Abstract
Plant secondary metabolites (PSMs) defend plants against abiotic stresses, including those caused by climate change and against biotic stresses, such as herbivory and competition. There is a trade-off between allocating available carbon to growth and defence in stressful environments. However, our knowledge about trade-off is limited, especially when abiotic and biotic stresses co-occur. We aimed to understand the combined effect of increasing precipitation and humidity, the tree's competitive status, and canopy position on leaf secondary metabolites (LSMs) and fine root secondary metabolites (RSMs) in Betula pendula. We sampled 8-year-old B. pendula trees growing in the free air humidity manipulation (FAHM) experimental site, where treatments included elevated relative air humidity and elevated soil moisture. A high-performance liquid chromatography–quadrupole-time of flight mass spectrometer (HPLC–qTOF-MS) was used to analyse secondary metabolites. Our results showed accumulation of LSM depends on the canopy position and competitive status. Flavonoids (FLA), dihydroxybenzoic acids (HBA), jasmonates (JA) and terpene glucosides (TG) were higher in the upper canopy, and FLA, monoaryl compounds (MAR) and sesquiterpenoids (ST) were higher in dominant trees. The FAHM treatments had a more distinct effect on RSM than on LSM. The RSMs were lower in elevated air humidity and soil moisture conditions than in control conditions. The RSM content depended on the competitive status and was higher in suppressed trees. Our study suggests that young B. pendula will allocate similar amounts of carbon to constitutive chemical leaf defence, but a lower amount to root defence (per fine root biomass) under higher humidity.
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 this study will be available from the corresponding author upon reasonable request.
Code availability
Not applicable.
References
Agati G, Cerovic ZG, Pinelli P, Tattini M (2011) Light-induced accumulation of ortho-dihydroxylated flavonoids as non-destructively monitored by chlorophyll fluorescence excitation techniques. Environ Exp Bot 73:3–9. https://doi.org/10.1016/j.envexpbot.2010.10.002
Baraza E, Gómez JM, Hódar JA, Zamora R (2004) Herbivory has a greater impact in shade than in sun: response of Quercus pyrenaica seedlings to multifactorial environmental variation. Can J Botany 82:357–364. https://doi.org/10.1139/B04-004
Braak CJF ter, Smilauer P (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (version 4.5). www.canoco.com, 33, Biometris (WU MAT),
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:1–16. https://doi.org/10.3389/fpls.2015.00547
Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368. https://doi.org/10.2307/3544308
Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20. https://doi.org/10.1016/j.plaphy.2013.05.009
Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the Barnacle Chthamalus Stellatus. Ecology 42:710–723. https://doi.org/10.2307/1933500
Danell K, Haukioja E, Huss-Danell K (1997) Morphological and chemical responses of mountain birch leaves and shoots to winter browsing along a gradient of plant productivity. Écoscience 4:296–303. https://doi.org/10.1080/11956860.1997.11682408
De La Rosa TM, Julkunen-Tiitto R, Lehto T, Aphalo PJ (2001) Secondary metabolites and nutrient concentrations in silver birch seedlings under five levels of daily UV-B exposure and two relative nutrient addition rates. New Phytol 150:121–131. https://doi.org/10.1046/j.1469-8137.2001.00079.x
Dey PM, Brownleader MD, Harborne JB (1997) The plant, the cell and its molecular components. In: Deyo PM, Harborne JBBT-PB (eds) Plant Biochemistry. Academic Press, London, pp 1–47
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097. https://doi.org/10.2307/3870059
Dongh YH, Mitra D, Kootstra A, Lister C, Lancaster J (1995) Postharvest stimulation of skin color in royal gala apple. J Am Soc Hortic Sci 120:95–100. https://doi.org/10.21273/jashs.120.1.95
Downum K, Lee D, Hallé F, Quirke M, Towers N (2001) Plant secondary compounds in the canopy and understorey of a tropical rain forest in Gabon. J Trop Ecol 17:477–481. https://doi.org/10.1017/S0266467401001341
Elger A, Lemoine DG, Fenner M, Hanley ME (2009) Plant ontogeny and chemical defence: older seedlings are better defended. Oikos 118:767–773. https://doi.org/10.1111/J.1600-0706.2009.17206.X
Elowson S (1996) Birch – a high-producing species? – Perttu K, Koppel A (eds) Short rotation willow coppice for renewable energy and improved environment. Uppsala, Swedish Univ for Agricultural Sciences, pp 107–112
Fanourakis D, Aliniaeifard S, Sellin A, Giday H, Körner O, Rezaei Nejad A et al (2020) Stomatal behavior following mid- or long-term exposure to high relative air humidity: a review. Plant Physiol Biochem 153:92–105. https://doi.org/10.1016/j.plaphy.2020.05.024
Gershenzon J, Croteau Rodney (1991) Terpenoids. Herbiv their Interact with Second Plant Metab 165–219. https://doi.org/10.1016/B978-0-12-597183-6.50010-3
Hansen AH, Jonasson S, Michelsen A, Julkunen-Tiitto R (2006) Long-term experimental warming, shading and nutrient addition affect the concentration of phenolic compounds in arctic-alpine deciduous and evergreen dwarf shrubs. Oecologia 147:1–11. https://doi.org/10.1007/s00442-005-0233-y
Hansen R, Mander Ü, Soosaar K, Maddison M, Lõhmus K, Kupper P et al (2013) Greenhouse gas fluxes in an open air humidity manipulation experiment. Landsc Ecol 28:637–649. https://doi.org/10.1007/s10980-012-9775-7
Hartley SE, Firn RD (1989) Phenolic biosynthesis, leaf damage, and insect herbivory in birch (Betula pendula). J Chem Ecol 15:275–283. https://doi.org/10.1007/BF02027789
Haukioja E, Niemelä P (1979) Birch leaves as a resource for herbivores: seasonal occurrence of increased resistance in foliage after mechanical damage of adjacent leaves. Oecologia 39:151–159. https://doi.org/10.1007/BF00348065
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. https://doi.org/10.1086/417659
Heyworth CJ, Iason GR, Temperton V, Jarvis PG, Duncan AJ (1998) The effect of elevated CO2 concentration and nutrient supply on carbon-based plant secondary metabolites in Pinus sylvestris L. Oecologia 115:344–350. https://doi.org/10.1007/s004420050526
Hobbie EA, Agerer R (2010) Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327:71–83. https://doi.org/10.1007/s11104-009-0032-z
Hofland-Zijlstra JD, Berendse F (2009) The effect of nutrient supply and light intensity on tannins and mycorrhizal colonisation in Dutch heathland ecosystems. Plant Ecol 201:661–675. https://doi.org/10.1007/s11258-008-9554-3
Hynynen J, Niemistö P, Viherä-Aarnio A, Brunner A, Hein S, Velling P (2010) Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in Northern Europe. Forestry 83:103–119. https://doi.org/10.1093/forestry/cpp035
Iason GR, Dicke M, Hartley SE (2012) The integrative roles of plant secondary metabolites in natural systems. Ecol Plant Second Metab. https://doi.org/10.1017/cbo9780511675751.002
Idris A, Linatoc AC, Abu Bakar MF, Ibrahim Takai Z, Audu Y (2018) Effect of light quality and quantity on the accumulation of flavonoid in plant species. J Sci Technol 10:32–45. https://doi.org/10.30880/jst.2018.10.03.006
IUSS Working Group WRB (2007) World reference base for soil resources 2006. First update 2007. World Soil Resour Rep No. 103. (FAO: Rome)
Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012) Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiol 160:1719–1727. https://doi.org/10.1104/pp.112.206524
Johnson SN, Erb M, Hartley SE (2016) Roots under attack: contrasting plant responses to below- and aboveground insect herbivory. New Phytol 210:413–418. https://doi.org/10.1111/NPH.13807
Jones T, Kulseth S, Mechtenberg K, Jorgenson C, Zehfus M, Brown P et al (2006) Simultaneous evolution of competitiveness and defense: Induced switching in Arabis drummondii. Plant Ecol 184:245–257. https://doi.org/10.1007/s11258-005-9070-7
Julkunen-Tiitto R, Rousi M, Bryant J, Sorsa S, Keinänen M, Sikanen H (1996) Chemical diversity of several Betulaceae species: comparison of phenolics and terpenoids in northern birch stems. Trees - Struct Funct 11:16–22. https://doi.org/10.1007/s004680050053
Kanerva T, Regina K, Rämö K, Ojanperä K, Manninen S (2007) Fluxes of N2O, CH4 and CO2 in a meadow ecosystem exposed to elevated ozone and carbon dioxide for three years. Environ Pollut 145:818–828. https://doi.org/10.1016/j.envpol.2006.03.055
Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242. https://doi.org/10.1016/j.tplants.2005.03.002
Koide T, Saito H, Shirota T, Lopez LML, Maximov TC, Hasegawa S et al (2010) Effects of changes in the soil environment associated with heavy precipitation on soil greenhouse gas fluxes in a Siberian larch forest near Yakutsk. Soil Sci Plant Nutr 56:645–662. https://doi.org/10.1111/j.1747-0765.2010.00484.x
Komenda M, Koppmann R (2002) Monoterpene emissions from Scots pine (Pinus sylvestris): field studies of emission rate variabilities. J Geophys Res 107:1–13. https://doi.org/10.1029/2001JD000691
Koricheva J, Haukioja E (1995) Variations in chemical composition of birch foliage under air pollution stress and their consequences for Eriocrania miners. Environ Pollut 88:41–50. https://doi.org/10.1016/0269-7491(95)91046-N
Kotilainen T, Tegelberg R, Julkunen-Tiitto R, Lindfors A, Aphalo PJ (2008) Metabolite specific effects of solar UV-A and UV-B on alder and birch leaf phenolics. Glob Chang Biol 14:1294–1304. https://doi.org/10.1111/j.1365-2486.2008.01569.x
Król A, Amarowicz R, Weidner S (2014) Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress. Acta Physiol Plant 36:1491–1499. https://doi.org/10.1007/s11738-014-1526-8
Kuokkanen K, Yan S, Niemelä P (2003) Effects of elevated CO2 and temperature on the leaf chemistry of birch Betula pendula (Roth) and the feeding behaviour of the weevil Phyllobius maculicornis. Agric for Entomol 5:209–217. https://doi.org/10.1046/j.1461-9563.2003.00177.x
Kupper P, Sõber J, Sellin A, Tullus A, Räim O, Lubenets K et al (2011) An experimental facility for free air humidity manipulation (FAHM) can alter water flux through deciduous tree canopy. Environ Exp Bot 72:432–438. https://doi.org/10.1016/j.envexpbot.2010.09.003
Kupper P, Rohula G, Inno L, Ostonen I, Sellin A, Sõber A (2017) Impact of high daytime air humidity on nutrient uptake and night-time water flux in silver birch, a boreal forest tree species. Reg Environ Chang 17:2149–2157. https://doi.org/10.1007/s10113-016-1092-2
Lam SK, Lin E, Norton R, Chen D (2011) The effect of increased atmospheric carbon dioxide concentration on emissions of nitrous oxide, carbondioxide and methane from a wheat field in a semi-arid environment in northern China. Soil Biol Biochem 43:458–461. https://doi.org/10.1016/j.soilbio.2010.10.012
Lankau RA (2012) Coevolution between invasive and native plants driven by chemical competition and soil biota. Proc Natl Acad Sci USA 109:11240–11245. https://doi.org/10.1073/pnas.1201343109
Lavola A (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiol 18:53–58. https://doi.org/10.1093/treephys/18.1.53
Lihavainen J, Keinänen M, Keski-Saari S, Kontunen-Soppela S, Sõber A, Oksanen E (2016) Artificially decreased vapour pressure deficit in field conditions modifies foliar metabolite profiles in birch and aspen. J Exp Bot 67:4367–4378. https://doi.org/10.1093/jxb/erw219
Lindner M, Fitzgerald JB, Zimmermann NE, Reyer C, Delzon S, van der Maaten E et al (2014) Climate change and European forests: what do we know, what are the uncertainties, and what are the implications for forest management? J Environ Manage 146:69–83. https://doi.org/10.1016/j.jenvman.2014.07.030
Litvak ME, Constable JVH, Monson RK (2002) Supply and demand processes as controls over needle monoterpene synthesis and concentration in Douglas fir [Pseudotsuga menziesii (Mirb.) Franco]. Oecologia 132:382–391. https://doi.org/10.1007/s00442-002-0964-y
Llusià J, Peñ J, Alessio GA, Estiarte M (2006) Seasonal contrasting changes of foliar concentrations of terpenes and other volatile organic compound in four dominant species of a Mediterranean shrubland submitted to a field experimental drought and warming. Physiol Plant 127:632–649. https://doi.org/10.1111/j.1399-3054.2006.00693.x
Loponen J, Ossipov V, Lempa K, Haukioja E, Pihlaja K (1998) Concentrations and among-compound correlations of individual phenolics in white birch leaves under air pollution stress. Chemosphere 37:1445–1456. https://doi.org/10.1016/S0045-6535(98)00135-0
Lutter R, Tullus A, Kanal A, Tullus T, Vares A, Tullus H (2015) Growth development and plant–soil relations in midterm silver birch (Betula pendula Roth) plantations on previous agricultural lands in hemiboreal Estonia. Eur J for Res 134:653–667. https://doi.org/10.1007/s10342-015-0879-x
McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320. https://doi.org/10.1086/282909
Mikkelsen TN, Beier C, Jonasson S, Holmstrup M, Schmidt IK, Ambus P et al (2008) Experimental design of multifactor climate change experiments with elevated CO2, warming and drought: the CLIMAITE project. Funct Ecol 22:185–195. https://doi.org/10.1111/j.1365-2435.2007.01362.x
Ministry of the Environment of the Republic of Estonia (2021) Kliimamuutuste olemus | Keskkonnaministeerium. https://envir.ee/kliima/kliima/kliimamuutuste-olemus#kliimamuutused-ja-pr. Accessed 9 May 2022
Mooney HA, Drake BG, Luxmoore RJ, Oechel WC, Pitelka LF (1991) Predicting ecosystem responses to elevated CO2 concentrations. Bioscience 41:96–104. https://doi.org/10.2307/1311562
Mosier AR, Morgan JA, King JY, LeCain D, Milchunas DG (2002) Soil-atmosphere exchange of CH4, CO2, NOx, and N2O in the Colorado shortgrass steppe under elevated CO2. Plant Soil 240:201–211. https://doi.org/10.1023/A:1015783801324
Niemistö P (1995) Influence of initial spacing and row-to-row distance on the growth and yield of silver birch (betula pendula). Scand J for Res 10:245–255. https://doi.org/10.1080/02827589509382890
Niglas A, Kupper P, Tullus A, Sellin A (2014) Responses of sap flow, leaf gas exchange and growth of hybrid aspen to elevated atmospheric humidity under field conditions. AoB Plants 6:1–14. https://doi.org/10.1093/aobpla/plu021
Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant, Cell Environ 30:1052–1071. https://doi.org/10.1111/j.1365-3040.2007.01683.x
Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741. https://doi.org/10.1111/j.1365-3040.2009.01979.x
Ostonen I, Lõhmus K, Lasn R (1999) The role of soil conditions in fine root ecomorphology in Norway spruce (Picea abies (L.) Karst.). Plant Soil 208:283–292. https://doi.org/10.1023/A:1004552907597
Parts K, Tedersoo L, Lõhmus K, Kupper P, Rosenvald K, Sõber A et al (2013) Increased air humidity and understory composition shape short root traits and the colonizing ectomycorrhizal fungal community in silver birch stands. For Ecol Manage 310:720–728. https://doi.org/10.1016/j.foreco.2013.09.017
Peñuelas J, Llusià J (1997) Effects of carbon dioxide, water supply, and seasonality on terpene content and emission by Rosmarinus officinalis. J Chem Ecol 23:979–993. https://doi.org/10.1023/B:JOEC.0000006383.29650.d7
Poeydebat C, Jactel H, Moreira X, Koricheva J, Barsoum N, Bauhus J et al (2020) Climate affects neighbour-induced changes in leaf chemical defences and tree diversity-herbivory relationships. Funct Ecol 35:67–81. https://doi.org/10.1111/1365-2435.13700
Powell JS, Raffa KF (1999) Sources of variation in concentration and composition of foliar monoterpenes in tamarack (Larix laricina) seedlings: roles of nutrient availability, time of season, and plant architecture. J Chem Ecol 25:1771–1797. https://doi.org/10.1023/A:1020973514476
Ramachandra Rao S, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153. https://doi.org/10.1016/S0734-9750(02)00007-1
Rosenvald K, Tullus A, Ostonen I, Uri V, Kupper P, Aosaar J et al (2014) The effect of elevated air humidity on young silver birch and hybrid aspen biomass allocation and accumulation - acclimation mechanisms and capacity. For Ecol Manage 330:252–260. https://doi.org/10.1016/j.foreco.2014.07.016
Rosenvald K, Lõhmus K, Rohula-Okunev G, Lutter R, Kupper P, Tullus A (2020) Elevated atmospheric humidity prolongs active growth period and increases leaf nitrogen resorption efficiency of silver birch. Oecologia 193:449–460. https://doi.org/10.1007/s00442-020-04688-8
Rusalepp L, Lutter R, Hepner H, Kaasik A, Tullus A (2021) Secondary metabolites in leaves of hybrid aspen are affected by the competitive status and early thinning in dense coppices. Ann for Sci 78:1. https://doi.org/10.1007/s13595-020-01014-3
Sellin A, Tullus A, Niglas A, Õunapuu E, Karusion A, Lõhmus K (2013) Humidity-driven changes in growth rate, photosynthetic capacity, hydraulic properties and other functional traits in silver birch (Betula pendula). Ecol Res 28:523–535. https://doi.org/10.1007/s11284-013-1041-1
Sellin A, Alber M, Keinänen M, Kupper P, Lihavainen J, Lõhmus K et al (2017) Growth of northern deciduous trees under increasing atmospheric humidity: possible mechanisms behind the growth retardation. Reg Environ Chang 17:2135–2148. https://doi.org/10.1007/S10113-016-1042-Z
Shelton AL (2000) Variable chemical defences in plants and their effects on herbivore behaviour. Evol Ecol Res 2:231–249
Snow MD, Bard RR, Olszyk DM, Minster LM, Hager AN, Tingey DT (2003) Monoterpene levels in needles of Douglas fir exposed to elevated CO2 and temperature. Physiol Plant 117:352–358. https://doi.org/10.1034/j.1399-3054.2003.00035.x
Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55. https://doi.org/10.1086/367580
Sutinen R, Teirilä A, Pänttäjä M, Sutinen ML (2002) Distribution and diversity of tree species with respect to soil electrical characteristics in Finnish Lapland. Can J for Res 32:1158–1170. https://doi.org/10.1139/x02-076
Svyatyna K, Riemann M (2012) Light-dependent regulation of the jasmonate pathway. Protoplasma 249:137–145. https://doi.org/10.1007/s00709-012-0409-3
Takahashi A, Takeda K, Ohnishi T (1991) Light-induced anthocyanin reduces the extent of damage to DNA in UV-irradiated Centaurea cyanus cells in culture. Plant Cell Physiol 32:541–547. https://doi.org/10.1016/0165-1161(92)91606-r
Team R core (2022) R: The r project for statistical computing. https://www.r-project.org/. Accessed 27 Jul 2022
Tegelberg R, Julkunen-Tiitto R (2001) Quantitative changes in secondary metabolites of dark-leaved willow (Salix myrsinifolia) exposed to enhanced ultraviolet-B radiation. Physiol Plant 115:174. https://doi.org/10.1034/j.1399-3054.2002.1150120.x
Thorpe AS, Aschehoug ET, Atwater DZ, Callaway RM (2011) Interactions among plants and evolution. J Ecol 99:729–740. https://doi.org/10.1111/j.1365-2745.2011.01802.x
Tullus A, Kupper P, Sellin A, Parts L, Sõber J, Tullus T et al (2012) Climate change at Northern latitudes: rising atmospheric humidity decreases transpiration, N-uptake and growth rate of hybrid aspen. PLoS ONE 7:e42648. https://doi.org/10.1371/journal.pone.0042648
Tullus A, Kupper P, Kaasik A, Tullus H, Lõhmus K, Sõber A et al (2017) The competitive status of trees determines their responsiveness to increasing atmospheric humidity – a climate trend predicted for northern latitudes. Glob Chang Biol 23:1961–1974. https://doi.org/10.1111/GCB.13540
Tullus A, Rosenvald K, Lutter R, Kaasik A, Kupper P, Sellin A (2020) Coppicing improves the growth response of short-rotation hybrid aspen to elevated atmospheric humidity. For Ecol Manage 459:117825. https://doi.org/10.1016/j.foreco.2019.117825
Tullus A, Rusalepp L, Lutter R, Rosenvald K, Kaasik A, Rytter L et al (2021) Climate and competitive status modulate the variation in secondary metabolites more in leaves than in fine roots of Betula pendula. Front Plant Sci 12:2746. https://doi.org/10.3389/fpls.2021.746165
Ullah C, Unsicker SB, Reichelt M, Gershenzon J, Hammerbacher A (2019) Accumulation of catechin and proanthocyanidins in black poplar stems after infection by Plectosphaerella populi: hormonal regulation, biosynthesis and antifungal activity. Front Plant Sci 10:1–15. https://doi.org/10.3389/fpls.2019.01441
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in annals of botany. Ann Bot 111:1021–1058. https://doi.org/10.1093/aob/mct067
Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ et al (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169. https://doi.org/10.1111/nph.14003
Weiner J (1986) How competition for light and nutrients affects size variability in ipomoea tricolor populations. Ecology 67:1425–1427. https://doi.org/10.2307/1938699
Williams MA, Rice CW, Owensby CE (2000) Carbon dynamics and microbial activity in tallgrass prairie exposed to elevated CO2 for 8 years. Plant Soil 227:127–137. https://doi.org/10.1023/A:1026590001307
Zhao YH, Jia X, Wang WK, Liu T, Huang SP, Yang MY (2016) Growth under elevated air temperature alters secondary metabolites in Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soils. Sci Total Environ 565:586–594. https://doi.org/10.1016/j.scitotenv.2016.05.058
Zwetsloot MJ, Ucros JM, Wickings K, Wilhelm RC, Sparks J, Buckley DH et al (2020) Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil. Soil Biol Biochem 145:107797. https://doi.org/10.1016/j.soilbio.2020.107797
Acknowledgements
We are thankful to Riho Meier and Urmas Lanto for the maintenance and technical supervision of the FAHM experiment in 2019. We also thank the laboratory of plant biochemistry at the Estonian University of Life Sciences for measuring foliar nutrients.
Funding
This work was supported by the Estonian Research Council grants PSG7, PRG1434, and PRG916 and by the European Commission's Horizon 2020 programme under grant agreement no. 101000406 (project ONEforest).
Author information
Authors and Affiliations
Contributions
AT conceived the idea, AT and PK set up the experimental design, and AT and PM supervised the study. RL, KR, and GR conducted the sampling, LR conducted the laboratory work for chemical analysis, GR conducted the laboratory work for fine root samples and KR for leaf biomass, BK, AT, and BB conducted the statistical analysis in cooperation with AK. BK wrote the manuscript with support from AT. All authors contributed to the improvement and revision of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare they have no competing interests.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Ülo Niinemets.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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
Kharel, B., Rusalepp, L., Bhattarai, B. et al. Effects of air humidity and soil moisture on secondary metabolites in the leaves and roots of Betula pendula of different competitive status. Oecologia 202, 193–210 (2023). https://doi.org/10.1007/s00442-023-05388-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-023-05388-9