Abstract
Background and aims
Increased atmospheric nitrogen (N) deposition under global climate change is known to reduce plant species richness in terrestrial ecosystems, with potentially important implications for ecosystem function and processes. However, knowledge gaps remain in our understanding of how N deposition affects the different aspects of plant community diversity (e.g., species, functional, and phylogenetic diversity) and how these impacts propagate to affect ecosystem multifunctionality.
Methods
Here, we investigated plant species, functional and phylogenetic diversity along a nitrogen gradient (0, 0.5, 1, 3, 6, 12, 24, 48 g N m−2 yr−1) in a desert steppe. In addition, ecosystem multifunctionality was determined by eight functions to assess the relationship between plant community diversity and ecosystem multifunctionality.
Results
We showed that N addition increased plant functional diversity, but not species and phylogenetic diversity. Along the nitrogen addition gradient, the ecosystem multifunctionality increased first and then decreased which peaked at an addition rate of 24 g·m−2·yr−1. Importantly, functional diversity was positively correlated with ecosystem multifunctionality. Furthermore, the structural equation model showed that N addition increased ecosystem multifunctionality both directly and by increasing functional diversity.
Conclusion
The positive relationships between MF and functional diversity suggest that the change and distribution of plant functional traits are beneficial for complementary utilization of N, thus maintaining ecosystem multifunctionality. The superiority of functional diversity over species and phylogenetic diversity highlights an important role of functional diversity in regulating ecosystem functioning to N addition.
Similar content being viewed by others
Data availability
All data included in this study are available upon request by contact with the corresponding author.
References
Angelini C, van der Heide T, Griffin JN, Morton JP, Derksen-Hooijberg M, Lamers LPM, Smolders AJP, Silliman BR (2015) Foundation species' overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes. P Roy Soc B-Biol Sci 282. https://doi.org/10.1098/Rspb.2015.0421
Antiqueira PAP, Petchey OL, Romero GQ (2018) Warming and top predator loss drive ecosystem multifunctionality. Ecol Lett 21:72–82. https://doi.org/10.1111/ele.12873
Bai YF, Wu JG, Clark CM, Naeem S, Pan QM, Huang JH, Zhang LX, Han XG (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Global Change Biol 16:358–372. https://doi.org/10.1111/j.1365-2486.2009.01950.x
Bastlova D, Cizkova H, Bastl M, Kvet J (2004) Growth of Lythrum salicaria and Phragmites australis plants originating from a wide geographical area: response to nutrient and water supply. Glob Ecol Biogeogr 13:259–271. https://doi.org/10.1111/j.1466-822X.2004.00089.x
Bowker MA, Maestre FT, Mau RL (2013) Diversity and patch-size distributions of biological soil crusts regulate dryland ecosystem multifunctionality. Ecosystems 16:923–933. https://doi.org/10.1007/s10021-013-9644-5
Bradford MA, Wood SA, Bardgett RD, Black HIJ, Bonkowski M, Eggers T, Grayston SJ, Kandeler E, Manning P, Setala H, Jones TH (2014) Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. P Natl Acad Sci USA 111:14478–14483. https://doi.org/10.1073/pnas.1413707111
Brandt AJ, Seabloom EW, Cadotte MW (2019) Nitrogen alters effects of disturbance on annual grassland community diversity: Implications for restoration. J Ecol 107:2054–2064. https://doi.org/10.1111/1365-2745.13245
Britton AJ, Mitchell RJ, Fisher JM, Riach DJ, Taylor AFS (2018) Nitrogen deposition drives loss of moss cover in alpine moss-sedge heath via lowered C: N ratio and accelerated decomposition. New Phytol 218:470–478. https://doi.org/10.1111/nph.15006
Byrnes JEK, Gamfeldt L, Isbell F, Lefcheck JS, Griffin JN, Hector A, Cardinale BJ, Hooper DU, Dee LE, Duffy JE (2014) Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol Evol 5:111–124. https://doi.org/10.1111/2041-210x.12143
Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. P Natl Acad Sci USA 105:17012–17017. https://doi.org/10.1073/pnas.0805962105
Casanoves F, Pla L, Di Rienzo JA, Diaz S (2011) FDiversity: a software package for the integrated analysis of functional diversity. Methods Ecol Evol 2:233–237. https://doi.org/10.1111/j.2041-210X.2010.00082.x
Chalcraft DR, Cox SB, Clark C, Cleland EE, Suding KN, Weiher E, Pennington D (2008) Scale-dependent responses of plant biodiversity to nitrogen enrichment. Ecology 89:2165–2171. https://doi.org/10.1890/07-0971.1
Chen Q, Wang YD, Zou CB, Wang ZL (2017) Aboveground biomass invariance masks significant belowground productivity changes in response to salinization and nitrogen loading in reed marshes. Wetlands 37:985–995. https://doi.org/10.1007/s13157-017-0932-2
Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715. https://doi.org/10.1038/nature06503
Cui HY, Sun W, Delgado-Baquerizo M, Song WZ, Ma JY, Wang KY, Ling XL (2020) Phosphorus addition regulates the responses of soil multifunctionality to nitrogen over-fertilization in a temperate grassland. Plant Soil. https://doi.org/10.1007/s11104-020-04620-2
de Vries W, Solberg S, Dobbertin M, Sterba H, Laubhann D, van Oijen M, Evans C, Gundersen P, Kros J, Wamelink GWW, Reinds GJ, Sutton MA (2009) The impact of nitrogen deposition on carbon sequestration by European forests and heathlands. Forest Ecol Manag 258:1814–1823. https://doi.org/10.1016/j.foreco.2009.02.034
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7. https://doi.org/10.1038/Ncomms10541
Dias T, Crous CJ, Ochoa-Hueso R, Manrique E, Martins-Loucao MA, Cruz C (2020) Nitrogen inputs may improve soil biocrusts multifunctionality in dryland ecosystems. Soil Biol Biochem 149. https://doi.org/10.1016/j.soilbio.2020.107947
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity-ecosystem-function relationships. Ecology 92:1573–1581. https://doi.org/10.1890/10-1245.1
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320:889–892. https://doi.org/10.1126/science.1136674
Goulding KWT, Bailey NJ, Bradbury NJ, Hargreaves P, Howe M, Murphy DV, Poulton PR, Willison TW (1998) Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytol 139:49–58. https://doi.org/10.1046/j.1469-8137.1998.00182.x
Grime JP (2006) Trait convergence and trait divergence in herbaceous plant communities: Mechanisms and consequences. J Veg Sci 17:255–260. https://doi.org/10.1111/j.1654-1103.2006.tb02444.x
Guo X, Zuo X, Yue P, Li X, Hu Y, Chen M, Yu Q (2022) Direct and indirect effects of precipitation change and nutrients addition on desert steppe productivity in inner mongolia, northern china. Plant Soil 471:527–540
Harpole WS, Tilman D (2007) Grassland species loss resulting from reduced niche dimension. Nature 446:791–793. https://doi.org/10.1038/nature05684
Harpole WS, Sullivan LL, Lind EM, Firn J, Adler PB, Borer ET, Chase J, Fay PA, Hautier Y, Hillebrand H, MacDougallm AS, Seabloom EW, Williams R, Bakker JD, Cadotte MW, Chaneton EJ, Chu CJ, Cleland EE, D’Antonio C, Davies KF, Gruner DS, Hagenah N, Kirkman K, Knops JMH, La Pierre KJ, McCulley RL, Moore JL, Morgan JW, Prober SM, Risch AC, Schuetz M, Stevens CJ, Wragg PD (2016) Addition of multiple limiting resources reduces grassland diversity. Nature 537:93–96. https://doi.org/10.1038/nature19324
Harpole WS, Sullivan LL, Lind EM, Firn J, Adler PB, Borer ET, Chase J, Fay PA, Hautier Y, Hillebrand H, MacDougall AS, Seabloom EW, Bakker JD, Cadotte MW, Chaneton EJ, Chu C, Hagenah N, Kirkman K, La Pierre KJ, Moore JL, Morgan JW, Prober SM, Risch AC, Schuetz M, Stevens CJ (2017) Out of the shadows: multiple nutrient limitations drive relationships among biomass, light and plant diversity. Funct Ecol 31:1839–1846. https://doi.org/10.1111/1365-2435.12967
Hautier Y, Niklaus PA, Hector A (2009) Competition for Light Causes Plant Biodiversity Loss After Eutrophication. Science 324:636–638. https://doi.org/10.1126/science.1169640
Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188-U6. https://doi.org/10.1038/nature05947
Helmus MR, Bland TJ, Williams CK, Ives AR (2007) Phylogenetic measures of biodiversity. Am Nat 169:E68–E83. https://doi.org/10.1086/511334
Hutchinson GE (1957) Concluding remarks. Quant Biol 22:415–427. https://doi.org/10.1002/9780470866795.ch10
Kominoski JS, Rosemond AD, Benstead JP, Gulis V, Manning DWP (2018) Experimental nitrogen and phosphorus additions increase rates of stream ecosystem respiration and carbon loss. Limnol Oceanogr 63:22–36. https://doi.org/10.1002/lno.10610
Krizek DT, Kramer GF, Mirecki RM (1997) Influence of UV-B radiation and putrescine on shoot and root growth of cucumber seedlings grown in nutrient solution. J Plant Nutr 20:613–623. https://doi.org/10.1080/01904169709365281
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
Lavorel S, Grigulis K (2012) How fundamental plant functional trait relationships scale-up to trade-offs and synergies in ecosystem services. J Ecol 100:128–140. https://doi.org/10.1111/j.1365-2745.2011.01914.x
Lefcheck JS, Byrnes JEK, Isbell F, Gamfeldt L, Griffin JN, Eisenhauer N, Hensel MJS, Hector A, Cardinale BJ, Duffy JE (2015) Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat Commun 6. https://doi.org/10.1038/Ncomms7936
Li S, Dong SK, Shen H, Han YH, Zhang J, Xu YD, Gao XX, Yang MY, Li Y, Zhao ZZ, Liu SL, Zhou HK, Dong QM, Yeomans JC (2019) Different responses of multifaceted plant diversities of alpine meadow and alpine steppe to nitrogen addition gradients on Qinghai-Tibetan Plateau. Sci Total Environ 688:1405–1412. https://doi.org/10.1016/j.scitotenv.2019.06.211
Li M, Zhang XZ, Niu B, He YT, Wang XT, Wu JS (2020) Changes in plant species richness distribution in Tibetan alpine grasslands under different precipitation scenarios. Glob Ecol Conserv 21. https://doi.org/10.1016/j.gecco.2019.e00848
Liu XJ, Duan L, Mo JM, Du EZ, Shen JL, Lu XK, Zhang Y, Zhou XB, He CN, Zhang FS (2011) Nitrogen deposition and its ecological impact in China: an overview. Environ Pollut 159:2251–2264. https://doi.org/10.1016/j.envpol.2010.08.002
Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. https://doi.org/10.1038/nature11917
Luo G, Rensing C, Chen H, Liu M, Wang M, Guo S, Ling N, Shen Q (2018) Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Funct Ecol 32:1103–1116. https://doi.org/10.1111/1365-2435.13039
Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R (2012) Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100:317–330. https://doi.org/10.1111/j.1365-2745.2011.01918.x
Mason NWH, Mouillot D, Lee WG, Wilson JB (2010) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118. https://doi.org/10.1111/j.0030-1299.2005.13886.x
Matson P, Lohse KA, Hall SJ (2002) The globalization of nitrogen deposition: Consequences for terrestrial ecosystems. Ambio 31:113–119. https://doi.org/10.1639/0044-7447(2002)031
Miao RH, Ma J, Liu YZ, Liu YC, Yang ZL, Guo MX (2019) Variability of aboveground litter inputs alters soil carbon and nitrogen in a coniferous-broadleaf mixed forest of central China. Forests 10. https://doi.org/10.3390/F10020188
Olff H, Pegtel DM (1994) Characterisation of the type and extent of nutrient limitation in grassland vegetation using a bioassay with intact sods. Plant Soil 163:217–224. https://doi.org/10.1007/bf00007971
Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quetier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/BT12225
Pilkington MG, Caporn S, Carroll JA, Cresswell N, Lee JA, Ashenden TW, Brittain SA, Reynolds B, Emmett BA (2005) Effects of increased deposition of atmospheric nitrogen on an upland moor: leaching of N species and soil solution chemistry. Environ Pollut 135:29–40. https://doi.org/10.1016/j.envpol.2004.10.016
Polley HW, Isbell FI, Wilsey BJ (2013) Plant functional traits improve diversity-based predictions of temporal stability of grassland productivity. Oikos 122:1275–1282. https://doi.org/10.1111/j.1600-0706.2013.00338.x
Ratcliffe S, Wirth C, Jucker T, van der Plas F, Scherer-Lorenzen M, Verheyen K, Allan E, Benavides R, Bruelheide R, Ohse B, Paquette A, Ampoorter E, Bastias CC, Bauhus J, Bonal B et al (2017) Biodiversity and ecosystem functioning relations in European forests depend on environmental context. Ecol Lett 20:1414–1426. https://doi.org/10.1111/ele.12849
Ren Z, Li Q, Chu C, Zhao L, Zhang J, Ai D, Yang Y, Wang G (2010) Effects of resource additions on species richness and ANPP in an alpine meadow community. J Plant Ecol 3:25–31. https://doi.org/10.1093/jpe/rtp034
Ren HY, Xu ZW, Huang JH, Clark C, Chen SP, Han XG (2011) Nitrogen and water addition reduce leaf longevity of steppe species. Ann Bot-London 107:145–155. https://doi.org/10.1093/aob/mcq219
Roth T, Kohli L, Rihm B, Amrhein V, Achermann B (2015) Nitrogen deposition and multi-dimensional plant diversity at the landscape scale. Roy Soc Open Sci 2. https://doi.org/10.1098/Rsos.150017
Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879. https://doi.org/10.1126/science.1094678
van der Plas F (2019) Biodiversity and ecosystem functioning in naturally assembled communities. Biol Rev https://doi.org/10.1111/brv.12499
van Paassen JG, Britton AJ, Mitchell RJ, Street LE, Johnson D, Coupar A, Woodin SJ (2020) Legacy effects of nitrogen and phosphorus additions on vegetation and carbon stocks of upland heaths. New Phytol 228:226–237. https://doi.org/10.1111/nph.16671
Venail P, Gross K, Oakley TH, Narwani A, Allan E, Flombaum P, Isbell F, Joshi J, Reich PB, Tilman D, van Ruijven J, Cardinale BJ (2015) Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct Ecol 29:615–626. https://doi.org/10.1111/1365-2435.12432
Wu X, Wang X, Tang Z, Shen Z, Zheng C, Xia X, Fang J (2015) The relationship between species richness and biomass changes from boreal to subtropical forests in China. Ecography 38:602–613. https://doi.org/10.1111/ecog.00940
Xu ZW, Li MH, Zimmermann NE, Li SP, Li H, Ren HY, Sun H, Han XG, Jiang Y, Jiang L (2018) Plant functional diversity modulates global environmental change effects on grassland productivity. J Ecol 106:1941–1951. https://doi.org/10.1111/1365-2745.12951
Yan Y, Zhang Q, Buyantuev A, Liu Q, Niu J (2020) Plant functional β diversity is an important mediator of effects of aridity on soil multifunctionality. Sci Total Environ 726:138529. https://doi.org/10.1016/j.scitotenv.2020.138529
Yang X, Li GY, Li SP, Xu QN, Wang PD, Song HH, Sun DY, Zhong MX, Zhou ZX, Song J, Ru JY, Wan SQ, Jiang L (2019) Resource addition drives taxonomic divergence and phylogenetic convergence of plant communities. J Ecol 107:2121–2132. https://doi.org/10.1111/1365-2745.13253
Yue K, Jarvie S, Senior AM, Van Meerbeek K, Peng Y, Ni XY, Wu FZ, Svenning JC (2020) Changes in plant diversity and its relationship with productivity in response to nitrogen addition, warming and increased rainfall. Oikos 129:939–952. https://doi.org/10.1111/oik.07006
Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, Aarssen L, Bertin RI, Calaminus A, Govaerts R, Hemmings F, Leishman MR, Oleksyn J, Soltis PS, Swenson NG, Warman L, Beaulieu JM (2014) Three keys to the radiation of angiosperms into freezing environments (2014). Nature 514:394–394. https://doi.org/10.1038/nature13842
Zavaleta ES, Pasari JR, Hulvey KB, Tilman GD (2010) Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. P Natl Acad Sci USA 107:1443–1446. https://doi.org/10.1073/pnas.0906829107
Zhang NL, Wan SQ, Li LH, Bi J, Zhao MM, Ma KP (2008) Impacts of urea N addition on soil microbial community in a semi-arid temperate steppe in northern China. Plant Soil 311:19–28. https://doi.org/10.1007/s11104-008-9650-0
Zhang DY, PengYF LF, Yang GB, Wang J, Yu JC, Zhou GY, Yang YH (2019) Trait identity and functional diversity co-drive response of ecosystem productivity to nitrogen enrichment. J Ecol 107:2402–2414. https://doi.org/10.1111/1365-2745.13184
Funding
This work was financially supported by the Second Tibetan Plateau Scientific Expedition and Research program (No. 2019QZKK0305) and National Natural Science Foundation of China (No. 42071140).
Author information
Authors and Affiliations
Contributions
Xiaoan Zuo designed this experiment; Aixia Guo, Xiangyun Li, Ping Yue, Shenglong Zhao and Peng Lv contributed significantly to analysis and manuscript preparation; Ya Hu performed the data analyses and wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Responsible Editor: Long Li.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hu, Y., Guo, A., Li, X. et al. Multi-trait functional diversity predicts ecosystem multifunctionality under nitrogen addition in a desert steppe. Plant Soil 491, 33–44 (2023). https://doi.org/10.1007/s11104-022-05731-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05731-8