Abstract
Purpose
Herbivore grazing and nitrogen (N) input may alter the multiple ecosystem functions (i.e., multifunctionality, hereafter) associated with carbon (C), N, and phosphorus (P) cycling. Most studies on variations in plant diversity, soil biotic or abiotic factors, and linkages to ecosystem functions have focused on grazing or N enrichment alone. Few studies have combined these two factors to explore the role of plant resource stoichiometry (C:N:P ratios) in ecosystem multifunctionality (EMF) control. Here, we evaluated the direct and indirect effects of stocking rate (0, 2.7, 5.3, and 8.7 sheep ha− 1) and N addition rate (0, 5, 10, and 20 g N m− 2 yr− 1) on a range of ecosystem functions and EMF via changing plant diversity, soil pH and plant resource stoichiometry in a typical steppe on the Loess Plateau.
Results
We found that increasing stocking rate and interaction between grazing and N addition significantly decreased EMF, while increasing N addition rate significantly promoted EMF. Grazing decreased soil NH4+-N, soil NO3−-N, aboveground biomass, and plant C, N, and P pools, but increased soil total N and P at 8.7 and 5.3 sheep ha− 1, respectively. N addition increased soil NH4+-N, NO3−-N, and total P. Plant aboveground biomass, and plant C, N, and P pools increased at the lower N addition rate (≤ 5 g N m− 2 yr− 1) under grazing. The structural equation models indicated that (1) EMF was driven by the direct effects of grazing and the indirect effects of grazing on plant resource stoichiometry and soil pH; (2) EMF increased with increasing N addition rates, but such positive response of EMF to increasing N addition rates was alleviated at high levels of plant resource stoichiometry and diversity; and (3) the indirect effects of plant diversity induced by grazing and N addition had moderate effects on EMF via the variations of plant resource stoichiometry.
Conclusions
This study demonstrated grazing and N addition had contrasting effects on ecosystem multifunctionality in a typical steppe, and highlighted the capacity of plant diversity in balancing plant elements that serve as a key mechanism in the maintenance of EMF in response to intensive grazing and N enrichment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Abbas M, Ebeling A, Oelmann Y et al (2013) Biodiversity effects on plant stoichiometry. PLoS ONE 8:e58179. https://doi.org/10.1371/journal.pone.0058179
Allan E, Manning P, Alt F et al (2015) Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol Lett 18:834–843. https://doi.org/10.1111/ele12469
Archer E (2018) rfPermute: Estimate permutation p-values for random forest. Importance Metrics. R package version 2.5. https://cran.rstudio.com/web/packages/rfPermute/. Accessed Mar 10 2022
Baert JM, Eisenhauer N, Janssen CR, De Laender F (2018) Biodiversity effects on ecosystem functioning respond unimodally to environmental stress. Ecol Lett 21:1191–1199. https://doi.org/10.1111/ele.13088
Bobbink R, Hicks K, Galloway J et al (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59. https://doi.org/10.1890/08-1140.1
Borer ET, Harpole WS, Adler PB et al (2020) Nutrients cause grassland biomass to outpace herbivory. Nat Commun 11:6036. https://doi.org/10.1038/s41467-020-19870-y
Borer ET, Seabloom EW, Gruner DS et al (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520. https://doi.org/10.1038/nature13144
Breiman L (2001) Random forests. Mach Learn 45:5–32
Byrnes JEK, Gamfeldt L, Isbell F et al (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
Chen D, Xing W, Lan Z et al (2019) Direct and indirect effects of nitrogen enrichment on soil organisms and carbon and nitrogen mineralization in a semi-arid grassland. Funct Ecol 33:175–187. https://doi.org/10.1111/1365-2435.13226
Cui H, Sun W, Delgado-Baquerizo M et al (2020) Contrasting effects of N fertilization and mowing on ecosystem multifunctionality in a meadow steppe. Soil Ecol Lett 2:268–280. https://doi.org/10.1007/s42832-020-0046-2
Cutler DR, Edwards TC, Beard KH et al (2007) Random forests for classification in ecology. Ecology 88(11):2783–2792. https://doi.org/10.1890/07-0539.1
Daufresne T (2021) A consumer-driven recycling theory for the impact of large herbivores on terrestrial ecosystem stoichiometry. Ecol Lett 24:2598–2610. https://doi.org/10.1111/ele.13876
Delgado-Baquerizo M, Reich PB, Trivedi C et al (2020) Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol 4:210–220. https://doi.org/10.1038/s41559-019-1084-y
Dib V, Pires APF, Nova CC et al (2020) Biodiversity-mediated effects on ecosystem functioning depend on the type and intensity of environmental disturbances. Oikos 129:433–443. https://doi.org/10.1111/oik06768
Frank DA, Wallen RL, Hamilton EW et al (2018) Manipulating the system: How large herbivores control bottom-up regulation of grasslands. J Ecol 106:434–443. https://doi.org/10.1111/1365-2745.12884
Garnier E, Lavorel S, Ansquer P et al (2007) Assessing the effects of land-use change on plant traits, communities and ecosystem functioning in grasslands: A standardized methodology and lessons from an application to 11 European sites. Ann Bot 99:967–985. https://doi.org/10.1093/aob/mcl215
Giling DP, Beaumelle L, Phillips HRP et al (2019) A niche for ecosystem multifunctionality in global change research. Glob Change Biol 25:763–774. https://doi.org/10.1111/gcb.14528
Guiz J, Ebeling A, Eisenhauer N et al (2018) Interspecific competition alters leaf stoichiometry in 20 grassland species. Oikos 127:903–914. https://doi.org/10.1111/oik.04907
Hu Y, Sistla S, Wei H et al (2020) Legacy effects of nitrogen deposition on plant nutrient stoichiometry in a temperate grassland. Plant Soil 446:503–513. https://doi.org/10.1007/s11104-019-04357-7
Huang H (2018) ggcor: extended tools for correlation analysis and visualization. R package version: 0.7.6. https://github.com/houyunhuang/ggcor. Accessed July 22 2020.
Jing X, Sanders NJ, Shi Y et al (2015) The links between ecosystem multifunctionality and above- and belowground biodiversity are mediated by climate. Nat Commun 6:8159. https://doi.org/10.1038/ncomms9159
Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450. https://doi.org/10.2307/2404783
Lefcheck J, Byrnes j (2016) Grace j PiecewiseSEM: Piecewise structural equation modeling. R package version 2.1.2. https://cran.r-project.org/web/packages/piecewiseSEM/. Accessed by 20 Dec 2020
Li J, Yang C, Liu X, Shao X (2019) Inconsistent stoichiometry response of grasses and forbs to nitrogen and water additions in an alpine meadow of the Qinghai-Tibet Plateau. Agr Ecosyst Environ 279:178–186. https://doi.org/10.1016/j.agee.2018.12.016
Li L, Zhang J, He XZ, Hou F (2021a) Different effects of sheep excrement type and supply level on plant and soil C:N:P stoichiometry in a typical steppe on the loess plateau. Plant Soil 462:45–58. https://doi.org/10.1007/s11104-021-04880-6
Li L, Zhang J, He XZ, Hou F (2021b) Sheep trampling modifies soil and plant C:N:P stoichiometry in a typical steppe of the Loess Plateau. Rangel Ecol Manag 76:100–108. https://doi.org/10.1016/j.rama.2021.02.008
Li W, Xu F, Zheng S et al (2017) Patterns and thresholds of grazing-induced changes in community structure and ecosystem functioning: species-level responses and the critical role of species traits. J Appl Ecol 54:963–975. https://doi.org/10.1111/1365-2664.12806
Liu J, Liu W, Long X et al (2020) Effects of nitrogen addition on C:N:P stoichiometry in moss crust-soil continuum in the N-limited Gurbantünggüt Desert, Northwest China. Eur J Soil Biol 98:103174. https://doi.org/10.1016/j.ejsobi.2020.103174
Liu X, Shi X, Zhang S (2021) Soil abiotic properties and plant functional diversity co-regulate the impacts of nitrogen addition on ecosystem multifunctionality in an alpine meadow. Sci Total Environ 780:146476. https://doi.org/10.1016/j.scitotenv.2021.146476
Maestre FT, Quero JL, Gotelli NJ et al (2012) Plant species richness and ecosystem multifunctionality in global drylands. Science 335:214–218. https://doi.org/10.1126/science.1215442
Mao J, Mao Q, Zheng M, Mo J (2020) Responses of foliar nutrient status and stoichiometry to nitrogen addition in different ecosystems: a meta-analysis. J Geophys Res Biogeosci 125:e2019JG005347. https://doi.org/10.1029/2019JG005347
Meyer ST, Ptacnik R, Hillebrand H et al (2018) Biodiversity-multifunctionality relationships depend on identity and number of measured functions. Nat Ecol Evol 2:44–49. https://doi.org/10.1038/s41559-017-0391-4
Oksanen J, Blanchet FG, Friendly M et al (2020) Vegan: community ecology package. R package version 2.5-7. https://cran.r-project.org/package=vegan. Accessed by 28 Nov 2020
Ren H, Eviner VT, Gui W et al (2018) Livestock grazing regulates ecosystem multifunctionality in semi-arid grassland. Funct Ecol 32:2790–2800. https://doi.org/10.1111/1365-2435.13215
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/. Accessed 18 May 2021
Sardans J, Grau O, Chen HYH et al (2017) Changes in nutrient concentrations of leaves and roots in response to global change factors. Glob Chang Biol 23:3849–3856. https://doi.org/10.1111/gcb.13721
Schrama M, Heijning P, Bakker JP et al (2013) Herbivore trampling as an alternative pathway for explaining differences in nitrogen mineralization in moist grasslands. Oecologia 172:231–243. https://doi.org/10.1007/s00442-012-2484-8
Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana
Shipley B (2013) The AIC model selection method applied to path analytic models compared using ad-separation test. Ecology 94:560–564. https://doi.org/10.1890/12-0976.1
Smith B, Wilson JB (1996) A consumer’s guide to evenness indices. Oikos 76:70–82. https://doi.org/10.2307/3545749
Sparks DL, Page AL, Loeppert PA et al (1996) Methods of soil analysis part 3: chemical methods. Soil Science Society of America and American Society of Agronomy, Madison, p 1424
Stevens CJ (2019) Nitrogen in the environment. Science 363:578–580. https://doi.org/10.1126/science.aav82
Stevens CJ, Lind EM, Hautier Y et al (2015) Anthropogenic nitrogen deposition predicts local grassland primary production worldwide. Ecology 96:1459–1465. https://doi.org/10.1890/14-1902.1
Van Reeuwijk LP (2002) Procedures for soil analysis 6th edition. International soil reference and information centre (ISRIC), Wageningen
Wang Y, Wang D, Shi B, Sun W (2020) Differential effects of grazing, water, and nitrogen addition on soil respiration and its components in a meadow steppe. Plant Soil 447:581–598. https://doi.org/10.1007/s11104-019-04410-5
Wang Z, Han G, Hao X et al (2017) Effect of manipulating animal stocking rate on the carbon storage capacity in a degraded desert steppe. Ecol Res 32:1001–1009. https://doi.org/10.1007/s11284-017-1516-6
Yang F, Niu K, Collins CG et al (2019) Grazing practices affect the soil microbial community composition in a Tibetan alpine meadow. Land Degrad Dev 30:49–59. https://doi.org/10.1002/ldr.3189
Yang Z, Zhu Q, Zhan W et al (2018) The linkage between vegetation and soil nutrients and their variation under different grazing intensities in an alpine meadow on the eastern Qinghai-Tibetan Plateau. Ecol Eng 110:128–136. https://doi.org/10.1016/j.ecoleng.2017.11.001
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.090682910
Zhang P, Yang Z, Wu J (2021a) Livestock grazing promotes ecosystem multifunctionality of a coastal salt marsh. J Appl Ecol 58:2124–2134. https://doi.org/10.1111/1365-2664.13957
Zhang R, Wang Z, Niu S et al (2021b) Diversity of plant and soil microbes mediates the response of ecosystem multifunctionality to grazing disturbance. Sci Total Environ 776:145730. https://doi.org/10.1016/j.scitotenv.2021.145730
Zhang R, Tian D, Chen HYH et al (2022) Biodiversity alleviates the decrease of grassland multifunctionality under grazing disturbance: A global meta-analysis. Global Ecol Biogeogr 31:155–167. https://doi.org/10.1111/geb.13408
Zheng S, Chi Y, Yang X et al (2021) Direct and indirect effects of nitrogen enrichment and grazing on grassland productivity through intraspecific trait variability. J Appl Ecol 59:598–610. https://doi.org/10.1111/1365-2664.14078
Zhou XP, Yang HQ (2018) Dynamic damage localization in crack-weakened rock mass: Strain energy density factor approach. Theor Appl Fract Mec 97:289–302. https://doi.org/10.1016/j.tafmec.2017.05.006
Acknowledgements
We thank three anonymous reviewers for their constructive comments and suggestions, which have significantly improved the paper. This research was supported by the Program for National Program for S&T Collaboration of Developing Countries (KY202002011), Innovative Research Team in University (Grant No. IRT_17R50), the Key R&D Program of Ningxia Hui Autonomous Region (2019BBF02001), the Technological Support for Grassland Ecological Management (GARS-08) and ‘Lanzhou City's Scientific Research Funding Subsidy to Lanzhou University’.
Funding
This research was supported by the Program for National Program for S&T Collaboration of Developing Countries (KY202002011), Innovative Research Team in University (Grant No. IRT_17R50), the Key R&D Program of Ningxia Hui Autonomous Region (2019BBF02001), the Technological Support for Grassland Ecological Management (GARS-08) and ‘Lanzhou City's Scientific Research Funding Subsidy to Lanzhou University’.
Author information
Authors and Affiliations
Contributions
Fujiang Hou, Lan Li, Xiumin Zhang, Junqi Hu, and Mengyuan Wang contributed to the study’s conception and design. Lan Li and Zhen Wang prepared materials and collected data. Lan Li, and Xiong Z. He analysed the data. Lan Li wrote the first draft of the manuscript and all authors revised the manuscript. All authors approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Wen-Hao Zhang.
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.
ESM 1
(DOCX 145 KB)
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
Li, L., He, X.Z., Zhang, X. et al. Different effects of grazing and nitrogen addition on ecosystem multifunctionality are driven by changes in plant resource stoichiometry in a typical steppe. Plant Soil 481, 179–194 (2022). https://doi.org/10.1007/s11104-022-05624-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05624-w