Abstract
Understanding the relationship between nitrogen addition and the diversity and productivity of alpine grassland plant communities is important for the sustainable development of grassland ecosystems. However, it is unclear how nitrogen addition, growth stage, and interactions between these factors affect plant biomass and diversity when regulating soil and plant nutrient factors. This study researched the temporal variations in plant community diversity and biomass after nitrogen addition in an alpine grassland from 2020 to 2021. Furthermore, this study used structural equation modeling to determine the direct and indirect pathways of plant and soil factors regulating plant biomass and diversity. Results showed that (1) nitrogen addition had significant effects on aboveground biomass, belowground biomass, and total biomass, while growth stage only had significant effects on aboveground biomass. Nitrogen addition, growth stage, and their interaction significantly affected the Shannon–Wiener diversity, the Margalef species richness, and the Pielou evenness. (2) Redundancy analysis indicated that total aboveground phosphorus, aboveground ammonium nitrogen, soil total nitrogen, and soil available nitrogen were the most significant explanatory variables for plant biomass variation, while soil available nitrogen, total soil nitrogen, and total belowground nitrogen were the key predicting factors for plant community composition variation. (3) Structural equation modeling revealed that plant biomass and diversity changed with nitrogen addition and growth stage. Nitrogen addition directly increased aboveground, belowground, and total biomass and indirectly affected plant biomass through the effectiveness of aboveground ammonium nitrogen, total aboveground phosphorus, and total soil nitrogen. Plant diversity was directly affected by the growth stage and indirectly by nitrogen addition through soil nitrogen and root nitrogen, which further affected plant diversity and evenness indices. The decrease in plant community diversity and species richness caused by nitrogen addition and different growth stages indirectly and negatively affected aboveground plant biomass. Overall, the results of this study indicate that plant biomass and diversity in alpine grasslands are affected by exogenous nitrogen addition and growth stage.
REFERENCES
Vitousek, P. and Howarth, R., Nitrogen limitation on land and in the sea: How can it occur?, Biogeochemistry, 1991, vol. 13, pp. 87–115.
Zhang, J. Q., Li, Q., Ren, Z. W., et al., Effect of nitrogen addition on species richness and its relationship with aboveground productivity in alpine meadow plant communities on the Tibetan Plateau, J. Plant Ecol., 2010, vol. 34, pp. 1125–1131.
Clark, C.M., Cleland, E.E., Collins, S.L., et al., Environmental and plant community determinants of species loss following nitrogen enrichment, Ecol. Lett., 2007, vol.10, pp. 596–607. https://doi.org/10.1111/j.1461-0248.2007.01053.x
Peter, M., Vitousek, S.P., Benjamin, Z., et al., Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions, Ecol. Appl., 2010, vol. 20, pp. 5–15.
Volio, M.L., Koerner, S.E., La Pierre, K.J., et al., Changes in plant community composition, not diversity, during a decade of nitrogen and phosphorus additions drive above-ground productivity in a tallgrass prairie, J. Ecol., 2014, vol. 102, pp. 1649–1660. https://doi.org/10.1111/1365-2745.12312
Christopher, M., Clark, P.E., Morefield, F.S., et al., Estimated losses of plant biodiversity in the United States from historical N deposition (1985–2010), Ecology, 2013, vol. 94, pp. 1441–1448.
Wang, J., Gao, Y., Zhang, Y., et al., Asymmetry in above- and belowground productivity responses to N addition in a semi-arid temperate steppe, Global Change Biol., 2019, vol. 25, pp. 2958–2969. https://doi.org/10.1111/gcb.14719
Piao, S., Liu, Q., Chen, A., et al., Plant phenology and global climate change: Current progresses and challenges, Global Change Biol., 2019, vol. 25, pp. 1922–1940. https://doi.org/10.1111/gcb.14619
Franziska, K. and Christian, K., The role of photoperiodism in alpine plant development, Arct., Antarct., Alp. Res., 2003, vol. 35, no. 3, pp. 361–368.
Gonsamo, A., Chen, J.M., and Ooi, Y.W., Peak season plant activity shift towards spring is reflected by increasing carbon uptake by extratropical ecosystems, Global Change Biol., 2018, vol. 24, pp. 2117–2128. https://doi.org/10.1111/gcb.14001
Wang, H., Liu, H., Cao, G., et al., Alpine grassland plants grow earlier and faster but biomass remains unchanged over 35 years of climate change, Ecol. Lett., 2020, vol. 23, no. 4, pp. 701–710.
Xie, Y., Civco, D.L., and Silander, J.A., Species-specific spring and autumn leaf phenology captured by time-lapse digital cameras, Ecosphere, 2018, vol. 9, p. e02089. https://doi.org/10.1002/ecs2.2089
Oehri, J., Schmid, B., Schaepman-Strub, G., et al., Biodiversity promotes primary productivity and growing season lengthening at the landscape scale, Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, pp. 10160–10165. https://doi.org/10.1073/pnas.1703928114
Wang, S. P., Causes of vegetation degradation and conservation strategies in the “Three River Source” area of Qinghai Province, J. Grassl. Sci., 2003, vol. 33, pp. 1–9.
De, K.J., Effect of fertilization on primary productivity and soil nutrients in alpine meadows in the Sanjiangyuan region, Ying Yong Sheng Tai Xue Bao, 2015, vol. 25, pp. 3458–3468.
Lu, G. X., Li, X., Dang, N., et al., Effects of different forms and ratios of nitrogen on the growth height and biomass of alpine meadow plants, J. Grassl., 2018, vol. 26, pp. 210–215.
Shi, J.J., Hong, B.Z., Ma, Y.S., et al., Effects of fertilization and weed control on the characteristics of artificial grassland communities in the Sanjiangyuan area, Chin. Acta Pra. Sin., 2011, vol. 19, no. 5, pp. 724–728.
Yang, S., Zhao, W., and Pereira, P., Determinations of environmental factors on interactive soil properties across different land-use types on the Loess Plateau, China, Sci. Total Environ., 2020, vol. 738, p. 140270. https://doi.org/10.1016/j.scitotenv.2020.140270
Hooper, D.U., Adair, E.C., Cardinale, B.J., et al., A global synthesis reveals biodiversity loss as a major driver of ecosystem change, Nature, 2012, vol. 486, pp. 105–108. https://doi.org/10.1038/nature11118
Cleland, E.E., Chuine, I., Menzel, A., et al., Shifting plant phenology in response to global change, Trends Ecol. Evol., 2007, vol. 22, pp. 357–365. https://doi.org/10.1016/j.tree.2007.04.003
Sun, S. and Frelich, L.E., Flowering phenology and height growth pattern are associated with maximum plant height, relative growth rate and stem tissue mass density in herbaceous grassland species, J. Ecol., 2011, vol. 99, pp. 991–1000. https://doi.org/10.1111/j.1365-2745.2011.01830.x
Damgaard, C., Ejrnaes, R., Stevens, C.J., et al., Intra-specific spatial aggregation in acidic grasslands: Effects of acidification and nitrogen deposition on spatial patterns of plant communities, J. Veg. Sci., 2013, vol. 24, pp. 25–32. https://doi.org/10.1111/j.1654-1103.2012.01438.x
Eskelinen, A., Gravuer, K., Harpole, W.S., et al., Resource-enhancing global changes drive a whole-ecosystem shift to faster cycling but decrease diversity, Ecology, 2020, vol. 101, p. e03178. https://doi.org/10.1002/ecy.3178
Stevens, C.J., David, T.I., Storkey, J., et al., Atmospheric nitrogen deposition in terrestrial ecosystems: Its impact on plant communities and consequences across trophic levels, Funct. Ecol., 2018, vol. 32, pp. 1757–1769. https://doi.org/10.1111/1365-2435.13063
Zhao, Y., Yang, B., Li, M., et al., Community composition, structure and productivity in response to nitrogen and phosphorus additions in a temperate meadow, Sci. Total Environ., 2019, vol. 654, pp. 863–871.
Hoover, S.E., Ladley, J.J., Shchepetkina, A.A., et al., Warming, CO2, and nitrogen deposition interactively affect a plant-pollinator mutualism, Ecol. Lett., 2012, vol. 15, pp. 227–234. https://doi.org/10.1111/j.1461-0248.2011.01729.x
Wolf, A.A., Zavaleta, E.S., and Selmants, P.C., Flowering phenology shifts in response to biodiversity loss, Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, pp. 3463–3468. https://doi.org/10.1073/pnas.1608357114
Martha, R. and Luis, E., Reproductive ecology of five sympatric Agave Littaea (Agavaceae) species in central Mexico, Am. J. Bot., 2005, vol. 92, pp. 1330–1341.
Chun-Li, L.I., Qi, L.I., Liang, Z., et al., Responses of plant community biomass to nitrogen and phosphorus additions in natural and restored grasslands around Qinghai Lake Basin, Chin. J. Plant Ecol., 2016, vol. 40, pp. 1015–1027. https://doi.org/10.17521/cjpe.2016.0048
Wu, H., Xiang, W., Ouyang, S., et al., Linkage between tree species richness and soil microbial diversity improves phosphorus bioavailability, Funct. Ecol., 2019, vol. 33, pp. 1549–1560. https://doi.org/10.1111/1365-2435.13355
Zhou, X., Wu, W., Niu, K., et al., Realistic loss of plant species diversity decreases soil quality in a Tibetan alpine meadow, Agric., Ecosyst. Environ., 2019, vol. 279, pp. 25–32. https://doi.org/10.1016/j.agee.2019.03.019
Clark, C.M. and Tilman, D., Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands, Nature, 2008, vol. 451, pp. 712–715. https://doi.org/10.1038/nature06503
Maisto, G., De, M.A., Meola, A., et al., Nutrient dynamics in litter mixtures of four Mediterranean maquis species decomposing in situ, Soil Biol. Biochem., 2011, vol. 43, pp. 520–530. https://doi.org/10.1016/j.soilbio.2010.11.017
Liu, X., Tan, N., Zhou, G., et al., Plant diversity and species turnover co-regulate soil nitrogen and phosphorus availability in Dinghushan forests, southern China, Plant Soil, 2021, vol. 464, pp. 257–272. https://doi.org/10.1007/s11104-021-04940-x
Pang, X.P. and Guo, Z.G., Plateau pika disturbances alter plant productivity and soil nutrients in alpine meadows of the Qinghai-Tibetan Plateau, China, Rangeland J., 2017, vol.39, no. 2, pp. 133–144. https://doi.org/10.1071/rj16093
Li, C., Zheng, Z., Peng, Y., et al., Precipitation and nitrogen addition enhance biomass allocation to aboveground in an alpine steppe, Ecol. Evol., 2019, vol. 9, pp. 12 193–12 201. https://doi.org/10.1002/ece3.5706
Chen, Z., Xiong, P., Zhou, J., et al., Effects of plant diversity on semiarid grassland stability depends on functional group composition and dynamics under N and P addition, Sci. Total Environ., 2021, vol. 799, p. 149482. https://doi.org/10.1016/j.scitotenv.2021.149482
Bloor, J.M.G., Pichon, P., Falcimagne, R., et al., Effects of warming, summer drought, and CO2 enrichment on aboveground biomass production, flowering phenology, and community structure in an upland grassland ecosystem, Ecosystems, 2010, vol. 13, pp. 888–900. https://doi.org/10.1007/s10021-010-9363-0
Zhang, B., Cao, J., Bai, Y., et al., Effects of rainfall amount and frequency on vegetation growth in a Tibetan alpine meadow, Clim. Change, 2012, vol. 118, pp. 197–212. https://doi.org/10.1007/s10584-012-0622-2
Ehleringer, S.S.A.J.R., Water Use Trade-offs and optimal adaptations to pulse-driven arid ecosystems, J. Ecol., 2001, vol. 89, pp. 464–480.
Barr, A.G., Black, T.A., Hogg, E.H., et al., Climatic controls on the carbon and water balances of a boreal aspen forest, 1994–2003, Global Change Biol., 2007, vol. 13, pp. 561–576. https://doi.org/10.1111/j.1365-2486.2006.01220.x
Loik, M.E., Sensitivity of water relations and photosynthesis to summer precipitation pulses for Artemisia tridentata and Purshia tridentata, Plant Ecol., 2007, vol. 191, pp. 95–108.
Engel, E.C., Weltzin, J.F., Norby, R.J., et al., Responses of an old-field plant community to interacting factors of elevated [CO2], warming, and soil moisture, J. Plant Ecol., 2009, vol. 2, pp. 1–11. https://doi.org/10.1093/jpe/rtn026
Rheault, G., Levesque, E., Proulx, R., Diversity of plant assemblages dampens the variability of the growing season phenology in wetland landscapes, BMC Ecol. Evol., 2021, vol. 21, pp. 91. https://doi.org/10.1186/s12862-021-01817-6
He, L.Y., Hu, Z.M., Li, S.G., et al., Effects of nitrogen and phosphorus additions on above-ground biomass of temperate grasslands in Inner Mongolia, Chin. J. Appl. Ecol., 2015, vol. 26, no. 8, pp. 2291–2297.
Kinugasa, T., Tsunekawa, A., and Shinoda, M., Increasing nitrogen deposition enhances post-drought recovery of grassland productivity in the Mongolian steppe, Oecologia, 2012, vol. 170, pp. 857–865. http://dx.doi.org/1010.1007/s00442-0
Bai, Y.f., Xing, Q., Pan, Q.M., et al., Primary production and rain use efficiency across a precipitation gradient on the Mongolia Plateau, Ecology, 2008, vol. 89, pp. 2140–2153.
Damgaard, C., Jensen, L., Frohn, L.M., et al., The effect of nitrogen deposition on the species richness of acid grasslands in Denmark: A comparison with a study performed on a European scale, Environ. Pollut., 2011, vol. 159, pp. 1778–1782. https://doi.org/10.1016/j.envpol.2011.04.003
James, J., Elser, T.A., Jill, S., et al., Shifts in Lake N : P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition, Science, 2009, vol. 326, no. 5954, pp. 835–837.
Xu, H., Qu, Q., Li, G., et al., Impact of nitrogen addition on plant-soil-enzyme C–N–P stoichiometry and microbial nutrient limitation, Soil Biol. Biochem., 2022, vol. 170, p. 108714. https://doi.org/10.1016/j.soilbio.2022.108714
Li, Z., Qiu, X., Sun, Y., et al., C : N : P stoichiometry responses to 10 years of nitrogen addition differ across soil components and plant organs in a subtropical Pleioblastus amarus forest, Sci. Total Environ., 2021, vol. 796, p. 148925. https://doi.org/10.1016/j.scitotenv.2021.148925
Wei, C., Yu, Q., Bai, E., et al., Nitrogen deposition weakens plant-microbe interactions in grassland ecosystems, Global Change Biol., 2013, vol. 19, pp. 3688–697.
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, 2019, vol. 22, pp. 1466–1477. https://doi.org/10.1007/s10021-019-00350-4
Tang, Z., Xu, W., Zhou, G., et al., Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China’s terrestrial ecosystems, Proc. Natl. Acad. Sci. U. S. A., 2018, vol. 115, pp. 4033–4038. https://doi.org/10.1073/pnas.1700295114
Biederman, L., Mortensen, B., Fay, P., et al., Nutrient addition shifts plant community composition towards earlier flowering species in some prairie ecoregions in the U.S. Central Plains, PLoS One, 2017, vol. 12, p. e0178440. https://doi.org/10.1371/journal.pone.0178440
Holger, B., Vicky, M.T., Christiane, R., et al., Aboveground overyielding in grassland mixtures is associated with reduced biomass partitioning to belowground organs, Ecol. Soc. Am., 2009, vol. 90, no. 6, pp. 1520–1530. http://www.jstor.org/stable/25592654
Fayiah, M., Dong, S., Li, Y., et al., The relationships between plant diversity, plant cover, plant biomass and soil fertility vary with grassland type on Qinghai-Tibetan Plateau, Agric., Ecosyst. Environ., 2019, vol. 286, p. 106659. https://doi.org/10.1016/j.agee.2019.106659
Zhou, X., Guo, Z., Zhang, P., et al., Shift in community functional composition following nitrogen fertilization in an alpine meadow through intraspecific trait variation and community composition change, Plant Soil, 2018, vol. 431, pp. 289–302. https://doi.org/10.1007/s11104-018-3771-x
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This study complies with the relevant regulations in China, where the study was conducted.
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This study was supported by the Construction of the Qinghai Sanjiangyuan Grassland Ecosystem National Field Scientific Observation and Research Station Chenduo Sub-station (K9922050). The authors declare no conflict of interest.
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Kejia De conceived and designed the experiments, conducted the experiments, provided ideas for recording the experiments, reviewed drafts of the paper and approved the final draft. Xuemei Xiang analyzed the data, prepared figures and tables, wrote or reviewed a draft of the paper and approved the final draft. Weishan Lin participated in the experiment, provided the analytical tools and approved the final draft. Xijie Wei participated in the experiment, provided the analytical tools and approved the final draft. Wei Wang participated in the experiments, provided the analytical tools and approved the final draft.
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Xuemei Xiang, De, K., Lin, W. et al. Response of Alpine Meadow Plant Diversity and Biomass to Nitrogen Addition and Growth Stage. Russ J Ecol 54, 439–453 (2023). https://doi.org/10.1134/S1067413623050144
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DOI: https://doi.org/10.1134/S1067413623050144