Abstract
Aims
Plants and soils are key factors in maintaining ecosystem multifunctionality (EMF). Yet, it remains unclear how climate factors regulate the EMF through soil properties and plant diversity of different plant functional groups in primary dark coniferous forests of subalpine regions.
Methods
Nine functional indicators related to carbon, nitrogen, phosphorus cycling and plant productivity, four leaf functional traits, mean annual precipitation (MAP) and mean annual temperature (MAT) were collected from 50 primary dark coniferous forests in ten sites on the eastern Qinghai-Tibetan Plateau. The EMF was calculated using two approaches. The averaging approach involves converting and averaging the functional indicators, and the multiple threshold approach quantifies the number of functions across different thresholds.
Results
MAP promoted EMF. Soil water content and shrub species richness had a significant positive effect on EMF, whereas herb species richness had a negative effect. Functional diversity and specific leaf area of tree species rather than richness had a significant positive effect on EMF, indicating the increase in functional traits was beneficial to EMF. Climatic factors could directly or indirectly affect EMF through species richness, functional diversity, and soil abiotic factors.
Conclusions
The effects of species richness on EMF varied among different plant functional groups, possibly related to different mechanisms, and highlighted the role of functional diversity in maintaining EMF. Spatial variation in climate could modify soil properties and plant diversity, further affecting EMF in primary dark coniferous forests. Hence, these findings should be considered in future predictions of how a changing climate could affect EMF.
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Data availability
The datasets analyzed in the study can be obtained from the corresponding author under reasonable request.
References
Baldrian P (2017) Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev 41:109–130. https://doi.org/10.1093/femsre/fuw040
Bardgett RD, Manning P, Morriën E et al (2013) Hierarchical responses of plant-soil interactions to climate change: consequences for the global carbon cycle. J Ecol 101:334–343. https://doi.org/10.1111/1365-2745.12043
Barry KE, Mommer L, van Ruijven J et al (2019) The future of complementarity: disentangling causes from consequences. Trends Ecol Evol 34:167–180. https://doi.org/10.1016/j.tree.2018.10.013
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
Cardinale BJ, Wright JP, Cadotte MW et al (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci 104:18123–18128. https://doi.org/10.1073/pnas.0709069104
Carrera AL, Bertiller MB (2010) Relationships among plant litter, fine roots, and soil organic C and N across an aridity gradient in northern Patagonia, Argentina. Ecoscience 17:276–286. https://doi.org/10.2980/17-3-3359
Chen J, Shi Z, Liu S et al (2022a) Altitudinal variation influences soil fungal community composition and diversity in Alpine-Gorge region on the eastern Qinghai-Tibetan Plateau. J Fungi 8:807. https://doi.org/10.3390/jof8080807
Chen W, Wang J, Chen X et al (2022b) Soil microbial network complexity predicts ecosystem function along elevation gradients on the Tibetan Plateau. Soil Biol Biochem 172:108766. https://doi.org/10.1016/j.soilbio.2022.108766
Chen M, Shi Z, Liu S et al (2023) Leaf functional traits have more contributions than climate to the variations of leaf stable carbon isotope of different plant functional types on the eastern Qinghai-Tibetan Plateau. Sci Total Environ 871:162036. https://doi.org/10.1016/j.scitotenv.2023.162036
Crawford MS, Barry KE, Clark AT et al (2021) The function-dominance correlation drives the direction and strength of biodiversity-ecosystem functioning relationships. Ecol Lett 24:1762–1775. https://doi.org/10.1111/ele.13776
Curtin D, Peterson ME, Anderson CR (2016) pH-dependence of organic matter solubility: base type effects on dissolved organic C, N, P, and S in soils with contrasting mineralogy. Geoderma 271:161–172. https://doi.org/10.1016/j.geoderma.2016.02.009
Dakos V, Matthews B, Hendry AP et al (2019) Ecosystem tipping points in an evolving world. Nat Ecol Evol 3:355–362. https://doi.org/10.1038/s41559-019-0797-2
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. https://doi.org/10.1038/nature04514
De Long JR, Jackson BG, Wilkinson A et al (2019) Relationships between plant traits, soil properties and carbon fluxes differ between monocultures and mixed communities in temperate grassland. J Ecol 107:1704–1719. https://doi.org/10.1111/1365-2745.13160
Dee LE, Ferraro PJ, Severen CN et al (2023) Clarifying the effect of biodiversity on productivity in natural ecosystems with longitudinal data and methods for causal inference. Nat Commun 14:2607. https://doi.org/10.1038/s41467-023-37194-5
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
Dong Z, Li H, Xiao J et al (2022) Soil multifunctionality of paddy field is explained by soil pH rather than microbial diversity after 8-years of repeated applications of biochar and nitrogen fertilizer. Sci Total Environ 853:158620. https://doi.org/10.1016/j.scitotenv.2022.158620
Fry EL, Johnson GN, Hall AL et al (2018) Drought neutralises plant-soil feedback of two mesic grassland forbs. Oecologia 186:1113–1125. https://doi.org/10.1007/s00442-018-4082-x
Garnier E, Cortez J, Billes G et al (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637. https://doi.org/10.1890/03-0799
Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. https://doi.org/10.1046/j.1365-2745.1998.00306.x
Hagan JG, Vanschoenwinkel B, Gamfeldt L (2021) We should not necessarily expect positive relationships between biodiversity and ecosystem functioning in observational field data. Ecol Lett 24:2537–2548. https://doi.org/10.1111/ele.13874
Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–190. https://doi.org/10.1038/nature05947
Hector A, Schmid B, Beierkuhnlein C et al (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127. https://doi.org/10.1126/science.286.5442.1123
Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. https://doi.org/10.1890/04-0922
Hu W, Ran J, Dong L et al (2021) Aridity-driven shift in biodiversity-soil multifunctionality relationships. Nat Commun 12:5350. https://doi.org/10.1038/s41467-021-25641-0
Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460. https://doi.org/10.1007/s004420050180
Hutchinson MF, Xu TB (2013) ANUSPLIN version 4.4 user guide. Australian National University, Canberra
Isbell F, Calcagno V, Hector A et al (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202. https://doi.org/10.1038/nature10282
Jiao S, Lu Y, Wei G (2022) Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Glob Change Biol 28:140–153. https://doi.org/10.1111/gcb.15917
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
Kaisermann A, de Vries FT, Griffiths RI et al (2017) Legacy effects of drought on plant-soil feedbacks and plant-plant interactions. New Phytol 215:1413–1424. https://doi.org/10.1111/nph.14661
Karlowsky S, Augusti A, Ingrisch J et al (2018) Land use in mountain grasslands alters drought response and recovery of carbon allocation and plant-microbial interactions. J Ecol 106:1230–1243. https://doi.org/10.1111/1365-2745.12910
Lauber CL, Strickland MS, Bradford MA et al (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415. https://doi.org/10.1016/j.soilbio.2008.05.021
Lawton JH (1994) What do species do in ecosystems. Oikos 71:367–374. https://doi.org/10.2307/3545824
Le Bagousse-Pinguet Y, Soliveres S, Gross N et al (2019) Phylogenetic, functional, and taxonomic richness have both positive and negative effects on ecosystem multifunctionality. Proc Natl Acad Sci 116:8419–8424. https://doi.org/10.1073/pnas.1815727116
Li SF, Huang XB, Lang XD et al (2020) Cumulative effects of multiple biodiversity attributes and abiotic factors on ecosystem multifunctionality in the Jinsha river valley of southwestern China. For Ecol Manag 472:118281. https://doi.org/10.1016/j.foreco.2020.118281
Li K, Zhang H, Li X et al (2021) Field management practices drive ecosystem multifunctionality in a smallholder-dominated agricultural system. Agricult Ecosyst Environ 313:107389. https://doi.org/10.1016/j.agee.2021.107389
Li J, Li S, Huang X et al (2022) Plant diversity and soil properties regulate the microbial community of monsoon evergreen broad-leaved forest under different intensities of woodland use. Sci Total Environ 821:153565. https://doi.org/10.1016/j.scitotenv.2022.153565
Liu D, Ogaya R, Barbeta A et al (2015) Contrasting impacts of continuous moderate drought and episodic severe droughts on the aboveground-biomass increment and litterfall of three coexisting Mediterranean woody species. Glob Change Biol 21:4196–4209. https://doi.org/10.1111/gcb.13029
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
Liu S, Xu G, Chen H et al (2023) Contrasting responses of soil microbial biomass and extracellular enzyme activity along an elevation gradient on the eastern Qinghai-Tibetan Plateau. Front Microbiol 14:974316. https://doi.org/10.3389/fmicb.2023.974316
Loreau M, Naeem S, Inchausti P et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. https://doi.org/10.1126/science.1064088
Luo YH, Cadotte MW, Burgess KS et al (2019) Greater than the sum of the parts: how the species composition in different forest strata influence ecosystem function. Ecol Lett 22:1449–1461. https://doi.org/10.1111/ele.13330
Luo Y, Wang X, Ouyang Z et al (2020) A review of biomass equations for China’s tree species. Earth Syst Sci Data 12:21–40. https://doi.org/10.5194/essd-12-21-2020
Luo YH, Cadotte MW, Liu J et al (2022) Multitrophic diversity and biotic associations influence subalpine forest ecosystem multifunctionality. Ecology 103:e3745. https://doi.org/10.1002/ecy.3745
Maestre FT, Quero José L, Gotelli Nicholas J et al (2012) Plant species richness and ecosystem multifunctionality in global drylands. Science 335:214–218. https://doi.org/10.1126/science.1215442
Manning P, Van Der Plas F, Soliveres S et al (2018) Redefining ecosystem multifunctionality. Nat Ecol Evol 2:427–436. https://doi.org/10.1038/s41559-017-0461-7
Mason NWH, Mouillot D, Lee WG et al (2005) 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
Migliavacca M, Musavi T, Mahecha MD et al (2021) The three major axes of terrestrial ecosystem function. Nature 598:468–472. https://doi.org/10.1038/s41586-021-03939-9
Moir J, Tiessen H (2007) Characterization of available P by sequential extraction. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis. CRC Press, Boca Raton, pp 293–306
Pfisterer AB, Schmid B (2002) Diversity-dependent production can decrease the stability of ecosystem functioning. Nature 416:84–86. https://doi.org/10.1038/416084a
Pugnaire FI, Morillo José A, Peñuelas J et al (2019) Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems. Sci Adv 5:eaaz1834. https://doi.org/10.1126/sciadv.aaz1834
Rousk J, Bååth E, Brookes PC et al (2010a) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. https://doi.org/10.1038/ismej.2010.58
Rousk J, Brookes PC, Bååth E (2010b) The microbial PLFA composition as affected by pH in an arable soil. Soil Biol Biochem 42:516–520. https://doi.org/10.1016/j.soilbio.2009.11.026
Rowland L, da Costa AC, Oliveira AA et al (2018) Shock and stabilisation following long-term drought in tropical forest from 15 years of litterfall dynamics. J Ecol 106:1673–1682. https://doi.org/10.1111/1365-2745.12931
Song MH, Zhu JF, Li YK et al (2020) Shifts in functional compositions predict desired multifunctionality along fragmentation intensities in an alpine grassland. Ecol Indic 112:106095. https://doi.org/10.1016/j.ecolind.2020.106095
Suseela V, Tharayil N, Xing B et al (2015) Warming and drought differentially influence the production and resorption of elemental and metabolic nitrogen pools in Quercus rubra. Glob Change Biol 21:4177–4195. https://doi.org/10.1111/gcb.13033
Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci 94:1857–1861. https://doi.org/10.1073/pnas.94.5.1857
Valencia E, Maestre FT, Le Bagousse-Pinguet Y et al (2015) Functional diversity enhances the resistance of ecosystem multifunctionality to aridity in Mediterranean drylands. New Phytol 206:660–671. https://doi.org/10.1111/nph.13268
Valencia E, Gross N, Quero JL et al (2018) Cascading effects from plants to soil microorganisms explain how plant species richness and simulated climate change affect soil multifunctionality. Glob Change Biol 24:5642–5654. https://doi.org/10.1111/gcb.14440
Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. https://doi.org/10.1126/science.1094875
Wolters V, Silver WL, Bignell DE et al (2000) Effects of global changes on above-and belowground biodiversity in terrestrial ecosystems: implications for ecosystem functioning. Bioscience 50:1089–1098. https://doi.org/10.1641/0006-3568(2000)050[1089:eogcoa]2.0.co;2
Wright JS (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14. https://doi.org/10.1007/s004420100809
Yuan Z, Ali A, Ruiz-Benito P et al (2020) Above- and below-ground biodiversity jointly regulate temperate forest multifunctionality along a local-scale environmental gradient. J Ecol 108:2012–2024. https://doi.org/10.1111/1365-2745.13378
Zavaleta ES, Pasari JR, Hulvey KB et al (2010) Sustaining multiple ecosystem functions in grassland. communities requires higher biodiversity. Proc Natl Acad Sci 107:1443–1446. https://doi.org/10.1073/pnas.0906829107
Zhang Y, Gu F, Liu S et al (2013) Variations of carbon stock with forest types in subalpine region of southwestern China. For Ecol Manage 300:88–95. https://doi.org/10.1016/j.foreco.2012.06.010
Zhang H, Ye C, Wang S (2022) Elevation dependence of climate effects on ecosystem multifunctionality states over the Qinghai-Tibet Plateau. Glob Ecol Conserv 36:e02066. https://doi.org/10.1016/j.gecco.2022.e02066
Zheng Q, Hu Y, Zhang S et al (2019) Soil multifunctionality is affected by the soil environment and by microbial community composition and diversity. Soil Biol Biochem 136:107521. https://doi.org/10.1016/j.soilbio.2019.107521
Acknowledgements
The work was supported by the Fundamental Research Funds of CAF (CAFYBB2021ZA002-2, CAFYBB2022QC002, CAFYBB2022SY021 and CAFYBB2022SY024), the National Key Research and Development Program of China (2021YFD2200405) and the National Natural Science Foundation of China (32201321).
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All of the authors contributed to our research. Zuomin Shi and Feifan Li conceived the ideas and designed the research. Feifan Li, Shun Liu, Gexi Xu, Miaomiao Zhang, Xiangwen Cao, Miao Chen, Jian Chen, Hongshuang Xing and Shanshan Gong participated in plot construction and data collecting. Feifan Li analyzed the data and wrote the first draft. Zuomin Shi reviewed the draft. All authors commented and approved the final manuscript.
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Li, F., Shi, Z., Liu, S. et al. Soil properties and plant diversity co-regulate ecosystem multifunctionality of subalpine primary dark coniferous forest on the eastern Qinghai-Tibetan Plateau. Plant Soil 493, 207–219 (2023). https://doi.org/10.1007/s11104-023-06222-0
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DOI: https://doi.org/10.1007/s11104-023-06222-0