  100. 100.

    Gundale, M. J., Deluca, T. H. & Nordin, A. Bryophytes attenuate anthropogenic nitrogen inputs in boreal forests. Glob. Change Biol. 17, 2743–2753 (2011).

    Article  Google Scholar 

  101. 101.

    Gundale, M. J., From, F., Bach, L. H. & Nordin, A. Anthropogenic nitrogen deposition in boreal forests has a minor impact on the global carbon cycle. Glob. Change Biol. 20, 276–286 (2014).

    Article  Google Scholar 

  102. 102.

    Gundale, M. J., Hyodo, F., Nilsson, M.-C. & Wardle, D. A. Nitrogen niches revealed through species and functional group removal in a boreal shrub community. Ecology 93, 1695–1706 (2012).

    Article  PubMed  Google Scholar 

  103. 103.

    Gurmesa, G. A. et al. Nitrogen input 15N signatures are reflected in plant 15N natural abundances in subtropical forests in China. Biogeosciences 14, 2359–2370 (2017).

    Article  CAS  Google Scholar 

  104. 104.

    Haberer, K. et al. Effects of long-term free-air ozone fumigation on δ15N and total N in Fagus sylvatica and associated mycorrhizal fungi. Plant Biol. 9, 242–252 (2007).

    Article  CAS  PubMed  Google Scholar 

  105. 105.

    Hall, S. J., Hale, R. L., Baker, M. A., Bowling, D. R. & Ehleringer, J. R. Riparian plant isotopes reflect anthropogenic nitrogen perturbations: robust patterns across land use gradients. Ecosphere 6, 1137–1146 (2015).

    Google Scholar 

  106. 106.

    Hamerlynck, E. P. & McAuliffe, J. R. Growth and foliar δ15N of a Mojave desert shrub in relation to soil hydrological dynamics. J. Arid Environ. 74, 1569–1571 (2010).

    Article  Google Scholar 

  107. 107.

    Havik, G., Catenazzi, A. & Holmgren, M. Seabird nutrient subsidies benefit non-nitrogen fixing trees and alter species composition in South American coastal dry forests. PloS ONE 9, e86381 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Hawke, D. et al. Foliar and soil N and δ15N as restoration metrics at Pūtaringamotu Riccarton Bush, Christchurch city. J. R. Soc. N. Z. 47, 319–335 (2017).

    Article  Google Scholar 

  109. 109.

    Hellmann, C., Grosse-Stoltenberg, A., Laustroeer, V., Oldeland, J. & Werner, C. Retrieving nitrogen isotopic signatures from fresh leaf reflectance spectra: disentangling δ15N from biochemical and structural leaf properties. Front. Plant Sci. 6, 307 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Hellmann, C., Grosse-Stoltenberg, A., Thiele, J., Oldeland, J. & Werner, C. Heterogeneous environments shape invader impacts: integrating environmental, structural and functional effects by isoscapes and remote sensing. Sci. Rep. 7, 4118 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Hellmann, C., Rascher, K. G., Oldeland, J. & Werner, C. Isoscapes resolve species-specific spatial patterns in plant-plant interactions in an invaded Mediterranean dune ecosystem. Tree Physiol. 36, 1460–1470 (2016).

    Article  CAS  PubMed  Google Scholar 

  112. 112.

    Hellmann, C. et al. Impact of an exotic N2-fixing Acacia on composition and N status of a native Mediterranean community. Acta Oecol. 37, 43–50 (2011).

    Article  Google Scholar 

  113. 113.

    Hellmann, C., Werner, C. & Oldeland, J. A spatially explicit dual-isotope approach to map regions of plant-plant interaction after exotic plant invasion. PLoS ONE 11, e0159403 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 114.

    Hobbie, E. A., Rice, S. F., Weber, N. S. & Smith, J. E. Isotopic evidence indicates saprotrophy in post-fire Morchella in Oregon and Alaska. Mycologia 108, 638–645 (2016).

    Article  CAS  PubMed  Google Scholar 

  115. 115.

    Hobbie, J. E. et al. Mycorrhizal fungi supply nitrogen to host plants in Arctic tundra and boreal forests: 15N is the key signal. Can. J. Microbiol. 55, 84–94 (2009).

    Article  CAS  PubMed  Google Scholar 

  116. 116.

    Hofmeister, J., Hosek, J., Buzek, F. & Rolecek, J. Foliar N concentration and δ15N signature reflect the herb layer species diversity and composition in oak-dominated forests. Appl. Veg. Sci. 15, 318–328 (2012).

    Article  Google Scholar 

  117. 117.

    Hofmockel, K. S. et al. Sources of increased N uptake in forest trees growing under elevated CO2: results of a large-scale 15N study. Glob. Change Biol. 17, 3338–3350 (2011).

    Article  Google Scholar 

  118. 118.

    Hogberg, P. et al. Recovery of ectomycorrhiza after ‘nitrogen saturation’ of a conifer forest. New Phytol. 189, 515–525 (2011).

    Article  PubMed  Google Scholar 

  119. 119.

    Hogberg, P. & Alexander, I. J. Roles of root symbioses in African woodland and forest: evidence from 15N abundance and foliar analysis. J. Ecol. 83, 217–224 (1995).

    Article  Google Scholar 

  120. 120.

    Hoogmoed, M., Cunningham, S. C., Baker, P., Beringer, J. & Cavagnaro, T. R. N-fixing trees in restoration plantings: effects on nitrogen supply and soil microbial communities. Soil Biol. Biochem. 77, 203–212 (2014).

    Article  CAS  Google Scholar 

  121. 121.

    Houle, D., Moore, J. D., Ouimet, R. & Marty, C. Tree species partition N uptake by soil depth in boreal forests. Ecology 95, 1127–1133 (2014).

    Article  CAS  PubMed  Google Scholar 

  122. 122.

    Hudson, J. M. G., Henry, G. H. R. & Cornwell, W. K. Taller and larger: shifts in Arctic tundra leaf traits after 16 years of experimental warming. Glob. Change Biol. 17, 1013–1021 (2011).

    Article  Google Scholar 

  123. 123.

    Hyodo, F., Kusaka, S., Wardle, D. A. & Nilsson, M.-C. Changes in stable nitrogen and carbon isotope ratios of plants and soil across a boreal forest fire chronosequence. Plant Soil 364, 315–323 (2013).

    Article  CAS  Google Scholar 

  124. 124.

    Ingram, L. J. & Adams, M. A. Does season and grazing influence the δ13C and δ15N of C4 native grasses in semi-arid rangelands of the Pilbara region of NW Australia? Agric. Ecosyst. Environ. 236, 277–284 (2017).

    Article  CAS  Google Scholar 

  125. 125.

    Jiang, C. & Zhang, X. N isotopes and N cycle in the TieShanPing subtropical forest ecosystem, southwestern China. Environ. Monit. Assess. 154, 301–308 (2009).

    Article  CAS  PubMed  Google Scholar 

  126. 126.

    Kahmen, A., Wanek, W. & Buchmann, N. Foliar δ15N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient. Oecologia 156, 861–870 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  127. 127.

    Kang, H. et al. Variation in foliar δ15N among oriental oak (Quercus variabilis) stands over eastern China: patterns and interactions. J. Geochem. Explor. 110, 8–14 (2011).

    Article  CAS  Google Scholar 

  128. 128.

    Kearsley, E. et al. Functional community structure of African monodominant Gilbertiodendron dewevrei forest influenced by local environmental filtering. Ecol. Evol. 7, 295–304 (2017).

    Article  PubMed  Google Scholar 

  129. 129.

    Kenzo, T., Tanaka-Oda, A., Mastuura, Y. & Hinzman, L. D. Morphological and physicochemical traits of leaves of different life-forms of various broadleaf woody plants in interior Alaska. Can. J. For. Res. 46, 1475–1482 (2016).

    Article  CAS  Google Scholar 

  130. 130.

    Kleinebecker, T. et al. Evidence from the real world: 15N natural abundances reveal enhanced nitrogen use at high plant diversity in Central European grasslands. J. Ecol. 102, 456–465 (2014).

    Article  CAS  Google Scholar 

  131. 131.

    Klopatek, J. M., Barry, M. J. & Johnson, D. W. Potential canopy interception of nitrogen in the Pacific Northwest, USA. For. Ecol. Manage. 234, 344–354 (2006).

    Article  Google Scholar 

  132. 132.

    Koba, K. et al. δ15N of soil N and plants in a N-saturated, subtropical forest of southern China. Rapid Commun. Mass Spectrom. 24, 2499–2506 (2010).

    Article  CAS  PubMed  Google Scholar 

  133. 133.

    Koch, P. L. & Fox, L. R. Browsing impacts on the stable isotope composition of chaparral plants. Ecosphere 8, e01686 (2017).

    Article  Google Scholar 

  134. 134.

    Korner, C., Leuzinger, S., Riedl, S., Siegwolf, R. T. & Streule, L. Carbon and nitrogen stable isotope signals for an entire alpine flora, based on herbarium samples. Alp. Bot. 126, 153–166 (2016).

    Article  Google Scholar 

  135. 135.

    Kranabetter, J. & Meeds, J. Tree ring δ15N as validation of space-for-time substitution in disturbance studies of forest nitrogen status. Biogeochemistry 134, 201–215 (2017).

    Article  CAS  Google Scholar 

  136. 136.

    Kranabetter, J. M., Dube, S. & Lilles, E. An investigation into the contrasting growth response of lodgepole pine and white spruce to harvest-related soil disturbance. Can. J. For. Res. 47, 340–348 (2016).

    Article  CAS  Google Scholar 

  137. 137.

    Kranabetter, J. M. & MacKenzie, W. H. Contrasts among mycorrhizal plant guilds in foliar nitrogen concentration and δ15N along productivity gradients of a boreal forest. Ecosystems 13, 108–117 (2010).

    Article  CAS  Google Scholar 

  138. 138.

    Kuang, Y. et al. Nitrogen deposition influences nitrogen isotope composition in soil and needles of Pinus massoniana forests along an urban-rural gradient in the Pearl River Delta of south China. J. Soils Sediments 11, 589–595 (2011).

    Article  CAS  Google Scholar 

  139. 139.

    Ladd, B., Pepper, D. A. & Bonser, S. P. Competition intensity at local versus regional spatial scales. Plant Biol. 12, 772–779 (2010).

    Article  CAS  PubMed  Google Scholar 

  140. 140.

    Laiolo, P., Carlos Illera, J., Melendez, L., Segura, A. & Ramon Obeso, J. Abiotic, biotic, and evolutionary control of the distribution of C and N isotopes in food webs. Am. Nat. 185, 169–182 (2015).

    Article  PubMed  Google Scholar 

  141. 141.

    Laughlin, D. C., Fule, P. Z., Huffman, D. W., Crouse, J. & Laliberte, E. Climatic constraints on trait‐based forest assembly. J. Ecol. 99, 1489–1499 (2011).

    Article  Google Scholar 

  142. 142.

    LeDuc, S. D., Rothstein, D. E., Yermakov, Z. & Spaulding, S. E. Jack pine foliar δ15N indicates shifts in plant nitrogen acquisition after severe wildfire and through forest stand development. Plant Soil 373, 955–965 (2013).

    Article  CAS  Google Scholar 

  143. 143.

    Li, Y., Xue, J., Clinton, P. W. & Dungey, H. S. Genetic parameters and clone by environment interactions for growth and foliar nutrient concentrations in radiata pine on 14 widely diverse New Zealand sites. Tree Genet. Genomes 11, 10 (2015).

    Article  Google Scholar 

  144. 144.

    Liu, X., Wang, G., Li, J. & Wang, Q. Nitrogen isotope composition characteristics of modern plants and their variations along an altitudinal gradient in Dongling Mountain in Beijing. Sci. China Ser. D Earth Sci. 53, 128–140 (2010).

    Article  CAS  Google Scholar 

  145. 145.

    Liu, X. et al. Foliar δ13C and δ15N values of C3 plants in the Ethiopia Rift Valley and their environmental controls. Chin. Sci. Bull. 52, 1265–1273 (2007).

    Article  CAS  Google Scholar 

  146. 146.

    Ma, L. et al. Ecophysiological and foliar nitrogen concentration responses of understorey Acacia spp. and Eucalyptus sp. to prescribed burning. Environ. Sci. Pollut. R. 22, 10254–10262 (2015).

    Article  CAS  Google Scholar 

  147. 147.

    Makarov, M. I. et al. Determinants of 15N natural abundance in leaves of co-occurring plant species and types within an alpine lichen heath in the Northern Caucasus. Arct. Antarct. Alp. Res. 46, 581–590 (2014).

    Article  Google Scholar 

  148. 148.

    Maranon-Jimenez, S., Castro, J., Ignacio Querejeta, J., Fernandez-Ondono, E. & Allen, C. D. Post-fire wood management alters water stress, growth, and performance of pine regeneration in a Mediterranean ecosystem. For. Ecol. Manage. 308, 231–239 (2013).

    Article  Google Scholar 

  149. 149.

    Matsushima, M., Choi, W.-J. & Chang, S. X. White spruce foliar δ13C and δ15N indicate changed soil N availability by understory removal and N fertilization in a 13-year-old boreal plantation. Plant Soil 361, 375–384 (2012).

    Article  CAS  Google Scholar 

  150. 150.

    Mayor, J. R., Schuur, E. A. G., Mack, M. C., Hollingsworth, T. N. & Baath, E. Nitrogen isotope patterns in Alaskan black spruce reflect organic nitrogen sources and the activity of ectomycorrhizal fungi. Ecosystems 15, 819–831 (2012).

    Article  CAS  Google Scholar 

  151. 151.

    Mayor, J. R., Wright, S. J., Schuur, E. A. G., Brooks, M. E. & Turner, B. L. Stable nitrogen isotope patterns of trees and soils altered by long-term nitrogen and phosphorus addition to a lowland tropical rainforest. Biogeochemistry 119, 293–306 (2014).

    Article  CAS  Google Scholar 

  152. 152.

    McGlynn, T. P. et al. Spurious and functional correlates of the isotopic composition of a generalist across a tropical rainforest landscape. BMC Ecol. 9, 23–23 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. 153.

    McLauchlan, K. K., Craine, J. M., Nippert, J. B. & Ocheltree, T. W. Lack of eutrophication in a tallgrass prairie ecosystem over 27 years. Ecology 95, 1225–1235 (2014).

    Article  PubMed  Google Scholar 

  154. 154.

    Medina, E., Cuevas, E. & Lugo, A. E. Substrate chemistry and rainfall regime regulate elemental composition of tree leaves in karst forests. Forests 8, 182 (2017).

    Article  Google Scholar 

  155. 155.

    Menge, D. N. L., Baisden, W. T., Richardson, S. J., Peltzer, D. A. & Barbour, M. M. Declining foliar and litter δ15N diverge from soil, epiphyte and input δ15N along a 120,000 yr temperate rainforest chronosequence. New Phytol. 190, 941–952 (2011).

    Article  CAS  PubMed  Google Scholar 

  156. 156.

    Menyailo, O. V., Makarov, M. I. & Cheng, C. H. Isotopic composition of carbon (δ13C) and nitrogen (δ15N) in foliage and soil as a function of tree species. Dokl. Biol. Sci. 456, 209–211 (2014).

    Article  CAS  PubMed  Google Scholar 

  157. 157.

    Mercado, A. R. Jr, Van Noordwijk, M. & Cadisch, G. Positive nitrogen balance of Acacia mangium woodlots as fallows in the Philippines based on 15N natural abundance data of N2 fixation. Agroforest. Syst. 81, 221–233 (2011).

    Article  Google Scholar 

  158. 158.

    Meyer, W. M. III & Yeung, N. W. Trophic relationships among terrestrial molluscs in a Hawaiian rain forest: analysis of carbon and nitrogen isotopes. J. Trop. Ecol. 27, 441–445 (2011).

    Article  Google Scholar 

  159. 159.

    Morford, S. L., Houlton, B. Z. & Dahlgren, R. A. Increased forest ecosystem carbon and nitrogen storage from nitrogen rich bedrock. Nature 477, 78–81 (2011).

    Article  CAS  PubMed  Google Scholar 

  160. 160.

    Msanne, J. et al. Ecophysiological responses of native invasive woody Juniperus virginiana L. to resource availability and stand characteristics in the semiarid grasslands of the Nebraska Sandhills. Photosynthetica 55, 219–230 (2017).

    Article  Google Scholar 

  161. 161.

    Murphy, B. P. & Bowman, D. M. J. S. The carbon and nitrogen isotope composition of Australian grasses in relation to climate. Funct. Ecol. 23, 1040–1049 (2009).

    Article  Google Scholar 

  162. 162.

    Nielsen, J. A., Frew, R. D., Whigham, P. A., Callaway, R. M. & Dickinson, K. J. M. Thyme travels: 15N isoscapes of Thymus vulgaris L. invasion in lightly grazed pastoral communities. Austral Ecol. 41, 28–39 (2016).

    Article  Google Scholar 

  163. 163.

    Ogaya, R. & Penuelas, J. Changes in leaf δ13C and δ15N for three Mediterranean tree species in relation to soil water availability. Acta Oecol. 34, 331–338 (2008).

    Article  Google Scholar 

  164. 164.

    Pasquini, S. C. & Santiago, L. S. Nutrients limit photosynthesis in seedlings of a lowland tropical forest tree species. Oecologia 168, 311–319 (2012).

    Article  CAS  PubMed  Google Scholar 

  165. 165.

    Pellegrini, A. F. A., Hoffmann, W. A. & Franco, A. C. Carbon accumulation and nitrogen pool recovery during transitions from savanna to forest in central Brazil. Ecology 95, 342–352 (2014).

    Article  PubMed  Google Scholar 

  166. 166.

    Perakis, S. S. & Kellogg, C. H. Imprint of oaks on nitrogen availability and δ15N in California grassland-savanna: a case of enhanced N inputs? Plant Ecol. 191, 209–220 (2007).

    Article  Google Scholar 

  167. 167.

    Perakis, S. S., Tepley, A. J. & Compton, J. E. Disturbance and topography shape nitrogen availability and δ15N over long-term forest succession. Ecosystems 18, 573–588 (2015).

    Article  CAS  Google Scholar 

  168. 168.

    Perakis, S. S., Sinkhorn, E. R. & Compton, J. E. δ15N constraints on long-term nitrogen balances in temperate forests. Oecologia 167, 793–807 (2011).

    Article  PubMed  Google Scholar 

  169. 169.

    Peri, P. L. et al. Carbon (δ13C) and nitrogen (δ15N) stable isotope composition in plant and soil in Southern Patagonia’s native forests. Glob. Change Biol. 18, 311–321 (2012).

    Article  Google Scholar 

  170. 170.

    Pillar, V. D. & Sosinski, E. E. Jr An improved method for searching plant functional types by numerical analysis. J. Veg. Sci. 14, 323–332 (2003).

    Article  Google Scholar 

  171. 171.

    Pons, T. L., Perreijn, K., van Kessel, C. & Werger, M. J. A. Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytol. 173, 154–167 (2007).

    Article  CAS  PubMed  Google Scholar 

  172. 172.

    Powers, J. S. & Tiffin, P. Plant functional type classifications in tropical dry forests in Costa Rica: leaf habit versus taxonomic approaches. Funct. Ecol. 24, 927–936 (2010).

    Article  Google Scholar 

  173. 173.

    Priyadarshini, K. V. R. et al. Overlap in nitrogen sources and redistribution of nitrogen between trees and grasses in a semi-arid savanna. Oecologia 174, 1107–1116 (2014).

    Article  CAS  PubMed  Google Scholar 

  174. 174.

    Ren, H. et al. Exacerbated nitrogen limitation ends transient stimulation of grassland productivity by increased precipitation. Ecol. Monogr. 87, 457–469 (2017).

    Article  Google Scholar 

  175. 175.

    Roa-Fuentes, L. L., Templer, P. H. & Campo, J. Effects of precipitation regime and soil nitrogen on leaf traits in seasonally dry tropical forests of the Yucatan Peninsula, Mexico. Oecologia 179, 585–597 (2015).

    Article  PubMed  Google Scholar 

  176. 176.

    Roberts, P., Blumenthal, S. A., Dittus, W., Wedage, O. & Lee-Thorp, J. A. Stable carbon, oxygen, and nitrogen, isotope analysis of plants from a South Asian tropical forest: implications for primatology. Am. J. Primatol. 79, e22656 (2017).

    Article  CAS  Google Scholar 

  177. 177.

    Roggy, J. C. et al. Complementary N uptake strategies between tree species in tropical rainforest. Int. Sch. Res. Notices 2014, 427194 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  178. 178.

    Roggy, J. C., Prevost, M. F., Garbaye, J. & Domenach, A. M. Nitrogen cycling in the tropical rain forest of French Guiana: comparison of two sites with contrasting soil types using δ15N. J. Trop. Ecol. 15, 1–22 (1999).

    Article  Google Scholar 

  179. 179.

    Rosado, B. H. P. & de Mattos, E. A. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J. Veg. Sci. 21, 43–54 (2010).

    Article  Google Scholar 

  180. 180.

    Ruiz-Navarro, A., Barbera, G. G., Albaladejo, J. & Querejeta, J. I. Plant δ15N reflects the high landscape-scale heterogeneity of soil fertility and vegetation productivity in a Mediterranean semiarid ecosystems. New Phytol. 212, 1030–1043 (2016).

    Article  CAS  PubMed  Google Scholar 

  181. 181.

    Salmon, V. G. et al. Nitrogen availability increases in a tundra ecosystem during five years of experimental permafrost thaw. Glob. Change Biol. 22, 1927–1941 (2016).

    Article  Google Scholar 

  182. 182.

    Santiago, L., Silvera, K., Andrade, J. & Dawson, T. Functional strategies of tropical dry forest plants in relation to growth form and isotopic composition. Environ. Res. Lett. 12, 115006 (2017).

    Article  CAS  Google Scholar 

  183. 183.

    Schimann, H. et al. Differing nitrogen use strategies of two tropical rainforest late successional tree species in French Guiana: evidence from 15N natural abundance and microbial activities. Soil Biol. Biochem. 40, 487–494 (2008).

    Article  CAS  Google Scholar 

  184. 184.

    Scott, E. E., Perakis, S. S. & Hibbs, D. E. δ15N patterns of Douglas-fir and red alder riparian forests in the Oregon coast range. Forest Sci. 54, 140–147 (2008).

    Google Scholar 

  185. 185.

    Selmants, P. C. & Hart, S. C. Substrate age and tree islands influence carbon and nitrogen dynamics across a retrogressive semiarid chronosequence. Glob. Biogeochem. Cycles 22, GB1021 (2008).

    Article  CAS  Google Scholar 

  186. 186.

    Serbin, S. P., Singh, A., McNeil, B. E., Kingdon, C. C. & Townsend, P. A. Spectroscopic determination of leaf morphological and biochemical traits for northern temperate and boreal tree species. Ecol. Appl. 24, 1651–1669 (2014).

    Article  Google Scholar 

  187. 187.

    Shen, J. et al. Relationships of leaf nitrogen concentration and δ15N value in Humulus scandens with atmospheric NH3 and NO2. J. China Agricult. Univ. 15, 84–88 (2010).

    CAS  Google Scholar 

  188. 188.

    Silva, L. C. R., Gomez-Guerrero, A., Doane, T. A. & Horwath, W. R. Isotopic and nutritional evidence for species- and site-specific responses to N deposition and elevated CO2 in temperate forests. J. Geophys. Res. Biogeosci. 120, 1110–1123 (2015).

    Article  CAS  Google Scholar 

  189. 189.

    Smith, K. R., Mathias, J. M., McNeil, B. E., Peterjohn, W. T. & Thomas, R. B. Site-level importance of broadleaf deciduous trees outweighs the legacy of high nitrogen (N) deposition on ecosystem N status of Central Appalachian red spruce forests. Plant Soil 408, 343–356 (2016).

    Article  CAS  Google Scholar 

  190. 190.

    Song, M., Djagbletey, G., Nkrumah, E. E. & Huang, M. Patterns in leaf traits of leguminous and non-leguminous dominant trees along a rainfall gradient in Ghana. J. Plant Ecol. 9, 69–76 (2016).

    Article  Google Scholar 

  191. 191.

    Soper, F. M., Boutton, T. W. & Sparks, J. P. Investigating patterns of symbiotic nitrogen fixation during vegetation change from grassland to woodland using fine scale δ15N measurements. Plant Cell Environ. 38, 89–100 (2015).

    Article  CAS  PubMed  Google Scholar 

  192. 192.

    Soper, F. M. et al. Natural abundance (δ15N) indicates shifts in nitrogen relations of woody taxa along a savanna-woodland continental rainfall gradient. Oecologia 178, 297–308 (2015).

    Article  PubMed  Google Scholar 

  193. 193.

    Stephan, K., Kavanagh, K. L. & Koyama, A. Comparing the influence of wildfire and prescribed burns on watershed nitrogen biogeochemistry using 15N natural abundance in terrestrial and aquatic ecosystem components. PloS ONE 10, e0119560 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. 194.

    Szpak, P., White, C. D., Longstaffe, F. J., Millaire, J.-F. & Vasquez Sanchez, V. F. Carbon and nitrogen isotopic survey of northern Peruvian plants: baselines for paleodietary and paleoecological studies. PloS ONE 8, e53763 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. 195.

    Tanaka-Oda, A. et al. Variation in leaf and soil δ15N in diverse tree species in a lowland dipterocarp rainforest, Malaysia. Trees 30, 509–522 (2016).

    Article  CAS  Google Scholar 

  196. 196.

    Tanaka-Oda, A., Kenzo, T., Toriyama, J. & Matsuura, Y. Variability in the growth rates and foliage δ15N values of black spruce trees across a slope gradient in the Alaskan Interior. Can. J. For. Res. 46, 1483–1490 (2016).

    Article  Google Scholar 

  197. 197.

    Tang, B., Yin, C., Yang, H., Sun, Y. & Liu, Q. The coupling effects of water deficit and nitrogen supply on photosynthesis, WUE, and stable isotope composition in Picea asperata. Acta Physiol. Plant. 39, 148 (2017).

    Article  CAS  Google Scholar 

  198. 198.

    Templer, P. H. et al. Fog as a source of nitrogen for redwood trees: evidence from fluxes and stable isotopes. J. Ecol. 103, 1397–1407 (2015).

    Article  CAS  Google Scholar 

  199. 199.

    Thorpe, A. S., Perakis, S., Catricala, C. & Kaye, T. N. Nutrient limitation of native and invasive N2-fixing plants in northwest prairies. PLoS ONE 8, e84593 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. 200.

    Van der Colff, D., Dreyer, L. L., Valentine, A. & Roets, F. Comparison of nutrient cycling abilities between the invasive Acacia mearnsii and the native Virgilia divaricata trees growing sympatrically in forest margins in South Africa. S. Afr. J. Bot. 111, 358–364 (2017).

    Article  CAS  Google Scholar 

  201. 201.

    Viani, R. A. G., Rodrigues, R. R., Dawson, T. E. & Oliveira, R. S. Functional differences between woodland savannas and seasonally dry forests from south-eastern Brazil: evidence from 15N natural abundance studies. Austral Ecol. 36, 974–982 (2011).

    Article  Google Scholar 

  202. 202.

    Wang, A. et al. Variations in nitrogen-15 natural abundance of plant and soil systems in four remote tropical rainforests, southern China. Oecologia 174, 567–580 (2014).

    Article  PubMed  Google Scholar 

  203. 203.

    Wang, C. et al. Aridity threshold in controlling ecosystem nitrogen cycling in arid and semi-arid grasslands. Nat. Commun. 5, 4799 (2014).

    Article  CAS  PubMed  Google Scholar 

  204. 204.

    Wang, L. & Macko, S. A. Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell Environ. 34, 525–534 (2011).

    Article  CAS  PubMed  Google Scholar 

  205. 205.

    Wang, L., D’Odorico, P., O’Halloran, L. R., Caylor, K. & Macko, S. Combined effects of soil moisture and nitrogen availability variations on grass productivity in African savannas. Plant Soil 328, 95–108 (2010).

    Article  CAS  Google Scholar 

  206. 206.

    Wang, L., D’Odorico, P., Ries, L. & Macko, S. A. Patterns and implications of plant-soil δ13C and δ15N values in African savanna ecosystems. Quat. Res. 73, 77–83 (2010).

    Article  CAS  Google Scholar 

  207. 207.

    Wang, L., Okin, G. S., D’Odorico, P., Caylor, K. K. & Macko, S. A. Ecosystem-scale spatial heterogeneity of stable isotopes of soil nitrogen in African savannas. Landsc. Ecol. 28, 685–698 (2013).

    Article  Google Scholar 

  208. 208.

    Wang, L., Okin, G. S., Wang, J., Epstein, H. & Macko, S. A. Predicting leaf and canopy 15N compositions from reflectance spectra. Geophys. Res. Lett. 34, L02401 (2007).

    Google Scholar 

  209. 209.

    Wang, L., Shaner, P.-J. L. & Macko, S. Foliar δ15N patterns along successional gradients at plant community and species levels. Geophys. Res. Lett. 34, L16403 (2007).

  210. 210.

    Watkins, J. E. Jr, Rundel, P. W. & Cardelus, C. L. The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns. Oecologia 153, 225–232 (2007).

    Article  PubMed  Google Scholar 

  211. 211.

    Werner, C. & Máguas, C. Carbon isotope discrimination as a tracer of functional traits in a Mediterranean macchia plant community. Funct. Plant Biol. 37, 467–477 (2010).

    Article  CAS  Google Scholar 

  212. 212.

    Williams, M., Shimabokuro, Y. E. & Rastetter, E. B. LBA-ECO CD-09 Soil and Vegetation Characteristics, Tapajos National Forest, Brazil (Oak Ridge National Laboratory Distributed Active Archive Center, 2012).

  213. 213.

    Woodcock, P. et al. Assessing trophic position from nitrogen isotope ratios: effective calibration against spatially varying baselines. Naturwissenschaften 99, 275–283 (2012).

    Article  CAS  PubMed  Google Scholar 

  214. 214.

    Wu, T. & Huang, J. Effects of grazing on the δ15N values of foliage and soil in a typical steppe ecosystem in Inner Mongolia, China. J. Plant Ecol. (Chinese Version) 34, 160–169 (2010).

    CAS  Google Scholar 

  215. 215.

    Xiao, L., Yang, H., Sun, B., Li, X. & Guo, J. Stable isotope compositions of recent and fossil sun/shade leaves and implications for palaeoenvironmental reconstruction. Rev. Palaeobot. Palynol. 190, 75–84 (2013).

    Article  Google Scholar 

  216. 216.

    Yang, Y. et al. Vegetation and soil 15N natural abundance in alpine grasslands on the Tibetan Plateau: patterns and implications. Ecosystems 16, 1013–1024 (2013).

    Article  CAS  Google Scholar 

  217. 217.

    Yang, Y., Siegwolf, R. T. W. & Koerner, C. Species specific and environment induced variation of δ13C and δ15N in alpine plants. Front. Plant Sci. 6, 423 (2015).

    Google Scholar 

  218. 218.

    Yao, F. Y., Wang, G. A., Liu, X. J. & Song, L. Assessment of effects of the rising atmospheric nitrogen deposition on nitrogen uptake and long-term water-use efficiency of plants using nitrogen and carbon stable isotopes. Rapid Commun. Mass Spectrom. 25, 1827–1836 (2011).

    Article  CAS  PubMed  Google Scholar 

  219. 219.

    Ye, L. et al. Contrasting impacts of grass species on nitrogen cycling in a grazed Sudanian savanna. Acta Oecol. 63, 8–15 (2015).

    Article  Google Scholar 

  220. 220.

    Zhang, H.-Y. et al. Impacts of leguminous shrub encroachment on neighboring grasses include transfer of fixed nitrogen. Oecologia 180, 1213–1222 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. 221.

    Zhao, L. et al. The effects of short-term rainfall variability on leaf isotopic traits of desert plants in sand-binding ecosystems. Ecol. Eng. 60, 116–125 (2013).

    Article  Google Scholar 

  222. 222.

    Zmudczynska-Skarbek, K., Barcikowski, M., Zwolicki, A., Iliszko, L. & Stempniewicz, L. Variability of polar scurvygrass Cochlearia groenlandica individual traits along a seabird influenced gradient across Spitsbergen tundra. Polar Biol. 36, 1659–1669 (2013).

    Article  Google Scholar 

  223. 223.

    Sparks, J. A. & Crowley, B. E. Where did people forage in prehistoric Trinidad? Testing the utility of isotopic tools for tracking terrestrial resource use. J. Archaeol. Sci. Rep. 19, 968–978 (2018).

    Google Scholar 

  224. 224.

    Mosher, S. Carbon Isotope Discrimination and Nitrogen Isotope Values Indicate that Increased Relative Humidity from Fog Decreases Plant Water Use Efficiency in a Subtropical Montane Cloud Forest. MSc thesis, Univ. Cincinnati (2015).

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Acknowledgements

Funding for this research was in part provided by the BRIDGE Project (ANR-2006 Biodiversity Call) and from an ‘Investissement d’Avenir’ grant managed by the Agence Nationale de la Recherche (CEBA, grant no. ANR-10-LABX-0025) (J.C.R.); by the European Research Council through the Advanced Grant Project TREEPEACE (grant no. FP7-339728) and the Cluster of Excellence COTE (grant no. ANR-10-LABX-45) (S.D.); by NASA project no. NNX12AK56G and EU MSCA individual fellowship (project no. 705432) (R.G.); by COILEX (grant no. CGL2008-01671), ECOLPIN (grant no. AGL2011-24296) and EU MSCA individual fellowship (project no. 750252) (S.M.J.); and by the Russian Science Foundation (grant no. 16-14-10208) (M.M.). No funding was provided to J.M.C. or A.J.E. in support of this research.

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J.M.C. and A.J.E. conceived of the research, conducted analyses, generated figures and prepared the original draft. All authors contributed data and provided comments on manuscripts.

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Correspondence to Joseph M. Craine.

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Although J.M.C. is an owner of Jonah Ventures, a for-profit DNA sequencing company, the authors declare no competing interests in the publication of this research.

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Craine, J.M., Elmore, A.J., Wang, L. et al. Isotopic evidence for oligotrophication of terrestrial ecosystems. Nat Ecol Evol 2, 1735–1744 (2018). https://doi.org/10.1038/s41559-018-0694-0

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