Skip to main content

Advertisement

Log in

Belowground Biomass Response to Nutrient Enrichment Depends on Light Limitation Across Globally Distributed Grasslands

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Anthropogenic activities are increasing nutrient inputs to ecosystems worldwide, with consequences for global carbon and nutrient cycles. Recent meta-analyses show that aboveground primary production is often co-limited by multiple nutrients; however, little is known about how root production responds to changes in nutrient availability. At twenty-nine grassland sites on four continents, we quantified shallow root biomass responses to nitrogen (N), phosphorus (P) and potassium plus micronutrient enrichment and compared below- and aboveground responses. We hypothesized that optimal allocation theory would predict context dependence in root biomass responses to nutrient enrichment, given variation among sites in the resources limiting to plant growth (specifically light versus nutrients). Consistent with the predictions of optimal allocation theory, the proportion of total biomass belowground declined with N or P addition, due to increased biomass aboveground (for N and P) and decreased biomass belowground (N, particularly in sites with low canopy light penetration). Absolute root biomass increased with N addition where light was abundant at the soil surface, but declined in sites where the grassland canopy intercepted a large proportion of incoming light. These results demonstrate that belowground responses to changes in resource supply can differ strongly from aboveground responses, which could significantly modify predictions of future rates of nutrient cycling and carbon sequestration. Our results also highlight how optimal allocation theory developed for individual plants may help predict belowground biomass responses to nutrient enrichment at the ecosystem scale across wide climatic and environmental gradients.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Aerts RR, Boog GA, Van Der Aart PJM. 1991. The relation between above- and belowground biomass allocation patterns and competitive ability. Oecologia 87:551–9.

    CAS  PubMed  Google Scholar 

  • Anderson JM. 1991. The effects of climate change on decomposition processes in grassland and coniferous forests. Ecological Applications 1:326–47.

    CAS  PubMed  Google Scholar 

  • Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ. 1999. Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Functional Ecology 13:650–60.

    Google Scholar 

  • Bledsoe CS, Fahey TJ, Day FP, Ruess RW. 1999. Measurement of static root parameters: biomass, length, and distribution in the soil profile. Soils Methods for Long-Term Ecological Research. New York: Oxford University Press. p 413–36.

    Google Scholar 

  • Bloom AJ, Chapin FS, Mooney HA. 1985. Resource limitation in plants—an economic analogy. Annual Reviews of Ecology and Systematics 16:363–92.

    Google Scholar 

  • Blume E, Bischoff M, Reichert JM, Moorman T, Konopka A, Turco RF. 2002. Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season. Applied Soil Ecology 20:171–81.

    Google Scholar 

  • Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B. 2010. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications 20:30–59.

    CAS  PubMed  Google Scholar 

  • Bolker B. 2008. Chapter 4: Distributions, in: Ecological Models and Data in R. Princeton University Press, pp 103–146.

  • Borer ET, Harpole WS, Adler PB, Lind EM, Orrock JL, Seabloom EW, Smith MD. 2014a. Finding generality in ecology: a model for globally distributed experiments. Methods in Ecology and Evolution 5:65–73.

    Google Scholar 

  • Borer ET, Seabloom EW, Gruner DS, Harpole WS, Hillebrand H, Lind EM, Adler PB, Alberti J, Anderson TM, Bakker JD, Biederman L, Blumenthal D, Brown CS, Brudvig LA, Buckley YM, Cadotte M, Chu C, Cleland EE, Crawley MJ, Daleo P, Damschen EI, Davies KF, DeCrappeo NM, Du G, Firn J, Hautier Y, Heckman RW, Hector A, HilleRisLambers J, Iribarne O, Klein JA, Knops JMH, La Pierre KJ, Leakey ADB, Li W, MacDougall AS, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Mortensen B, O’Halloran LR, Orrock JL, Pascual J, Prober SM, Pyke DA, Risch AC, Schuetz M, Smith MD, Stevens CJ, Sullivan LL, Williams RJ, Wragg PD, Wright JP, Yang LH. 2014b. Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–20.

    CAS  PubMed  Google Scholar 

  • Cleland EE, Harpole WS. 2010. Nitrogen enrichment and plant communities. Annals of the New York Academy of Sciences 1195:46–61.

    CAS  PubMed  Google Scholar 

  • Craine JM, Wedin DA, Chapin FS, Reich PB. 2003. Relationship between the structure of root systems and resource use for 11 North American grassland plants. Plant Ecology 165:85–100.

    Google Scholar 

  • Dybzinski R, Mcnickle G. 2013. Game theory and plant ecology. Ecology Letters 16:545–55.

    PubMed  Google Scholar 

  • Eilers KG, Debenport S, Anderson S, Fierer N. 2012. Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biology & Biochemistry 50:58–65.

    CAS  Google Scholar 

  • Elser JJ, Bracken ME, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine, and terrestrial ecosystems. Ecology Letters 10:1115–211.

    Google Scholar 

  • Falkowski P, Scholes R, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Högberg P, Linder S, Mackenzie FT. 2000. The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291–6.

    CAS  PubMed  Google Scholar 

  • Fay PA, Prober SM, Harpole WS, Knops JMH, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD, Adler P, Blumenthal DM, Buckley YM, Chu C, Cleland EE, Collins SL, Davies KF, Du G, Feng X, Firn J, Gruner DS, Hagenah N, Hautier Y, Heckman RW, Jin VL, Kirkman KP, Klein J, Ladwig LM, Li Q, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Risch AC, Schütz M, Stevens CJ, Wedin DA, Yang YH. 2015. Grassland productivity limited by multiple nutrients. Nature Plants 1:15080.

    CAS  PubMed  Google Scholar 

  • Field CB, Lobell DB, Peters HA, Chiariello NR. 2007. Feedbacks of terrestrial ecosystems to climate change. Annual Review of Environment and Resources 32:1–29.

    Google Scholar 

  • Follett R, Reed D. 2010. Soil carbon sequestration in grazing lands: societal benefits and policy implications. Rangeland Ecology Management 63:4–15.

    Google Scholar 

  • Fox J, Weisberg S. 2011. An R Companion to Applied Regression. 2nd edn. California: Thousand Oaks.

    Google Scholar 

  • Friedlingstein P, Joel G, Field CB, Fung IY. 1999. Toward an allocation scheme for global terrestrial carbon models. Global Change Biology 5:755–70.

    Google Scholar 

  • Gill RA, Kelly RH, Parton WJ, Day KA, Jackson RB, Morgan JA, Scurlock JMO, Tieszen LL, Castle JV, Ojima DS, Zhang XS. 2002. Using simple environmental variables to estimate belowground productivity in grasslands. Global Ecology and Biogeography 11:79–86.

    Google Scholar 

  • Gleeson SK, Tilman D. 1992. Plant allocation and the multiple limitation hypothesis. American Naturalist 139:1322–43.

    Google Scholar 

  • Goldberg, DE. 1990. Components of resource competition in plant communities. In: Perspectives on plant competition, pp. 27–49.

  • Grime JP, Campbell BD, Mackey JMI, Crick JC. 1991. Root plasticity, nitrogen capture and competitive ability. In: Atkinson D, Ed. Plant Root Growth: an Ecological Perspective. Oxford: Blackwell.

    Google Scholar 

  • Gurevitch J, Wilson P, Stone JL, Tees P, Stoutenburgh RJ. 1990. Competition among old-field perennials at different levels of soil fertility and available space. Journal of Ecology 78:727–44.

    Google Scholar 

  • Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE. 2011. Nutrient co-limitation of primary producer communities. Ecology Letters 14:852–62.

    PubMed  Google Scholar 

  • Hautier Y, Niklaus PA, Hector A. 2009. Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–8.

    CAS  PubMed  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25:1965–78.

    Google Scholar 

  • Hooper DU, Johnson L. 1999. Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–93.

    CAS  Google Scholar 

  • Hui DF, Jackson RB. 2006. Geographical and interannual variability in biomass partitioning in grassland ecosystems: a synthesis of field data. New Phytologist 169:85–93.

    CAS  PubMed  Google Scholar 

  • Iversen CM, McCormack ML, Powell AS, Blackwood CB, Freschet GT, Kattge J, Roumet C, Stover DB, Soudzilovskaia NA, Valverde-Barrantes OJ, Bodegom PM. 2017. A global Fine-Root Ecology Database to address belowground challenges in plant ecology. New Phytologist 215:15–26.

    PubMed  Google Scholar 

  • Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411.

    CAS  PubMed  Google Scholar 

  • Jackson RB, Schenk HJ, Jobbágy EG, Canadell J, Colello GD, Dickinson RE, Field CB, Friedlingstein P, Heimann M, Hibbard K, Kicklighter DW. 2000. Belowground consequences of vegetation change and their treatment in models. Ecological Applications 10:470–83.

    Google Scholar 

  • Jastrow JD. 1996. Soil aggregate formation and the accrual of particulate and mineral-associated organic matter. Soil Biology & Biochemistry 28:665–76.

    CAS  Google Scholar 

  • Jobbagy EG, Jackson RB. 2000. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecological Applications 10:423–36.

    Google Scholar 

  • Jobbagy EG, Jackson RB. 2001. The distribution of soil nutrients with depth: Global patterns and the imprint of plants. Biogeochemistry 53:51–77.

    CAS  Google Scholar 

  • LeBauer DS, Treseder KK. 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–9.

    PubMed  Google Scholar 

  • Lee M, Manning P, Rist J, Power SA, Marsh C. 2010. A global comparison of grassland biomass responses to CO2 and nitrogen enrichment. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365:2047–56.

    CAS  PubMed  Google Scholar 

  • Leith HHF. 1978. Primary productivity in ecosystems: Comparative analysis of global patterns. In: Leith HFH, ed. Patterns of primary production in the biosphere. Stroudberg, PA USA., Dowden, Hutchinson and Ross. pp. 342

  • Lind EM, Borer E, Seabloom E, Adler P, Bakker JD, Blumenthal DM, Crawley M, Davies K, Firn J, Gruner DS, Harpole WS. 2013. Life-history constraints in grassland plant species: a growth-defence trade-off is the norm. Ecology Letters 16:513–21.

    PubMed  Google Scholar 

  • Liu L, Greaver TL. 2010. A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecology Letters 13:819–28.

    PubMed  Google Scholar 

  • Lu M, Zhou X, Luo Y, Yang Y, Fang C, Chen J, Li B. 2011. Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agriculture, Ecosystems & Environment 140:234–44.

    CAS  Google Scholar 

  • Mack MC, Schuur EA, Bret-Harte MS, Shaver GR, Chapin FS. 2004. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–3.

    CAS  PubMed  Google Scholar 

  • McCarthy MC, Enquist BJ. 2007. Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Functional Ecology 21:713–20.

    Google Scholar 

  • Mueller KE, Hobbie SE, Tilman D, Reich PB. 2013. Effects of plant diversity, N fertilization, and elevated carbon dioxide on grassland soil N cycling in a long-term experiment. Global Change Biology 19:1249–61.

    PubMed  Google Scholar 

  • Michaletz ST, Cheng D, Kerkhoff AJ, Enquist BJ. 2014. Convergence of terrestrial plant production across global climate gradients. Nature 512:39–43.

    CAS  PubMed  Google Scholar 

  • Mokany K, Raison RJ, Prokushkin AS. 2006. Critical analysis of root : shoot ratios in terrestrial biomes. Global Change Biology 12:84–96.

    Google Scholar 

  • Nadelhoffer KJ, Aber JD, Melillo JM. 1985. Fine roots, net primary production, and soil nitrogen availability: a new hypothesis. Ecology 66:1377–90.

    Google Scholar 

  • Norby RJ, Luo Y. 2004. Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytologist 162:281–93.

    Google Scholar 

  • Olff H. 1992. Effects of light and nutrient availability on dry matter and N allocation in six successional grassland species. Oecologia 89:412–21.

    PubMed  Google Scholar 

  • Pinheiro J, Bates D, Debroy S, Sarkar D, R Core Development Team. 2013. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L. 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193:30–50.

    CAS  PubMed  Google Scholar 

  • Core Team R. 2017. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Rasse DP, Rumpel C, Dignac MF. 2005. Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant and Soil 269:341–56.

    CAS  Google Scholar 

  • Reynolds HL, D’Antonio C. 1996. The ecological significance of plasticity in root weight ratio in response to nitrogen: Opinion. Plant and Soil 185:75–97.

    CAS  Google Scholar 

  • Reich PB. 2002. Root-shoot relations: optimality in acclimation and adaptation or the ‘Emperor’s New Clothes’. In: Plant Roots: The Hidden Half, pp. 205–220.

  • Reich PB, Luo Y, Bradford JB, Poorter H, Perry CH, Oleksyn J. 2014. Temperature drives global patterns in forest biomass distribution in leaves, stems, and roots. Proceedings of National Academy of Sciences 111:13721–6.

    CAS  Google Scholar 

  • Schenk HJ, Jackson RB. 2002. The global biogeography of roots. Ecological Monographs 72:311–28.

    Google Scholar 

  • Scurlock JMO, Hall DO. 1998. The global carbon sink: a grassland perspective. Global Change Biology 4:229–33.

    Google Scholar 

  • Scurlock JMO, Johnson K, Olson RJ. 2002. Estimating net primary productivity from grassland biomass dynamics measurements. Global Change Biology 8:736–53.

    Google Scholar 

  • Sims PL, Singh JS. 1978. The structure and function of ten western North American grasslands: III. Net primary production, turnover and efficiencies of energy capture and water use. Journal of Ecology 66:573–97.

    Google Scholar 

  • Smithwick EA, Lucash MS, Mccormack ML, Sivandran G. 2014. Improving the representation of roots in terrestrial models. Ecological Modelling 291:193–204.

    CAS  Google Scholar 

  • Sposito G. 1989. The chemistry of soils. New York: Oxford University Press.

    Google Scholar 

  • Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S. 2005. Functional-and abundance-based mechanisms explain diversity loss due to N fertilization. Proceedings of the National Academy of Sciences of the United States of America 102:4387–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thornley JHM. 1972. A balanced quantitative model for root: shoot ratios in vegetative plants. Annals of Botany 36:431–41.

    Google Scholar 

  • Tilman D, Wedin D. 1991. Plant traits and resource reduction for five grasses growing on a nitrogen gradient. Ecology 72:685–700.

    Google Scholar 

  • Warton DI, Hui FK. 2011. The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10.

    PubMed  Google Scholar 

  • Weiner J. 2004. Allocation, plasticity and allometry in plants. Perspectives in Plant Ecology, Evolution and Systematics 6:207–15.

    Google Scholar 

  • Wilson JB. 1988. A review of evidence on the control of shoot: root ratio, in relation to models. Annals of Botany 61:433–49.

    Google Scholar 

  • Woodward FI, Osborne CP. 2000. The representation of root processes in models addressing the responses of vegetation to global change. New Phytologist 147:223–32.

    CAS  Google Scholar 

  • Xia J, Wan S. 2008. Global response patterns of terrestrial plant species to nitrogen addition. New Phytologist 179:428–39.

    CAS  PubMed  Google Scholar 

  • Yang Y, Fang J, Ji C, Han W. 2009. Above- and belowground biomass allocation in Tibetan grasslands. Journal of Vegetation Science 20:177–84.

    Google Scholar 

  • Yuan ZY, Chen HYH. 2012. A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proceedings of the Royal Society of London B: Biological Sciences 279:3796–802.

    CAS  Google Scholar 

  • Zeng DH, Li LJ, Fahey TJ, Yu ZY, Fan ZP, Chen FS. 2010. Effects of nitrogen addition on vegetation and ecosystem carbon in a semi-arid grassland. Biogeochemistry 98:185–93.

    CAS  Google Scholar 

  • Zomer RJ, Trabucco A, Bossio DA, van Straaten O, Verchot LV. 2008. Climate change mitigation: A spatial analysis of global land suitability for Clean Development Mechanism afforestation and reforestation. Agriculture, Ecosystems & Environment 126:67–80.

    Google Scholar 

Download references

Acknowledgements

This work was generated using data from the Nutrient Network (http://www.nutnet.org) experiment, funded at the site-scale by individual researchers. Coordination and data management have been supported by funding to E. Borer and E. Seabloom from the National Science Foundation Research Coordination Network (NSF-DEB-1042132) and Long Term Ecological Research (NSF-DEB-1234162 to Cedar Creek LTER) programs, and the Institute on the Environment (DG-0001-13). We also thank the Minnesota Supercomputer Institute for hosting project data and the Institute on the Environment for hosting Network meetings. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elsa E. Cleland.

Additional information

Author Contributions EEC analyzed the data and wrote the paper with input from all co-authors. All co-authors contributed to data collection.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2017 kb)

Supplementary material 2 (XLSX 70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cleland, E.E., Lind, E.M., DeCrappeo, N.M. et al. Belowground Biomass Response to Nutrient Enrichment Depends on Light Limitation Across Globally Distributed Grasslands. Ecosystems 22, 1466–1477 (2019). https://doi.org/10.1007/s10021-019-00350-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-019-00350-4

Keywords

Navigation