The relict arctic-alpine tundra provides a natural laboratory to study the potential impacts of climate change and anthropogenic disturbance on tundra vegetation. The Nardus stricta-dominated relict tundra grasslands in the Krkonoše Mountains have experienced shifting species dynamics over the past few decades. Changes in species cover of the four competing grasses-Nardus stricta, Calamagrostis villosa, Molinia caerulea, and Deschampsia cespitosa-were successfully detected using orthophotos. Leaf functional traits (anatomy/morphology, element accumulation, leaf pigments, and phenolic compound profiles), were examined in combination with in situ chlorophyll fluorescence in order to shed light on their respective spatial expansions and retreats. Our results suggest a diverse phenolic profile in combination with early leaf expansion and pigment accumulation has aided the expansion of C. villosa, while microhabitats may drive the expansion and decline of D. cespitosa in different areas of the grassland. N. stricta-the dominant species-is retreating, while M. caerulea did not demonstrate significant changes in territory between 2012 and 2018. We propose that the seasonal dynamics of pigment accumulation and canopy formation are important factors when assessing potential "spreader" species and recommend that phenology be taken into account when monitoring grass species using remote sensing.

Biospheric Sciences Laboratory Building 33 NASA Goddard Space Flight Center Greenbelt MD 20771 USA

Department of Applied Geoinformatics and Cartography Faculty of Science Charles University Albertov 6 12800 Prague Czech Republic

Department of Environmental Sciences University of Virginia Charlottesville VA 22904 USA

Department of Experimental Plant Biology Faculty of Science Charles University Viničná 5 12844 Prague Czech Republic

Global Change Research Institute Czech Academy of Sciences Bělidla 4a 60300 Brno Czech Republic

Goddard Earth Science Technology and Research 2 University of Maryland Baltimore County Baltimore MD 21250 USA

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Soukupová L., Krociánová M., Jeník J., Sekzra J. Artic-alpine tundra in the Krkonoše, the Sudetes. Opera Corcon. 1995;32:5–88.

Galvánek D., Janák M. Management of Natura 2000 Habitats. 6230 *Species-Rich Nardus Grasslands; European Commission Natura 2000 Technichal Report. 2008. [(accessed on 11 November 2022)]. Available online: https://ec.europa.eu/environment/nature/natura2000/management/habitats/pdf/6230_Nardus_grasslands.pdf.

Štursa J. Research and management of the giant mountains’arctic-alpine tundra (Czech Republic) [(accessed on 16 January 2023)];AMBIO J. Hum. Environ. 1998 27:358–360. Available online: https://www.semanticscholar.org/paper/RESEARCH-AND-MANAGEMENT-OF-THE-GIANT-TUNDRA-%C5%A0tursa/9bb9e54762754b8f2002c7decbd127fe27755443.

Lokvenc T. Analysis of anthropogenic changes of woody plant stands above the alpine timber line in the Krkonose Mts. Opera Corcon. 1995;32:99–114.

Novák J., Petr L., Treml V. Late-Holocene human-induced changes to the extent of alpine areas in the East Sudetes, Central Europe. Holocene. 2010;20:895–905. doi: 10.1177/0959683610365938. DOI

Brechtel H.M. Impact of Acid Deposition Caused by Air Pollution in Central Europe. In: Teller A., Mathy P., Jeffers J.N.R., editors. Responses of Forest Ecosystems to Environmental Changes. Springer; Dordrecht, The Netherlands: 1992. pp. 594–595.

Rusek J. Air-Pollution-Mediated Changes in Alpine Ecosystems and Ecotones. Ecol. Appl. 1993;3:409–416. doi: 10.2307/1941910. PubMed DOI

Myers-Smith I.H., Forbes B.C., Wilmking M., Hallinger M., Lantz T., Blok D., Tape K.D., Macias-Fauria M., Sass-Klaassen U., Lévesque E., et al. Shrub expansion in tundra ecosystems: Dynamics, impacts and research priorities. Environ. Res. Lett. 2011;6:045509. doi: 10.1088/1748-9326/6/4/045509. DOI

Myers-Smith I.H., Hik D.S. Climate warming as a driver of tundra shrubline advance. J. Ecol. 2018;106:547–560. doi: 10.1111/1365-2745.12817. DOI

Müllerová J. Anthropogenous Vegetation Changes in Alpine Tundra, a Remote Sensing Study from the Krkonoše Mountains, Czech Republic. Preliminary Results; Proceedings of the EUROMAB-Symposium, Austrian Academy of Sciences; Vienna, Austria. 15–19 September 1999; pp. 39–41.

Málková J. Kůlová Impact of dolomitic limestone on changes of species diversity along roads of the eastern Krkonoše Mts. Opera Corcon. 1995;32:11–130.

Husáková J. Subalpine turf communities with Deschampsia cespitosa along the tracks and paths in the Krkonoše (-Giant Mountains) National Park. Preslia. 1986;58:231–246.

Müllerová J., Vítková M. Long-term human impact on Alpine Tundra—25 years of changes assessed by aerial photography. South-East. Eur. J. Earth Obs. Geomat. 2014;3:483–487.

Harčarik J. Management of the dwarf pine plantations on the naturally valuable localities in the Giant Mountains. Opera Corcon. 2007;36:363–369.

Hejcman M., Klaudisová M., Hejcmanová P., Pavlů V., Jones M. Expansion of Calamagrostis villosa in sub-alpine Nardus stricta grassland: Cessation of cutting management or high nitrogen deposition? Agric. Ecosyst. Environ. 2009;129:91–96. doi: 10.1016/j.agee.2008.07.007. DOI

Vacek S., Bastl M., Lepš J. Vegetation changes in forests of the Krkonoše Mts. over a period of air pollution stress (1980–1995) Plant Ecol. 1999;143:1–11. doi: 10.1023/A:1009833313509. DOI

Chambers F.M., Mauquoy D., Todd P.A. Recent rise to dominance of Molinia caerulea in environmentally sensitive areas: New perspectives from palaeoecological data. J. Appl. Ecol. 1999;36:719–733. doi: 10.1046/j.1365-2664.1999.00435.x. DOI

Pyšek P. What do we know about Calamagrostis villosa?—A review of the species behaviour in secondary habitats. Preslia. 1993;64:284–289.

Hejcman M., Pavlu V., Peterova J., Ricarova P. The expansion of Calamagrostis villosa in the Giant Mountains—Preliminary results. [(accessed on 16 November 2022)];Acta Agrar. Et Silvestria Ser. Agrar. 2003 Available online: https://www.infona.pl//resource/bwmeta1.element.agro-article-728d3f02-df5b-4b54-8b6d-25603886a947.

Lokvenc T., Vacek S., Štursa J. Výzkum a Management Ekosystémů na území KRNAP. VÚLHM; Opočno, Czech Republic: 1996. Vývoj zdravotního stavu a plodivosti kleče horské v Krkonoších; pp. 224–228.

Nadarajah K.K. ROS Homeostasis in Abiotic Stress Tolerance in Plants. Int. J. Mol. Sci. 2020;21:5208. doi: 10.3390/ijms21155208. PubMed DOI PMC

Redza-Dutordoir M., Averill-Bates D.A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta. 2016;1863:2977–2992. doi: 10.1016/j.bbamcr.2016.09.012. PubMed DOI

Díaz S., Kattge J., Cornelissen J.H.C., Wright I.J., Lavorel S., Dray S., Reu B., Kleyer M., Wirth C., Colin Prentice I., et al. The global spectrum of plant form and function. Nature. 2016;529:167–171. doi: 10.1038/nature16489. PubMed DOI

Funk J.L., Larson J.E., Ames G.M., Butterfield B.J., Cavender-Bares J., Firn J., Laughlin D.C., Sutton-Grier A.E., Williams L., Wright J. Revisiting the Holy Grail: Using plant functional traits to understand ecological processes. Biol. Rev. Camb. Philos. Soc. 2017;92:1156–1173. doi: 10.1111/brv.12275. PubMed DOI

Palta J.P. Leaf chlorophyll content. Remote Sens. Rev. 1990;5:207–213. doi: 10.1080/02757259009532129. DOI

Demmig-Adams B., Gilmore A.M., Iii W.W.A. In vivo functions of carotenoids in higher plants. FASEB J. 1996;10:403–412. doi: 10.1096/fasebj.10.4.8647339. PubMed DOI

Grace S. Antioxidants and Reactive Oxygen Species in Plants. John Wiley & Sons; Hoboken, NJ, USA: 2008. Phenolics as antioxidants.

Agati G., Tattini M. Multiple functional roles of flavonoids in photoprotection. New Phytol. 2010;186:786–793. doi: 10.1111/j.1469-8137.2010.03269.x. PubMed DOI

Dixon R., Paiva N. Stress-Induced Phenylpropanoid Metabolism. Plant Cell. 1995;7:1085–1097. doi: 10.2307/3870059. PubMed DOI PMC

Gould K.S. Nature’s Swiss Army Knife: The Diverse Protective Roles of Anthocyanins in Leaves. J. Biomed. Biotechnol. 2004;2004:314–320. doi: 10.1155/S1110724304406147. PubMed DOI PMC

Jansen M.A.K., Hectors K., O’Brien N.M., Guisez Y., Potters G. Plant stress and human health: Do human consumers benefit from UV-B acclimated crops? Plant Sci. 2008;175:449–458. doi: 10.1016/j.plantsci.2008.04.010. DOI

Míka V., Kubáň V., Klejdus B., Odstrčilová V., Nerušil P. Phenolic compounds as chemical markers of low taxonomic levels in the family Poaceae. Plant Soil Environ. 2005;51:506. doi: 10.17221/3624-PSE. DOI

Venn S.E., Green K., Pickering C.M., Morgan J.W. Using plant functional traits to explain community composition across a strong environmental filter in Australian alpine snowpatches. Plant Ecol. 2011;212:1491–1499. doi: 10.1007/s11258-011-9923-1. DOI

Kupková L., Červená L., Suchá R., Jakešová L., Zagajewski B., Březina S., Albrechtová J. Classification of Tundra Vegetation in the Krkonoše Mts. National Park Using APEX, AISA Dual and Sentinel-2A Data. Eur. J. Remote Sens. 2017;50:29–46. doi: 10.1080/22797254.2017.1274573. DOI

Müllerová J. Use of digital aerial photography for sub-alpine vegetation mapping: A case study from the Krkonoše Mts., Czech Republic. Plant Ecol. 2005;175:259–272. doi: 10.1007/s11258-005-0063-3. DOI

Gitelson A.A., Merzlyak M.N. Remote estimation of chlorophyll content in higher plant leaves. Int. J. Remote Sens. 1997;18:2691–2697. doi: 10.1080/014311697217558. DOI

Lillesand T.M., Kiefer R.W., Chipman J. Remote Sensing and Image Interpretation. 6th ed. John Wiley & Sons; Hoboken, NJ, USA: 2008.

Hejcman M., Češková M., Pavlů V. Control of Molinia caerulea by cutting management on sub-alpine grassland. Flora-Morphol. Distrib. Funct. Ecol. Plants. 2010;205:577–582. doi: 10.1016/j.flora.2010.04.019. DOI

Björkman O., Demmig B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins | SpringerLink. Planta. 1987;170:489–504. doi: 10.1007/BF00402983. PubMed DOI

Johnson G.N., Young A.J., Scholes J.D., Horton P. The dissipation of excess excitation energy in British plant species. Plant Cell Environ. 1993;16:673–679. doi: 10.1111/j.1365-3040.1993.tb00485.x. DOI

Lawson T., Vialet-Chabrand S. Chlorophyll Fluorescence Imaging. In: Covshoff S., editor. Photosynthesis. Volume 1770. Humana Press; New York, NY, USA: 2018. pp. 121–140. Methods in Molecular Biology. PubMed DOI

Bantis F., Früchtenicht E., Graap J., Ströll S., Reininger N., Schäfer L., Pollastrini M., Holland V., Bussotti F., Radoglou K., et al. Special issue in honour of Prof. Reto J. Strasser—The JIP-test as a tool for forestry in times of climate change. Photosynthetica. 2020;58:409–421. doi: 10.32615/ps.2019.173. DOI

Ceppi M.G., Oukarroum A., Çiçek N., Strasser R.J., Schansker G. The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: A study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol. Plant. 2012;144:277–288. doi: 10.1111/j.1399-3054.2011.01549.x. PubMed DOI

Çiçek N., Oukarroum A., Strasser R., Schansker G. Salt stress effects on the photosynthetic electron transport chain in two chickpea lines differing in their salt stress tolerance. Photosynth. Res. 2018;136:291–301. doi: 10.1007/s11120-017-0463-y. PubMed DOI

Oukarroum A., Schansker G., Strasser R. Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiol. Plant. 2009;137:188–199. doi: 10.1111/j.1399-3054.2009.01273.x. PubMed DOI

Çiçek N., Kalaji H.M., Ekmekçi Y. Probing the photosynthetic efficiency of some European and Anatolian Scots pine populations under UV-B radiation using polyphasic chlorophyll a fluorescence transient. Photosynthetica. 2020;58:468–478. doi: 10.32615/ps.2019.151. DOI

Armstrong R.H., Common T.G., Davies G.J. The prediction of the in vivodigestibility of the diet of sheep and cattle grazing indigenous hill plant communities by in vitrodigestion, faecal nitrogen concentration or indigestible’ acid-detergent fibre—ARMSTRONG—1989—Grass and Forage Science—Wiley Online Library. Grass Forage Sci. 1989;44:303–313.

Leuschner C., Ellenberg H. Ecology of Central European Non-Forest Vegetation: Coastal to Alpine, Natural to Man-Made Habitats: Vegetation Ecology of Central Europe, Volume II. Volume 2. Springer; Berlin/Heidelberg, Germany: 2017.

Ceulemans T., Merckx R., Hens M., Honnay O. Plant species loss from European semi-natural grasslands following nutrient enrichment—Is it nitrogen or is it phosphorus? Glob. Ecol. Biogeogr. 2013;22:73–82. doi: 10.1111/j.1466-8238.2012.00771.x. DOI

CHAPIN F.S. Effects of Plant Traits on Ecosystem and Regional Processes: A Conceptual Framework for Predicting the Consequences of Global Change. Ann. Bot. 2003;91:455–463. doi: 10.1093/aob/mcg041. PubMed DOI PMC

Jin Y., Lai S., Chen Z., Jian C., Zhou J., Niu F., Xu B. Leaf Photosynthetic and Functional Traits of Grassland Dominant Species in Response to Nutrient Addition on the Chinese Loess Plateau. Plants. 2022;11:2921. doi: 10.3390/plants11212921. PubMed DOI PMC

Zorić N. Master’s Thesis. Norwegian University of Life Sciences; Ås, Norway: 2013. [(accessed on 10 November 2022)]. Level and distribution of genetic diversity in the European species Nardus stricta L. (Poaceae) inferred from chloroplast DNA and nuclear amplified fragment length polymorphism markers. Available online: https://nmbu.brage.unit.no/nmbu-xmlui/handle/11250/189603.

Ehleringer J.R., Comstock J. Leaf absorptance and leaf angle: Mechanisms for stress avoidance. In: Tenhunen J.D., Catarino F.M., Lange O.L., Oechel W.C., editors. Plant Response to Stress. Springer; Berlin/Heidelberg, Germany: 1987. pp. 55–76.

Lloyd K.M., Pollock M.L., Mason N.W.H., Lee W.G. Leaf trait-palatability relationships differ between ungulate species: Evidence from cafeteria experiments using naïve tussock grasses. N. Z. J. Ecol. 2010;34:219–226.

Smith W.K., Vogelmann T.C., DeLucia E.H., Bell D.T., Shepherd K.A. Leaf Form and Photosynthesis. BioScience. 1997;47:785–793. doi: 10.2307/1313100. DOI

Hunt L., Klem K., Lhotáková Z., Vosolsobě S., Oravec M., Urban O., Špunda V., Albrechtová J. Light and CO2 Modulate the Accumulation and Localization of Phenolic Compounds in Barley Leaves. Antioxidants. 2021;10:385. doi: 10.3390/antiox10030385. PubMed DOI PMC

Agati G., Azzarello E., Pollastri S., Tattini M. Flavonoids as antioxidants in plants: Location and functional significance. Plant Sci. Int. J. Exp. Plant Biol. 2012;196:67–76. doi: 10.1016/j.plantsci.2012.07.014. PubMed DOI

Ryan K.G., Swinny E.E., Markham K.R., Winefield C. Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves. Phytochemistry. 2002;59:23–32. doi: 10.1016/S0031-9422(01)00404-6. PubMed DOI

Agati G., Stefano G., Biricolti S., Tattini M. Mesophyll distribution of ‘antioxidant’ flavonoid glycosides in Ligustrum vulgare leaves under contrasting sunlight irradiance. Ann. Bot. 2009;104:853–861. doi: 10.1093/aob/mcp177. PubMed DOI PMC

Klimeš L., Klimešová J. The effects of mowing and fertilization on carbohydrate reserves and regrowth of grasses: Do they promote plant coexistence in species-rich meadows? Evol. Ecol. 2002;15:363–382. doi: 10.1023/A:1016041100087. DOI

Clayton W.D., Vorontsova M.S., Harman K.T., Williamson H. GrassBase—The Online World Grass Flora. 2006. [(accessed on 24 October 2022)]. Available online: http://www.kew.org/data/grasses-db.html.

Grant S.A., Torvell L., Sim E.M., Small J.L., Armstrong R.H. Controlled Grazing Studies on Nardus Grassland: Effects of Between-Tussock Sward Height and Species of Grazer on Nardus utilization and Floristic Composition in Two Fields in Scotland. J. Appl. Ecol. 1996;33:1053–1064. doi: 10.2307/2404685. DOI

Jones L.I. Studies on Hill Land in Wales. Welsh Plant Breeding Station; Aberystwyth, UK: 1967.

Krahulec F., Skálová H., Herben T., Hadincová V., Wildová R., Pecháčková S. Vegetation changes following sheep grazing in abandoned mountain meadows. Appl. Veg. Sci. 2001;4:97–102. doi: 10.1111/j.1654-109X.2001.tb00239.x. DOI

Mašková Z., Doležal J., Květ J., Zemek F. Long-term functioning of a species-rich mountain meadow under different management regimes. Agric. Ecosyst. Environ. 2009;132:192–202. doi: 10.1016/j.agee.2009.04.002. DOI

Ma Y.-Z., Holt N.E., Li X.-P., Niyogi K.K., Fleming G.R. Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc. Natl. Acad. Sci. USA. 2003;100:4377–4382. doi: 10.1073/pnas.0736959100. PubMed DOI PMC

Barrere J., Collet C., Saïd S., Bastianelli D., Verheyden H., Courtines H., Bonnet A., Segrestin J., Boulanger V. Do trait responses to simulated browsing in Quercus robur saplings affect their attractiveness to Capreolus capreolus the following year? Environ. Exp. Bot. 2022;194:104743. doi: 10.1016/j.envexpbot.2021.104743. DOI

Cornelissen J.H.C., Quested H.M., Gwynn-Jones D., Van Logtestijn R.S.P., De Beus M.A.H., Kondratchuk A., Callaghan T.V., Aerts R. Leaf digestibility and litter decomposability are related in a wide range of subarctic plant species and types. Funct. Ecol. 2004;18:779–786. doi: 10.1111/j.0269-8463.2004.00900.x. DOI

Lee D.W., Lowry J.B., Stone B.C. Abaxial Anthocyanin Layer in Leaves of Tropical Rain Forest Plants: Enhancer of Light Capture in Deep Shade. Biotropica. 1979;11:70–77. doi: 10.2307/2388175. DOI

Hughes N.M., Vogelmann T.C., Smith W.K. Optical effects of abaxial anthocyanin on absorption of red wavelengths by understorey species: Revisiting the back-scatter hypothesis. J. Exp. Bot. 2008;59:3435–3442. doi: 10.1093/jxb/ern193. PubMed DOI PMC

Steyn W.J., Wand S.J.E., Holcroft D.M., Jacobs G. Anthocyanins in vegetative tissues: A proposed unified function in photoprotection. New Phytol. 2002;155:349–361. doi: 10.1046/j.1469-8137.2002.00482.x. PubMed DOI

Sun J., Nishio J.N., Vogelmann T.C. High-light effects on CO2 fixation gradients across leaves. Plant Cell Environ. 1996;19:1261–1271. doi: 10.1111/j.1365-3040.1996.tb00004.x. DOI

Kovinich N., Kayanja G., Chanoca A., Otegui M.S., Grotewold E. Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signal. Behav. 2015;10:e1027850. doi: 10.1080/15592324.2015.1027850. PubMed DOI PMC

Cobbina J., Miller M.H. Purpling in Maize Hybrids as Influenced by Temperature and Soil Phosphorus. Agron. J. 1987;79:576–582. doi: 10.2134/agronj1987.00021962007900030035x. DOI

Chalker-Scott L. Do Anthocyanins Function of Osmoregulators in Leaf Tissues? Adv. Bot. Res. 2002;37:103–127.

Veresoglou D.S., Fitter A.H. Spatial and Temporal Patterns of Growth and Nutrient Uptake of Five Co-Existing Grasses. J. Ecol. 1984;72:259. doi: 10.2307/2260018. DOI

Olszowy M. What is responsible for antioxidant properties of polyphenolic compounds from plants? Plant Physiol. Biochem. 2019;144:135–143. doi: 10.1016/j.plaphy.2019.09.039. PubMed DOI

Hunt L., Fuksa M., Klem K., Lhotáková Z., Oravec M., Urban O., Albrechtová J. Barley Genotypes Vary in Stomatal Responsiveness to Light and CO2 Conditions. Plants. 2021;10:2533. doi: 10.3390/plants10112533. PubMed DOI PMC

Lin C.-M., Chen C.-T., Lee H.-H., Lin J.-K. Prevention of Cellular ROS Damage by Isovitexin and Related Flavonoids. Planta Med. 2002;68:365–367. doi: 10.1055/s-2002-26753. PubMed DOI

Ibaraki Y., Murakami J. Distribution of chlorophyll fluorescence parameter fv/fm within individual plants under various stress conditions. Acta Hortic. 2007;761:255–260. doi: 10.17660/ActaHortic.2007.761.33. DOI

Baker N.R. Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo. Annu. Rev. Plant Biol. 2008;59:89–113. doi: 10.1146/annurev.arplant.59.032607.092759. PubMed DOI

Sharma D.K., Andersen S.B., Ottosen C.-O., Rosenqvist E. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol. Plant. 2015;153:284–298. doi: 10.1111/ppl.12245. PubMed DOI

Rizza F., Pagani D., Stanca A.M., Cattivelli L. Use of chlorophyll fluorescence to evaluate the cold acclimation and freezing tolerance of winter and spring oats. Plant Breed. 2001;120:389–396. doi: 10.1046/j.1439-0523.2001.00635.x. DOI

Dias M.C., Correia S., Serôdio J., Silva A.M.S., Freitas H., Santos C. Chlorophyll fluorescence and oxidative stress endpoints to discriminate olive cultivars tolerance to drought and heat episodes. Sci. Hortic. 2018;231:31–35. doi: 10.1016/j.scienta.2017.12.007. DOI

Schansker G., Tóth S.Z., Strasser R.J. Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim. Biophys. Acta BBA-Bioenerg. 2005;1706:250–261. doi: 10.1016/j.bbabio.2004.11.006. PubMed DOI

Kalaji H.M., Oukarroum A., Alexandrov V., Kouzmanova M., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Allakhverdiev S.I., Goltsev V. Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol. Biochem. 2014;81:16–25. doi: 10.1016/j.plaphy.2014.03.029. PubMed DOI

Semelová V., Hejcman M., Pavlů V., Vacek S., Podrázský V. The Grass Garden in the Giant Mts. (Czech Republic): Residual effect of long-term fertilization after 62 years. Agric. Ecosyst. Environ. 2008;123:337–342. doi: 10.1016/j.agee.2007.07.005. DOI

Chadwick M.J. Nardus stricta L. J. Ecol. 1960;48:255–267. doi: 10.2307/2257324. DOI

Peñuelas J., Fernández-Martínez M., Ciais P., Jou D., Piao S., Obersteiner M., Vicca S., Janssens I.A., Sardans J. The bioelements, the elementome, and the biogeochemical niche. Ecology. 2019;100:e02652. doi: 10.1002/ecy.2652. PubMed DOI

Ahmad-Ramli M.F., Cornulier T., Johnson D. Partitioning of soil phosphorus regulates competition between Vaccinium vitis-idaea and Deschampsia cespitosa. Ecol. Evol. 2013;3:4243–4252. doi: 10.1002/ece3.771. PubMed DOI PMC

Alonso I., Hartley S.E., Thurlow M. Competition between heather and grasses on Scottish moorlands: Interacting effects of nutrient enrichment and grazing regime. J. Veg. Sci. 2001;12:249–260. doi: 10.2307/3236609. DOI

Schelfhout S., Wasof S., Mertens J., Vanhellemont M., Demey A., Haegeman A., DeCock E., Moeneclaey I., Vangansbeke P., Viaene N., et al. Effects of bioavailable phosphorus and soil biota on typical Nardus grassland species in competition with fast-growing plant species. Ecol. Indic. 2021;120:106880. doi: 10.1016/j.ecolind.2020.106880. DOI

Lepš J.J.P., Grime J.G. Hodgson and R. Hunt Comparative plant ecology. Folia Geobot. Phytotaxon. 1990;25:216. doi: 10.1007/BF02912743. DOI

Sochorová L., Jansa J., Verbruggen E., Hejcman M., Schellberg J., Kiers E.T., Johnson N.C. Long-term agricultural management maximizing hay production can significantly reduce belowground C storage. Agric. Ecosyst. Environ. 2016;220:104–114. doi: 10.1016/j.agee.2015.12.026. DOI

Clein J.S., Schimel J.P. Nitrogen turnover and availability during succession from alder to poplar in Alaskan taiga forests. Soil Biol. Biochem. 1995;27:743–752. doi: 10.1016/0038-0717(94)00232-P. DOI

Meier C.L., Bowman W.D. Phenolic-rich leaf carbon fractions differentially influence microbial respiration and plant growth. Oecologia. 2008;158:95–107. doi: 10.1007/s00442-008-1124-9. PubMed DOI

Beamish A., Raynolds M.K., Epstein H., Frost G.V., Macander M.J., Bergstedt H., Bartsch A., Kruse S., Miles V., Tanis C.M., et al. Recent trends and remaining challenges for optical remote sensing of Arctic tundra vegetation: A review and outlook. Remote Sens. Environ. 2020;246:111872. doi: 10.1016/j.rse.2020.111872. DOI

Heijmans M.M.P.D., Magnússon R., Lara M.J., Frost G.V., Myers-Smith I.H., van Huissteden J., Jorgenson M.T., Fedorov A.N., Epstein H.E., Lawrence D.M., et al. Tundra vegetation change and impacts on permafrost. Nat. Rev. Earth Environ. 2022;3:68–84. doi: 10.1038/s43017-021-00233-0. DOI

Franke A.K., Feilhauer H., Bräuning A., Rautio P., Braun M. Remotely sensed estimation of vegetation shifts in the polar and alpine tree-line ecotone in Finnish Lapland during the last three decades. For. Ecol. Manag. 2019;454:117668. doi: 10.1016/j.foreco.2019.117668. DOI

Meng B., Ge J., Liang T., Yang S., Gao J., Feng Q., Cui X., Huang X., Xie H. Evaluation of Remote Sensing Inversion Error for the Above-Ground Biomass of Alpine Meadow Grassland Based on Multi-Source Satellite Data. Remote Sens. 2017;9:372. doi: 10.3390/rs9040372. DOI

Červená L., Pinlová G., Lhotáková Z., Neuwirthová E., Kupková L., Potůčková M., Lysák J., Campbell P., Albrechtová J. Determination of Chlorophyll Content in Selected Grass Communities of Krkonoše Mts. Tundra Based on Laboratory Spectroscopy and Aerial Hyperspectral data; Proceedings of the International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences, Volume XLIII-B3-2022 XXIV ISPRS Congress (2022 edition); Nice, France. 6–11 June 2022; pp. 381–388.

Chen J.M., Black T.A. Defining leaf area index for non-flat leaves. Plant Cell Environ. 1992;15:421–429. doi: 10.1111/j.1365-3040.1992.tb00992.x. DOI

Ustin S.L., Gitelson A.A., Jacquemoud S., Schaepman M., Asner G.P., Gamon J.A., Zarco-Tejada P. Retrieval of foliar information about plant pigment systems from high resolution spectroscopy. Remote Sens. Environ. 2009;113:S67–S77. doi: 10.1016/j.rse.2008.10.019. DOI

Gitelson A.A., Chivkunova O.B., Merzlyak M.N. Nondestructive estimation of anthocyanins and chlorophylls in anthocyanic leaves. Am. J. Bot. 2009;96:1861–1868. doi: 10.3732/ajb.0800395. PubMed DOI

Chlus A., Townsend P.A. Characterizing seasonal variation in foliar biochemistry with airborne imaging spectroscopy. Remote Sens. Environ. 2022;275:113023. doi: 10.1016/j.rse.2022.113023. DOI

Bussotti F., Gerosa G., Digrado A., Pollastrini M. Selection of chlorophyll fluorescence parameters as indicators of photosynthetic efficiency in large scale plant ecological studies. Ecol. Indic. 2020;108:105686. doi: 10.1016/j.ecolind.2019.105686. DOI

Mancinelli A.L., Yang C.-P.H., Lindquist P., Anderson O.R., Rabino I. Photocontrol of Anthocyanin Synthesis: III. The Action of Streptomycin on the Synthesis of Chlorophyll and Anthocyanin 1. Plant Physiol. 1975;55:251–257. doi: 10.1104/pp.55.2.251. PubMed DOI PMC

Merzlyak M.N., Chivkunova O.B., Solovchenko A.E., Naqvi K.R. Light absorption by anthocyanins in juvenile, stressed, and senescing leaves. J. Exp. Bot. 2008;59:3903–3911. doi: 10.1093/jxb/ern230. PubMed DOI PMC

Fossen T., Slimestad R., Øvstedal D.O., Andersen Ø.M. Anthocyanins of grasses. Biochem. Syst. Ecol. 2002;30:855. doi: 10.1016/S0305-1978(02)00028-5. DOI

Singleton V.L., Rossi J.A. Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents. Am. J. Enol. Vitic. 1965;16:144–158.

Porra R., Thompson W., Kriedemann P. Determination of Accurate Extinction Coefficients and Simultaneous-Equations for Assaying Chlorophyll-a and Chlorophyll-B Extracted with 4 Different Solvents—Verification of the Concentration. Biochim. Biophys. Acta. 1989;975:384–394. doi: 10.1016/S0005-2728(89)80347-0. DOI

Wellburn A.R. The Spectral Determination of Chlorophylls a and b, as well as Total Carotenoids, Using Various Solvents with Spectrophotometers of Different Resolution. J. Plant Physiol. 1994;144:307–313. doi: 10.1016/S0176-1617(11)81192-2. DOI

Brauns F.E. The Chemistry of Lignin. Academic Press Inc.; New York, NY, USA: 1952.

Gardner R.O. Vanillin-Hydrochloric Acid as a Histochemical Test for Tannin. Stain Technol. 1975;50:315–317. doi: 10.3109/10520297509117081. PubMed DOI

Hutzler P., Fischbach R., Heller W., Jungblut T.P., Reuber S., Schmitz R., Veit M., Weissenböck G., Schnitzler J.-P. Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J. Exp. Bot. 1998;49:953–965. doi: 10.1093/jxb/49.323.953. DOI

Tattini M., Guidi L., Morassi-Bonzi L., Pinelli P., Remorini D., Degl’Innocenti E., Giordano C., Massai R., Agati G. On the role of flavonoids in the integrated mechanisms of response of Ligustrum vulgare and Phillyrea latifolia to high solar radiation. New Phytol. 2005;167:457–470. doi: 10.1111/j.1469-8137.2005.01442.x. PubMed DOI

Tang Y., Horikoshi M., Li W. ggfortify: Unified Interface to Visualize Statistical Results of Popular R Packages. R J. 2016;8:474–485. doi: 10.32614/RJ-2016-060. DOI

R Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2021. [(accessed on 11 November 2022)]. Available online: https://www.R-project.org/

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