Abstract
Stomata play a critical role in surface–atmosphere exchange by controlling the flux of water and CO2 between the leaf and the atmosphere. However, the driving factors for the vital parameter, the marginal water cost of the carbon gain (λ), are poorly understood in the subalpine regions. Therefore, we studied λ in subalpine plants at all across altitudes. There was a parabolic pattern in λ of trees with increasing elevation, the highest at 2700 m asl and 3500 m asl for the broadleaf trees and the coniferous trees, respectively, while the λ of species of herbs and shrub decreased with elevation. For all species, λ were higher during the mid-growing season than during the early and late growing seasons under the same conditions. Mean λ values were higher in herbs and shrubs than in trees, indicating a more conservative strategy for water use in trees than in herbs and shrubs in forest communities. Furthermore, a higher λ value of the broadleaf tree than of the coniferous tree suggests that angiosperm trees use water more profligately than gymnosperm trees. Environmental factors had opposite effects on λ for herbs, shrubs, and trees. Soil conditions were positively correlated with λ for herbs and shrubs, but negatively for trees. Vegetation factors negatively influenced λ for herbs and shrubs, while no significant relationship was found with trees. From the results of the structural equation model, the improved empirical models for the simulation of stomatal conductance(gs) simulation based on the optimal stomatal behavior theory can accurately estimate the gs of the main species in subalpine forest communities.
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References
Arneth A, Lloyd J, Šantrůčková H, Bird M, Grigoryev S, Kalaschnikov YN et al (2002) Response of central siberian scots pine to soil water deficit and long-term trends in atmospheric CO2 concentration: long-term 13c in siberian scots pine. Glob Biogeochem Cycl 16(1):5–13
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3543
Barradas VL, Pablo Ruiz-Cordova J, Esperon-Rodriguez M (2016) Microclimatology and ecophysiology of the urban vegetation of a city with tropical climate modified by altitude in Mexico. Bot Sci 94(4):775–786. https://doi.org/10.17129/botsci.627
Beniston M (2003) Climatic change in mountain regions: a review of possible impacts. Clim Change 59(1–2):5–31. https://doi.org/10.1023/a:1024458411589
Biondi D, Freni G, Iacobellis V, Mascaro G, Montanari A (2012) Validation of hydrological models: conceptual basis, methodological approaches and a proposal for a code of practice. Phys Chem Earth 42–44:70–76. https://doi.org/10.1016/j.pce.2011.07.037
Bjorkman AD et al (2020) Status and trends in Arctic vegetation: evidence from experimental warming and long-term monitoring. Ambio 49(3):678–692. https://doi.org/10.1007/s13280-019-01161-6
Blasini DE, Koepke DF, Grady KC, Allan GJ, Gehring CA, Whitham TG, Cushman SA, Hultine KR (2021) Adaptive trait syndromes along multiple economic spectra define cold and warm adapted ecotypes in a widely distributed foundation tree species. J Ecol 109(3):1298–1318. https://doi.org/10.1111/1365-2745.13557
Chen MP, Wang GZ, Zhou SX, Zhao JF, Zhang X, He CS, Zhang YJ, Song L, Tan ZH (2019) Studies on forest ecosystem physiology: marginal water-use efficiency of a tropical, seasonal, evergreen forest in Thailand. J for Res 30(6):2163–2173. https://doi.org/10.1007/s11676-018-0804-5
Cheng WG (1996) Exploration of precipitation features on extra-high zone of Mt Gongga. Mt Res 14(3):177–182
Chieppa J, Nielsen UN, Tissue DT, Power SA (2019) Drought and phosphorus affect productivity of a mesic grassland via shifts in root traits of dominant species. Plant Soil 444(1–2):457–473. https://doi.org/10.1007/s11104-019-04290-9
Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. In: Jennings DH (ed) Integration of activity in the higher plant. Cambridge University Press, Cambridge, pp 471–505
Dang QL, Marfo J, Du F, Man R, Inoue S (2021) CO2 stimulation and response mechanisms vary with light supply in boreal conifers. J Plant Ecol 14(2):291–300. https://doi.org/10.1093/jpe/rtaa086
Davidson KJ, Lamour J, Rogers A, Serbin SP (2022) Late-day measurement of excised branches results in uncertainty in the estimation of two stomatal parameters derived from response curves in Populus deltoides Bartr. × Populus nigra L. Tree Physiol 42(7):1377–1395. https://doi.org/10.1093/treephys/tpac006
Dawson CW, Abrahart RJ, See LM (2007) HydroTest: a web-based toolbox of evaluation metrics for the standardised assessment of hydrological forecasts. Environ Model Softw 22(7):1034–1052. https://doi.org/10.1016/j.envsoft.2006.06.008
De Kauwe MG, Kala J, Lin YS, Pitman AJ, Medlyn BE, Duursma RA, Abramowitz G, Wang YP, Miralles DG (2015) A test of an optimal stomatal conductance scheme within the CABLE land surface model. Geosci Model Dev 8(2):431–452. https://doi.org/10.5194/gmd-8-431-2015
Duffy JE, Lefcheck JS, Stuart-Smith RD, Navarrete SA, Edgar GJ (2016) Biodiversity enhances reef fish biomass and resistance to climate change. Proc Natl Acad Sci USA 113(22):6230–6235. https://doi.org/10.1073/pnas.1524465113
Dusenge ME, Madhavji S, Way DA (2020) Contrasting acclimation responses to elevated CO2 and warming between an evergreen and a deciduous boreal conifer. Glob Change Biol 26(6):3639–3657. https://doi.org/10.1111/gcb.15084
Duursma RA, Payton P, Bange MP, Broughton KJ, Smith RA, Medlyn BE, Tissue DT (2013) Near-optimal response of instantaneous transpiration efficiency to vapour pressure deficit, temperature and [CO2] in cotton (Gossypium hirsutum L.). Agric for Meteorol 168:168–176. https://doi.org/10.1016/j.agrformet.2012.09.005
Duursma RA, Barton CVM, Lin YS, Medlyn BE, Eamus D, Tissue DT, Ellsworth DS, McMurtrie RE (2014) The peaked response of transpiration rate to vapour pressure deficit in field conditions can be explained by the temperature optimum of photosynthesis. Agric for Meteorol 189:2–10. https://doi.org/10.1016/j.agrformet.2013.12.007
Feng QH, Mauro C, Cheng RM, Liu SR, Shi ZM (2013) Leaf functional trait responses of Quercus aquifolioides to high elevations. Int J Agric Biol 15(1):69–75
Gao GL, Zhang XY, Yu TF (2017) Comparison of leaf stomatal conductance models for typical desert riparian phreatophytes in northwestern China. Agrofor Syst 91(5):927–939. https://doi.org/10.1007/s10457-016-9968-1
Gardner A et al (2023) Optimal stomatal theory predicts CO2 responses of stomatal conductance in both gymnosperm and angiosperm trees. New Phytol 237(4):1229–1241. https://doi.org/10.1111/nph.18618
Gimeno TE, Crous KY, Cooke J, O’Grady AP, Osvaldsson A, Medlyn BE, Ellsworth DS (2016) Conserved stomatal behaviour under elevated CO2 and varying water availability in a mature woodland. Funct Ecol 30(5):700–709. https://doi.org/10.1111/1365-2435.12532
Göebel L, Coners H, Hertel D, Willinghoefer S, Leuschner C (2019) The role of low soil temperature for photosynthesis and stomatal conductance of three graminoids from different elevations. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00330
Gunn S, Farrar JF, Collis BE, Nason M (1999) Specific leaf area in barley: individual leaves versus whole plants. New Phytol 143(1):45–51. https://doi.org/10.1046/j.1469-8137.1999.00434.x
Guo XP, Wu MY, Cao XC, Wang ZC (2018) Spatial-temporal distribution and impact factors of irrigation water use efficiency in the grain production of China. Int J Agric Biol Eng 11(5):131–138. https://doi.org/10.25165/j.ijabe.20181105.3588
Héroult A, Lin YS, Bourne A, Medlyn BE, Ellsworth DS (2013) Optimal stomatal conductance in relation to photosynthesis in climatically contrasting Eucalyptus species under drought. Plant Cell Environ 36(2):262–274. https://doi.org/10.1111/j.1365-3040.2012.02570.x
Higgens RF, Pries CH, Virginia RA (2021) Trade-offs between wood and leaf production in arctic shrubs along a temperature and moisture gradient in west Greenland. Ecosystems 24(3):652–666. https://doi.org/10.1007/s10021-020-00541-4
Hollinger DY et al (1998) Forest-atmosphere carbon dioxide exchange in eastern Siberia. Agric for Meteorol 90(4):291–306. https://doi.org/10.1016/s0168-1923(98)00057-4
Hölttä T, Lintunen A, Chan T, Mäkelä A, Nikinmaa E (2017) A steady-state stomatal model of balanced leaf gas exchange, hydraulics and maximal source-sink flux. Tree Physiol 37(7):851–868. https://doi.org/10.1093/treephys/tpx011
Hu ZY, Wang GX, Sun XY (2017) Precipitation and air temperature control the variations of dissolved organic matter along an altitudinal forest gradient, Gongga Mountains, China. Environ Sci Pollut Res 24(11):10391–10400. https://doi.org/10.1007/s11356-017-8719-9
Hu ZY, Wang GX, Sun XY, Zhu MZ, Song CL, Huang KW, Chen XP (2018) Spatial-temporal patterns of evapotranspiration along an elevation gradient on Mount Gongga, Southwest China. Water Resour Res 54(6):4180–4192. https://doi.org/10.1029/2018wr022645
Hu ZY, Sun SQ, Sun XY, Lin S, Song CL, Wang GX (2023) Controlling factors of the spatial-temporal fluctuations in evapotranspiration along an elevation gradient across humid montane ecosystems. Water Resour Res. https://doi.org/10.1029/2022WR033228
Ji S, Tong L, Kang S, Li F, Lu H, Du T, Li S, Ding R (2017) A modified optimal stomatal conductance model under water-stressed condition. Int J Plant Prod 11(2):295–314
Katul GG, Palmroth S, Oren R (2009) Leaf stomatal responses to vapour pressure deficit under current and CO2-enriched atmosphere explained by the economics of gas exchange. Plant Cell Environ 32(8):968–979. https://doi.org/10.1111/j.1365-3040.2009.01977.x
Katul G, Manzoni S, Palmroth S, Oren R (2010) A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. Ann Bot 105(3):431–442. https://doi.org/10.1093/aob/mcp292
Kolari P, Lappalainen HK, Hanninen H, Hari P (2007) Relationship between temperature and the seasonal course of photosynthesis in Scots pine at northern timberline and in southern boreal zone. Tellus Ser B Chem Phys Meteorol 59(3):542–552. https://doi.org/10.1111/j.1600-0889.2007.00262.x
Körner C, Neumayer M, Menendezriedl SP, Smeetsscheel A (1989) Functional-morphology of mountain plants. Flora 182(5–6):353–383
Li YY et al (2020) Warming effects on morphological and physiological performances of four subtropical montane tree species. Ann for Sci. https://doi.org/10.1007/s13595-019-0910-3
Li QY, Serbin SP, Lamour J, Davidson KJ, Ely KS, Rogers A (2022) Implementation and evaluation of the unified stomatal optimization approach in the functionally assembled terrestrial ecosystem simulator (FATES). Geosci Model Dev 15(11):4313–4329. https://doi.org/10.5194/gmd-15-4313-2022
Lin YS et al (2015) Optimal stomatal behaviour around the world. Nat Clim Change 5(5):459–464. https://doi.org/10.1038/nclimate2550
Liu Z, Hikosaka K, Li F, Zhu L, Jin G (2021) Plant size, environmental factors and functional traits jointly shape the stem radius growth rate in an evergreen coniferous species across ontogenetic stages. J Plant Ecol 14(2):257–269. https://doi.org/10.1093/jpe/rtaa093
Lloyd J, Farquhar GD (1994) C-13 discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99(3–4):201–215. https://doi.org/10.1007/bf00627732
Mäkelä A, Berninger F, Hari P (1996) Optimal control of gas exchange during drought: theoretical analysis. Ann Bot 77(5):461–467. https://doi.org/10.1006/anbo.1996.0056
Manzoni S, Vico G, Katul G, Fay PA, Polley W, Palmroth S, Porporato A (2011) Optimizing stomatal conductance for maximum carbon gain under water stress: a meta-analysis across plant functional types and climates. Funct Ecol 25(3):456–467. https://doi.org/10.1111/j.1365-2435.2010.01822.x
Marron N, Villar M, Dreyer E, Delay D, Boudouresque E, Petit JM, Delmotte FM, Guehl JM, Brignolas F (2005) Diversity of leaf traits related to productivity in 31 Populus deltoides x Populus nigra clones. Tree Physiol 25(4):425–435. https://doi.org/10.1093/treephys/25.4.425
Mayor JR et al (2017) Elevation alters ecosystem properties across temperate treelines globally. Nature 542(7639):91–95. https://doi.org/10.1038/nature21027
Medlyn BE et al (2011a) Reconciling the optimal and empirical approaches to modelling stomatal conductance. Glob Change Biol 17(6):2134–2144. https://doi.org/10.1111/j.1365-2486.2010.02375.x
Medlyn BE, Duursma RA, Zeppel MJB (2011b) Forest productivity under climate change: a checklist for evaluating model studies. Wiley Interdiscip Rev Clim Change 2(3):332–355. https://doi.org/10.1002/wcc.108
Medlyn BE, Duursma RA, De Kauwe MG, Prentice IC (2013) The optimal stomatal response to atmospheric CO2 concentration: alternative solutions, alternative interpretations. Agric for Meteorol 182:200–203. https://doi.org/10.1016/j.agrformet.2013.04.019
Mekonnen ZA et al (2021) Arctic tundra shrubification: a review of mechanisms and impacts on ecosystem carbon balance. Environ Res Lett 16(5):10. https://doi.org/10.1088/1748-9326/abf28b
Motavita DF, Chow R, Guthke A, Nowak W (2019) The comprehensive differential split-sample test: a stress-test for hydrological model robustness under climate variability. J Hydrol 573:501–515. https://doi.org/10.1016/j.jhydrol.2019.03.054
Nikinmaa E, Holtta T, Hari P, Kolari P, Makela A, Sevanto S, Vesala T (2013) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant Cell Environ 36(3):655–669. https://doi.org/10.1111/pce.12004
Oliveira BF, Machac A, Costa GC, Brooks TM, Davidson AD, Rondinini C, Graham CH (2016) Species and functional diversity accumulate differently in mammals. Glob Ecol Biogeogr 25(9):1119–1130. https://doi.org/10.1111/geb.12471
Pathare VS, Crous KY, Cooke J, Creek D, Ghannoum O, Ellsworth DS (2017) Water availability affects seasonal CO2-induced photosynthetic enhancement in herbaceous species in a periodically dry woodland. Glob Change Biol 23(12):5164–5178. https://doi.org/10.1111/gcb.13778
Peters RL et al (2019) Contrasting stomatal sensitivity to temperature and soil drought in mature alpine conifers. Plant Cell Environ 42(5):1674–1689. https://doi.org/10.1111/pce.13500
Prentice IC, Dong N, Gleason SM, Maire V, Wright IJ (2014) Balancing the costs of carbon gain and water transport: testing a new theoretical framework for plant functional ecology. Ecol Lett 17(1):82–91. https://doi.org/10.1111/ele.12211
Qi Y et al (2023) Applicability of stomatal conductance models comparison for persistent water stress processes of spring maize in water resources limited environmental zone. Agric Water Manag. https://doi.org/10.1016/j.agwat.2022.108090
Shipley B, Lechowicz MJ (2000) The functional co-ordination of leaf morphology, nitrogen concentration, and gas exchange in 40 wetland species. Ecoscience 7(2):183–194. https://doi.org/10.1080/11956860.2000.11682587
Simin T, Davie-Martin CL, Petersen J, Hoye TT, Rinnan R (2022) Impacts of elevation on plant traits and volatile organic compound emissions in deciduous tundra shrubs. Sci Tot Environ. https://doi.org/10.1016/j.scitotenv.2022.155783
Stefanski A, Butler EE, Bermudez R, Montgomery RA, Reich PB (2022) Stomatal behaviour moderates the water cost of CO2 acquisition for 21 boreal and temperate species under experimental climate change. Plant Cell Environ. https://doi.org/10.1111/pce.14559
Sun HY, Wu YH, Zhou J, Bing HJ, Chen Y, Li N (2020a) Labile fractions of soil nutrients shape the distribution of bacterial communities towards phosphorus recycling systems over elevation gradients in Gongga Mountain SW, China. Eur J Soil Biol. https://doi.org/10.1016/j.ejsobi.2020.103185
Sun JY, Sun XY, Hu ZY, Wang GX (2020b) Exploring the influence of environmental factors in partitioning evapotranspiration along an elevation gradient on Mount Gongga, eastern edge of the Qinghai-Tibet Platea, China. J Mt Sci 17(2):384–396. https://doi.org/10.1007/s11629-019-5687-1
Tang Z, Zhai B, Wang G, Gessler A, Sun S, Hu Z (2023) Elevational variations in stem hydraulic efficiency and safety of Abies fabri. Funct Ecol. https://doi.org/10.1111/1365-2435.14408
Tao J et al (2018) Elevation-dependent effects of climate change on vegetation greenness in the high mountains of southwest China during 1982–2013. Int J Climatol 38(4):2029–2038. https://doi.org/10.1002/joc.5314
Tenkanen A, Keski-Saari S, Salojarvi J, Oksanen E, Keinanen M, Kontunen-Soppela S (2020) Differences in growth and gas exchange between southern and northern provenances of silver birch (Betula pendula Roth) in northern Europe. Tree Physiol 40(2):198–214. https://doi.org/10.1093/treephys/tpz124
Thomas DS, Eamus D, Bell D (1999) Optimization theory of stomatal behaviour-II. Stomatal responses of several tree species of north Australia to changes in light, soil and atmospheric water content and temperature. J Exp Bot 50(332):393–400. https://doi.org/10.1093/jxb/50.332.393
Tranquil W (1964) Physiology of plants at high altitudes. Ann Rev Plant Physiol 15:345–362. https://doi.org/10.1146/annurev.pp.15.060164.002021
Wang QL, He QJ, Zhou GS (2018) Applicability of common stomatal conductance models in maize under varying soil moisture conditions. Sci Total Environ 628–629:141–149. https://doi.org/10.1016/j.scitotenv.2018.01.291
Wang Z, Liu X, Zhu Z, Bao MW (2022) Comparisons of photosynthesis-related traits among understory lichens, mosses and vascular plant leaves in a high-elevation subalpine forest. J Plant Ecol 15(4):683–690. https://doi.org/10.1093/jpe/rtab109
Wu T et al (2020) Long-term effects of 7-year warming experiment in the field on leaf hydraulic and economic traits of subtropical tree species. Glob Change Biol 26(12):7144–7157. https://doi.org/10.1111/gcb.15355
Xu LK, Baldocchi DD (2003) Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiol 23(13):865–877. https://doi.org/10.1093/treephys/23.13.865
Zenes N, Kerr KL, Trugman AT, Anderegg WRL (2020) Competition and drought alter optimal stomatal strategy in tree seedlings. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00478
Zheng L, Shi GNP (2021) High-altitude tree growth responses to climate change across the Hindu Kush Himalaya. J Plant Ecol 14(5):829–842. https://doi.org/10.1093/jpe/rtab035
Acknowledgements
We express our gratitude to Zishu Tang for her contribution to the field measurements. We also thank Zhaoyong Hu for his writing assistance and Genxu Wang and Shouqin Sun for proofreading the article and providing valuable feedback on the manuscript. All authors reviewed the manuscript.
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This work was financed by the National Natural Science Foundation of China (grant number 42330508, 42271063) and the National Key Research and Development Program of China (grant number 2022FY100205), the Fundamental Research Funds for the Central Universities (YJ202079), and the National Natural Science Foundation of China (grant number 41901053).
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Zhai, B., Wang, G., Hu, Z. et al. Marginal water use efficiencies of different plant functional types along an elevation gradient in subalpine regions. Eur J Forest Res 143, 773–784 (2024). https://doi.org/10.1007/s10342-023-01654-w
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DOI: https://doi.org/10.1007/s10342-023-01654-w