Searching for a universal indicator of plant stress: a three-year study of three woody species in three environmental gradients in boreal forests

Mikhail V. Kozlov , Vitali Zverev , Elena L. Zvereva

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 99

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Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 99 DOI: 10.1007/s11676-025-01891-2
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Searching for a universal indicator of plant stress: a three-year study of three woody species in three environmental gradients in boreal forests

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Abstract

Stress in plants refers to adverse changes in their functioning. The occurrence and intensity of a stress can be assessed by alterations in plant traits, termed stress indicators. The ultimate goal of this study was to test whether six morpho-physiological plant traits, frequently used as stress indicators, respond consistently across species to various environmental stressors, with the aim of detecting universal stress indicators in forest tree species. We examined changes in vertical increment, leaf/needle size, shoot length, needle longevity, photosynthetic efficiency and fluctuating asymmetry in three common European tree species, mountain birch (Betula pubescens var. pumila), Norway spruce (Picea abies) and Scots pine (Pinus sylvestris) along three environmental gradients (elevation, pollution and seashore) from forests to stressful open environments. Data were collected in 2003, 2004 and 2005 from 297 trees growing naturally across 36 sites in north-western Russia. Fluctuating asymmetry was the only trait that did not vary among sites with differing levels of environmental stress. Leaf/needle size and shoot length occasionally changed along stress gradients, but the magnitude and direction of these changes differed by gradient type and species, resulting in no significant overall stress effect for either trait. In contrast, photosynthetic efficiency, vertical increment and needle longevity consistently decreased from low-stress to high-stress sites. The overall effect was significant for each of these three traits despite the magnitudes of these decreases differed depending on the gradient type and location, species, study year and individual tree. Replication at spatial, temporal and taxonomic levels ensured the robustness and reliability of our results that photosynthetic efficiency, vertical growth and needle longevity reliably captured a general stress syndrome and may serve as stress indicators in forest species.

The online version is available at https://link.springer.com/

Corresponding editor: Tao Xu

The online version contains supplementary material available at https://doi.org/10.1007/s11676-025-01891-2.

Keywords

Environmental stress gradients / Fluctuating asymmetry / Leaf size / Photosynthetic efficiency / Shoot length

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Mikhail V. Kozlov, Vitali Zverev, Elena L. Zvereva. Searching for a universal indicator of plant stress: a three-year study of three woody species in three environmental gradients in boreal forests. Journal of Forestry Research, 2025, 36(1): 99 DOI:10.1007/s11676-025-01891-2

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References

[1]

AertsR. The advantages of being evergreen. Trends Ecol Evol, 1995, 10(10): 402-407.

[2]

AndreucciF, BarbatoR, MassaN, BertaG. Phytosociological, phenological and photosynthetic analyses of the vegetation of a highly polluted site. Plant Biosyst Int J Deal Aspects Plant Biol, 2006, 140(2): 176-189.

[3]

BansalS, GerminoMJ. Variation in ecophysiological properties among conifers at an ecotonal boundary: comparison of establishing seedlings and established adults at timberline. J Veg Sci, 2010, 21(1): 133-142.

[4]

BowmanDMJS, BrienenRJW, GloorE, PhillipsOL, PriorLD. Detecting trends in tree growth: not so simple. Trends Plant Sci, 2013, 18(1): 11-17.

[5]

BresticM, AllakhverdievSI. Photosynthesis under biotic and abiotic environmental stress. Cells, 2022, 11243953.

[6]

BussottiF, PollastriniM. Revisiting the concept of stress in forest trees at the time of global change and issues for stress monitoring. Plant Stress, 2021, 2. 100013

[7]

ChauhanJ, PrathibhaM, SinghP, ChoyalP, MishraUN, SahaD, KumarR, AnuragiH, PandeyS, BoseB, MehtaB, DeyP, DwivediKK, GuptaNK, SinghalRK. Plant photosynthesis under abiotic stresses: damages, adaptive, and signaling mechanisms. Plant Stress, 2023, 10100296.

[8]

ClarkAJ, LandoltW, BucherJB, StrasserRJ. How wind affects the photosynthetic performance of trees: quantified with chlorophyll a fluorescence and open-top chambers. Photosynthetica, 2000, 38(3): 349-360.

[9]

CornelissenT, StilingP. Similar responses of insect herbivores to leaf fluctuating asymmetry. Arthropod Plant Interact, 2011, 5(1): 59-69.

[10]

CoryST, WoodLK, NeufeldHS. Phenology and growth responses of Fraser fir (Abies fraseri) Christmas trees along an elevational gradient, southern Appalachian Mountains, USA. Agric for Meteor, 2017, 243: 25-32.

[11]

CramerGR, UranoK, DelrotS, PezzottiM, ShinozakiK. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol, 2011, 11163.

[12]

DaleVH, BeyelerSC. Challenges in the development and use of ecological indicators. Ecol Indic, 2001, 1(1): 3-10.

[13]

DaleyPF. Chlorophyll fluorescence analysis and imaging in plant stress and disease. Can J Plant Pathol, 1995, 17(2): 167-173.

[14]

Dässler HG (ed) (1976) Einfluß von Luftverunreinigungen auf die Vegetation. Ursachen, Wirkungen, Gegenmaßnahmen. Gustav Fischer, Jena (in German)

[15]

De MarcoA, SicardP, FengZZ, AgathokleousE, AlonsoR, AraminieneV, AugustatisA, BadeaO, BeasleyJC, BranquinhoC, BruckmanVJ, CollaltiA, David-SchwartzR, DomingosM, DuEZ, GomezHG, HashimotoS, HoshikaY, JakovljevicT, McNultyS, OksanenE, KhaniabadiYO, PrescherAK, SaitanisCJ, SaseH, SchmitzA, VoigtG, WatanabeM, WoodMD, KozlovMV, PaolettiE. Strategic roadmap to assess forest vulnerability under air pollution and climate change. Glob Chang Biol, 2022, 28(17): 5062-5085.

[16]

DobbertinM. Tree growth as indicator of tree vitality and of tree reaction to environmental stress: a review. Eur J for Res, 2005, 124(4): 319-333.

[17]

DuanM, ChangSX. Nitrogen fertilization improves the growth of lodgepole pine and white spruce seedlings under low salt stress through enhancing photosynthesis and plant nutrition. For Ecol Manag, 2017, 404: 197-204.

[18]

EränenJK, KozlovMV. Interactions between mountain birch seedlings from differentiated populations in contrasting environments of subarctic Russia. Plant Ecol, 2009, 200(2): 167-177.

[19]

EwersFW, SchmidR. Longevity of needle fascicles of Pinus longaeva (Bristlecone pine) and other North American pines. Oecologia, 1981, 51(1): 107-115.

[20]

FilazzolaA, CahillJF. Replication in field ecology: Identifying challenges and proposing solutions. Methods Ecol Evol, 2021, 12(10): 1780-1792.

[21]

FreemanDC, GrahamJH, EmlenJM. Developmental stability in plants: symmetries, stress and epigenesis. Genetica, 1993, 89(1): 97-119.

[22]

GavrikovDE, ZverevV, RachenkoMA, PristavkaAA, KozlovMV. Experimental evidence questions the relationship between stress and fluctuating asymmetry in plants. Symmetry, 2023, 152339.

[23]

GottardiniE, CristofoliniF, CristoforiA, CaminF, CalderisiM, FerrettiM. Consistent response of crown transparency, shoot growth and leaf traits on Norway spruce (Picea abies (L.) H. Karst.) trees along an elevation gradient in northern Italy. Ecol Indic, 2016, 60: 1041-1044.

[24]

GrahamJH. Fluctuating asymmetry and developmental instability, a guide to best practice. Symmetry, 2021, 1319.

[25]

GrimeJPPlant strategies and vegetation processes, 1979, New York. Wiley.

[26]

GurevitchJ, HedgesLVSchneiderSM, GurevitchJ. Meta-analysis combining the results of independent experiments. Design and analysis of ecological experiments, 2001, Oxford. Oxford Univ Press. 347369

[27]

HadleyJL, SmithWK. Wind erosion of leaf surface wax in alpine timberline conifers. Arct Alp Res, 1989, 21(4): 392-398.

[28]

HagenSB, ImsRA, YoccozNG, SørlibråtenO. Fluctuating asymmetry as an indicator of elevation stress and distribution limits in mountain birch (Betula pubescens). Plant Ecol, 2008, 195(2): 157-163.

[29]

HassanMU, ChatthaMU, KhanI, ChatthaMB, AamerM, NawazM, AliA, KhanMAU, KhanTA. Nickel toxicity in plants: reasons, toxic effects, tolerance mechanisms, and remediation possibilities-a review. Environ Sci Pollut Res Int, 2019, 26(13): 12673-12688.

[30]

HespPA. Ecological processes and plant adaptations on coastal dunes. J Arid Environ, 1991, 21(2): 165-191.

[31]

JimenezMS, Gonzalez-RodriguezAM, MoralesD, CidMC, SocorroAR, CaballeroM. Evaluation of chlorophyll fluorescence as a tool for salt stress detection in roses. Photosynthetica, 1997, 33(2): 291-301.

[32]

Keleş. The effect of altitude on the growth and development of Trojan fir (Abies nordmanniana subsp. equi-trojani [Asch. & Sint. ex Boiss] Coode & Cullen) saplings. Cerne, 2020, 26(3): 381-392.

[33]

KenwardMG, RogerJH. An improved approximation to the precision of fixed effects from restricted maximum likelihood. Comput Stat Data Anal, 2009, 53(7): 2583-2595.

[34]

KozlovMV. Plant studies on fluctuating asymmetry in Russia: mythology and methodology. Russ J Ecol, 2017, 48(1): 1-9.

[35]

KozlovMV. Blind measurements did not confirm effects of forest fragmentation on fluctuating asymmetry of a tropical butterfly Morpho helenor. Naturwissenschaften, 2024, 111327.

[36]

Kozlov MV (2025) Fluctuating asymmetry in ecological and environmental research: Quo vadis?Funct Ecol 39(1): 4–8. https://doi.org/10.1111/1365-2435.14713

[37]

KozlovMV, ZverevV. Temperature and herbivory, but not pollution, affect fluctuating asymmetry of mountain birch leaves: results of 25-year monitoring around the copper-nickel smelter in Monchegorsk, northwestern Russia. Sci Total Environ, 2018, 640–641: 678-687.

[38]

KozlovMV, ZverevaEL. Confirmation bias in studies of fluctuating asymmetry. Ecol Indic, 2015, 57: 293-297.

[39]

KozlovMV, ZverevaE, ZverevVImpacts of point polluters on terrestrial biota: comparative analysis of 18 contaminated areas, 2009, Dordrecht. Springer.

[40]

KrannerI, MinibayevaFV, BeckettRP, SealCE. What is stress? Concepts, definitions and applications in seed science. New Phytol, 2010, 188(3): 655-673.

[41]

KullmanL. Recent cooling and recession of Norway spruce (Picea abies (L.) Karst.) in the forest—alpine tundra ecotone of the Swedish Scandes. J Biogeogr, 1996, 23(6): 843-854.

[42]

LichtenthalerHK. The stress concept in plants: an introduction. Ann N Y Acad Sci, 1998, 851: 187-198.

[43]

MájekováM, SpringerB, FerencV, GruntmanM, TielbörgerK. Leaf fluctuating asymmetry is not a reliable indicator of stress. Funct Ecol, 2024, 38(6): 1447-1457.

[44]

Maldonado-LópezY, Vaca-SánchezMS, Canché-DelgadoA, García-JaínSE, González-RodríguezA, CornelissenT, Cuevas-ReyesP. Leaf herbivory and fluctuating asymmetry as indicators of mangrove stress. Wetl Ecol Manag, 2019, 27(4): 571-580.

[45]

MidoloG, De FrenneP, HölzelN, WellsteinC. Global patterns of intraspecific leaf trait responses to elevation. Glob Chang Biol, 2019, 25(7): 2485-2498.

[46]

MiszalskiZ, NiewiadomskaE, KępaE, SkawińskiP. Evaluating the superoxide dismutase activity and chlorophyll fluorescence in Picea abies leaves growing at different altitudes. Photosynthetica, 2000, 38(3): 379-384.

[47]

MøllerAP, SwaddleJPAsymmetry, developmental stability, and evolution, 1997, Oxford. Oxford Univ Press.

[48]

NaXY, WangXW, XuHY, QiaoLN, WangS, LiuGF, YerzhanK, BotagozK. Analyzing and evaluating the salt tolerance of four kinds of birch seedlings. Bull Bot Res, 2015, 35(6): 873-882.

[49]

NaumannJC, AndersonJE, YoungDR. Linking physiological responses, chlorophyll fluorescence and hyperspectral imagery to detect salinity stress using the physiological reflectance index in the coastal shrub Myrica cerifera. Remote Sens Environ, 2008, 112(10): 3865-3875.

[50]

NowickaB, CiuraJ, SzymańskaR, KrukJ. Improving photosynthesis, plant productivity and abiotic stress tolerance—current trends and future perspectives. J Plant Physiol, 2018, 231: 415-433.

[51]

Odasz-AlbrigtsenAM, TømmervikH, MurphyP. Decreased photosynthetic efficiency in plant species exposed to multiple airborne pollutants along the Russian–Norwegian border. Can J Bot, 2000, 78(8): 1021-1033.

[52]

OdumEP. Trends expected in stressed ecosystems. Bioscience, 1985, 35(7): 419-422.

[53]

Palmer AR (1999) Detecting publication bias in meta-analyses:A case study of fluctuating asymmetry and sexual selection. American Naturalis 154:220–233. https://doi.org/10.7939/R3JW86Q0Q

[54]

PaulsenJ, KörnerC. A climate-based model to predict potential treeline position around the globe. Alp Bot, 2014, 124(1): 1-12.

[55]

PearcyRW, MuraokaH, ValladaresF. Crown architecture in Sun and shade environments: assessing function and trade-offs with a three-dimensional simulation model. New Phytol, 2005, 166(3): 791-800.

[56]

PolakMDevelopmental Instability: causes and Consequences, 2003, Oxford. Oxford Univ Press.

[57]

ReinhardtK, CastanhaC, GerminoMJ, KueppersLM. Ecophysiological variation in two provenances of Pinus flexilis seedlings across an elevation gradient from forest to alpine. Tree Physiol, 2011, 31(6): 615-625.

[58]

RobertsJA, ElliottKA, Gonzalez-CarranzaZH. Abscission, dehiscence, and other cell separation processes. Annu Rev Plant Biol, 2002, 53: 131-158.

[59]

RuotsalainenAL, MarkkolaAM, KozlovMV. Mycorrhizal colonisation of mountain birch (Betula pubescens ssp. czerepanovii) along three environmental gradients: does life in harsh environments alter plant-fungal relationships?. Environ Monit Assess, 2009, 148(1): 215-232.

[60]

SandnerTM, MatthiesD. Fluctuating asymmetry of leaves is a poor indicator of environmental stress and genetic stress by inbreeding in Silene vulgaris. Ecol Indic, 2017, 79: 247-253.

[61]

SAS Institute (2009) SAS/Stat User’s Guide, Version 9.2. SAS Institute, Cary, NC

[62]

SchoettleAW. The interaction between leaf longevity and shoot growth and foliar biomass per shoot in Pinus contorta at two elevations. Tree Physiol, 1990, 7: 209-214.

[63]

SchubertRBioindikation in Terrestrichen Ökosystemen, 1985, Stuttgart. G Fischer.

[64]

SelyeH. A syndrome produced by diverse nocuous agents. Nature, 1936, 138347932.

[65]

ShibaM, MizunoT, FukudaT. Effect of strong wind on laminas and petioles of Farfugium japonicum (L.) Kitam. Var. japonicum (Asteraceae). Front Plant Sci, 2023, 141182266.

[66]

ShulaevV, CortesD, MillerG, MittlerR. Metabolomics for plant stress response. Physiol Plant, 2008, 132(2): 199-208.

[67]

TaylorJE, WhitelawCA. Signals in abscission. New Phytol, 2001, 151(2): 323-340.

[68]

TreshowMAir pollution and plant life, 1984, Chichester. Wiley.

[69]

WangQW, LiuCG, ZhouWM, QiL, ZhouL, YuDP, DaiLM. Mobile carbon supply in trees and shrubs at the alpine treeline ecotone. Plant Ecol, 2018, 219(4): 467-479.

[70]

WhiteheadFH. Experimental studies of the effect of wind on plant growth and anatomy. New Phytol, 1963, 62(1): 86-90.

[71]

WilseyBJ, HaukiojaE, KorichevaJ, SulkinojaM. Leaf fluctuating asymmetry increases with hybridization and elevation in tree-line birches. Ecology, 1998, 79(6): 2092-2099.

[72]

WulffA, AhonenJ, KärenlampiL. Cell ultrastructural evidence of accelerated ageing of Norway spruce needles in industrial areas. New Phytol, 1996, 133(4): 553-561.

[73]

ZakharovVMKrivolutskyD. Analysis of fluctuating asymmetry as a method of biomonitoring at the population level. Bioindications of chemical and radioactive pollution, 1990, Moscow. Mir Publishers. 187198

[74]

ZakharovVM, TrofimovIE. Fluctuating asymmetry as an indicator of stress. Emerg Top Life Sci, 2022, 6(3): 295-301.

[75]

ZarnochSJ, BechtoldWA, StolteKW. Using crown condition variables as indicators of forest health. Can J for Res, 2004, 34(5): 1057-1070.

[76]

ZhangH, ZhaoY, ZhuJK. Thriving under stress: how plants balance growth and the stress response. Dev Cell, 2020, 55(5): 529-543.

[77]

ZverevV, KozlovMV, ZverevaEL. Changes in crown architecture as a strategy of mountain birch for survival in habitats disturbed by pollution. Sci Total Environ, 2013, 444: 212-223.

[78]

ZverevaEL, RoittoM, KozlovMV. Growth and reproduction of vascular plants in polluted environments: a synthesis of existing knowledge. Environ Rev, 2010, 18: 355-367.

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University of Turku (including Turku University Central Hospital)

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