Integrating morphological, anatomical, and physiological traits to explain elevational distributions in Himalayan steppe and alpine plants

. 2025 Oct ; 67 (10) : 2643-2657. [epub] 20250715

Jazyk angličtina Země China (Republic : 1949- ) Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40662507

Grantová podpora
GACR 24-11954S Grantová agentura České republiky

Understanding plant adaptive strategies that determine species distributions and ecological optima is crucial for predicting responses to global change drivers. While functional traits provide mechanistic insights into distribution patterns, the specific trait syndromes that best predict elevational optima, particularly in less-studied regions such as the Himalayas, remain unclear. This study employs a novel hierarchical framework integrating morphological, anatomical, and physiological traits to explain elevational distributions among 310 plant species across a 3,500-m gradient (2,650-6,150 m). We analyzed 95,000 floristic records collected from 4,062 localities spanning 80,000 km2 in Ladakh, NW Himalayas, India, to define elevational optima and link them with 17 functional traits from over 7,800 individuals. We assessed the roles of moisture and cold limitations on trait-optima relationships by comparing two contrasting habitats (dry steppe and wetter, colder alpine). The predictive power of functional traits was more pronounced in the alpine species facing more extreme abiotic stress than the steppe species. Our results indicate that conservative life history strategies strongly predict elevational optima in alpine areas, while drought avoidance and competitive dominance are key in steppe habitats. Trait syndromes combining short stature, compact growth forms, enhanced storage tissues, and features promoting water-use efficiency (δ13C), freezing resistance (fructan levels), and nutrient retention (high root nitrogen and leaf phosphorus) explained 61% of the variation in alpine species' optima. Conversely, lifespan and clonal propagation determined the optima of steppe species at lower elevations. The study emphasizes the importance of functional trait combinations in determining elevational optima, highlighting that alpine species prioritize resource conservation and stress tolerance, while steppe species focus on competitive growth strategies. This multi-trait approach contrasts with previous research focusing on single trait-elevation relationships, providing novel insights into the diverse mechanisms shaping elevational distributions and offering valuable predictive power for assessing vegetation responses to future climate change.

Zobrazit více v PubMed

Abeynayake, S.W. , Etzerodt, T.P. , Jonavičienė, K. , Byrne, S. , Asp, T. , and Boelt, B. (2015). Fructan metabolism and changes in fructan composition during cold acclimation in perennial ryegrass. Front. Plant Sci. 6: 329. PubMed PMC

Angel, R. , Conrad, R. , Dvorsky, M. , Kopecky, M. , Kotilínek, M. , Hiiesalu, I. , and Doležal, J. (2016). The root‐associated microbial community of the world's highest growing vascular plants. Microb. Ecol. 72: 394–406. PubMed PMC

Arroyo, M.T.K. , Cavieres, L.A. , Peñaloza, A. , and Arroyo‐Kalin, M.A. (2003). Positive associations between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecology, 169(1): 121–129.

Bliss, L.C. (1956). A comparison of plant development in microenvironments of arctic and alpine tundras. Ecol. Monogr. 26: 303–337.

Chlumská, Z. , Liancourt, P. , Hartmann, H. , Bartoš, M. , Altman, J. , Dvorský, M. , and Doležal, J. (2022). Species‐ and compound‐specific dynamics of nonstructural carbohydrates toward the world's upper distribution of vascular plants. Environ. Exp. Bot. 201: 104985.

Chondol, T. , Klimeš, A. , Altman, J. , Čapková, K. , Dvorský, M. , Hiiesalu, I. , and Doležal, J. (2023). Habitat preferences and functional traits drive longevity in Himalayan high‐mountain plants. Oikos 2023: e010073.

Chondol, T. , Korznikov, K.A. , and Doležal, J. (2024). Ecological significance of marcescence in Himalayan plants: Why is standing dead phytomass more important in demanding, resource‐limited environments? Funct. Ecol. 38: 942–954.

Doležal, J. , Chondol, T. , Chlumská, Z. , Altman, J. , Čapková, K. , Dvorský, M. , et al. (2024). Contrasting biomass allocations explain adaptations to cold and drought in the world's highest‐growing angiosperms. Ann. Bot. 134: 401–414. PubMed PMC

Doležal, J. , Dvorský, M. , Börner, A. , Wild, J. , and Schweingruber, F.H. (2018). Anatomy, Ageand Ecology of High Mountain Plants in Ladakh, the Western Himalaya. Springer, Cham.

Dolezal, J. , Dvorsky, M. , Kopecky, M. , Liancourt, P. , Hiiesalu, I. , Macek, M. , and Schweingruber, F. (2016). Vegetation dynamics at the upper elevational limit of vascular plants in Himalaya. Sci. Rep. 6: 24881. PubMed PMC

Dolezal, J. , Klimes, A. , Dvorsky, M. , Riha, P. , Klimesova, J. , and Schweingruber, F. (2019a). Disentangling evolutionary, environmental and morphological drivers of plant anatomical adaptations to drought and cold in Himalayan graminoids. Oikos 128: 1576–1587.

Dolezal, J. , Kopecký, M. , Dvorský, M. , Macek, M. , Rehakova, K. , Capkova, K. , and Altman, J. (2019b). Sink limitation of plant growth determines treeline in the arid Himalayas. Funct. Ecol. 33: 553–565.

Dong, N. , Prentice, I.C. , Harrison, S.P. , Song, Q.H. , and Zhang, Y.P. (2017). Biophysical homoeostasis of leaf temperature: A neglected process for vegetation and land‐surface modelling. Glob. Ecol. Biogeogr. 26: 998–1007.

Dvorský, M. , Altman, J. , Kopecký, M. , Chlumská, Z. , Řeháková, K. , Janatková, K. , and Doležal, J. (2015). Vascular plants at extreme elevations in eastern Ladakh, northwest Himalayas. Plant Ecol. Divers. 8: 571–584.

Dvorský, M. , Doležal, J. , De Bello, F. , Klimešová, J. , and Klimeš, L. (2011). Vegetation types of East Ladakh: Species and growth form composition along main environmental gradients. Appl. Veg. Sci. 14: 132–147.

Dvorský, M. , Macek, M. , Kopecký, M. , Wild, J. , and Doležal, J. (2017). Niche asymmetry of vascular plants increases with elevation. J. Biogeogr. 44: 1418–1425.

Farquhar, G.D. , Hubick, K.T. , Condon, A.G. , and Richards, R.A. (1989). Carbon isotope fractionation and plant water‐use efficiency. Stable Isotopes in Ecological Research. 21–40. 10.1007/978-1-4612-3498-2_2 DOI

Ganthaler, A. , Bär, A. , Dämon, B. , Losso, A. , Nardini, A. , Dullin, C. , et al. (2022). Alpine dwarf shrubs show high proportions of nonfunctional xylem: Visualization and quantification of species‐specific patterns. Plant Cell Environ. 45: 55–68. PubMed

Gardiner, B. , Berry, P. , and Moulia, B. (2016). Wind impacts on plant growth, mechanics and damage. Plant Sci. 245: 94–118. PubMed

Garnier, E. , Navas, M. , and Grigulis, K. (2015). Plant Functional Diversity: Organism Traits, Community Structure, and Ecosystem Properties. Oxford University Press, Oxford.

Gärtner, H. , and Schweingruber, F.H. (2013). Preparation Techniques.

Grime, J.P. (1974). Vegetation classification by reference to strategies. Nature 250: 26–31.

Halbritter, A.H. , Fior, S. , Keller, I. , Billeter, R. , Edwards, P.J. , Holderegger, R. , and Alexander, J.M. (2018). Trait differentiation and adaptation of plants along elevation gradients. J. Evol. Biol. 31: 784–800. PubMed

Henn, J. , Anderson, K. , Brigham, L. , Bueno de Mesquita, C. , Collins, C. , Elmendorf, S. , et al. (2024). Long‐term alpine plant responses to global change drivers depend on functional traits. Ecol. Lett. 27: e14518. PubMed

Hiltbrunner, E. , Arnaiz, J. , and Körner, C. (2021). Biomass allocation and seasonal non‐structural carbohydrate dynamics do not explain the success of tall forbs in short alpine grassland. Oecologia 197: 1063–1077. PubMed PMC

Ho, L.S.T. , Ane, C. , Lachlan, R. , Tarpinian, K. , Feldman, R. , Yu, Q. , and Ho, M.L.S.T. (2016). Package ‘phylolm’ CRAN. Available at: http://cran.rproject.org/web/packages/phylolm/ (Accessed February, 2018).

Huisman, J. , Olff, H. , and Fresco, L.F.M. (1993). A hierarchical set of models for species response analysis. J. Veg. Sci. 4: 37–46.

Hulshof, C.M. , Violle, C. , Spasojevic, M.J. , McGill, B. , Damschen, E. , Harrison, S. , and Enquist, B.J. (2013). Intra‐specific and inter‐specific variation in specific leaf area reveal the importance of abiotic and biotic drivers of species diversity across elevation and latitude. J. Veg. Sci. 24: 921–931.

Jones, H.G. (1992). Plants and Microclimate: A Quantitative Approach to Environmental Plant Physiology. Cambridge University Press, Cambridge.

Kirschbaum, M.U.F. , and Tompkins, D. (1990). Photosynthetic responses to phosphorus nutrition in

Klimešová, J. , Doležal, J. , Dvorský, M. , De Bello, F. , and Klimeš, L. (2011). Clonal growth forms in eastern Ladakh, Western Himalayas: Classification and habitat preferences. Folia Geobot. 46: 191–217.

Körner, C. (2021). Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems. Springer Nature, Cham.

Körner, C. , and Hiltbrunner, E. (2021). Why is the alpine flora comparatively robust against climatic warming? Diversity 13: 383.

Körner, C. , Farquhar, G.D. , and Wong, S.C. (1991). Carbon isotope discrimination by plants follows latitudinal and altitudinal trends. Oecologia 88: 30–40. PubMed

Liancourt, P. , and Doležal, J. (2023). Overgrowth competition or facilitation from cushion plants: Implication for the role of plant–plant interactions. Ecology 104: e3989. PubMed

Liancourt, P. , Le Bagousse‐Pinguet, Y. , Rixen, C. , and Doležal, J. (2017). SGH: Stress or strain gradient hypothesis? Insights from an elevation gradient on the roof of the world. Ann. Bot. 120: 29–38. PubMed PMC

Liancourt, P. , Song, X. , Macek, M. , Santrůček, J. , and Doležal, J. (2020). Plant's‐eye view of temperature governs elevational distributions. Glob. Chang. Biol. 26: 4094–4103. PubMed

Liu, M.Z. , and Osborne, C.P. (2013). Differential freezing resistance and photoprotection in C3 and C4 eudicots and grasses. J. Exp. Bot. 64: 2183–2191. PubMed PMC

Liu, R. , Yang, X. , Gao, R. , Huang, Z. , and Cornelissen, J.H.C. (2022). Coordination of economics spectra in leaf, stem and root within the genus

Livingston, D.P. , Hincha, D.K. , and Heyer, A.G. (2009). Fructan and its relationship to abiotic stress tolerance in plants. Cell. Mol. Life Sci. 66: 2007–2023. PubMed PMC

Macek, M. , Dvorský, M. , Kopecký, M. , Wild, J. , and Doležal, J. (2021). Elevational range size patterns of vascular plants in the Himalaya contradict Rapoport's rule. J. Ecol. 109: 4025–4037.

MacNeill, G.J. , Mehrpouyan, S. , Minow, M.A. , Patterson, J.A. , Tetlow, I.J. , and Emes, M.J. (2017). Starch as a source, starch as a sink: The bifunctional role of starch in carbon allocation. J. Exp. Bot. 68: 4433–4453. PubMed

Madsen‐Hepp, T.R. , Franklin, J. , McFaul, S. , Schauer, L. , and Spasojevic, M.J. (2023). Plant functional traits predict heterogeneous distributional shifts in response to climate change. Funct. Ecol. 37: 1449–1462.

Maharjan, S.K. , Sterck, F.J. , Dhakal, B.P. , Makri, M. , and Poorter, L. (2021). Functional traits shape tree species distribution in the Himalayas. J. Ecol. 109: 3818–3834.

McGill, B. , Enquist, B. , Weiher, E. , and Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends. Ecol. Evol. 21: 178–185. PubMed

Midolo, G. , De Frenne, P. , Hölzel, N. , and Wellstein, C. (2019). Global patterns of intraspecific leaf trait responses to elevation. Glob. Chang. Biol. 25: 2485–2498. PubMed

Morecroft, M.D. , Woodward, F.I. , and Marris, R.H. (1992). Altitudinal trends in leaf nutrient contents, leaf size and δ

Neuner, G. , Buchner, O. , and Braun, V. (2000). Short‐term changes in heat tolerance in the alpine cushion plant

Orme, D. , Freckleton, R. , Thomas, G. , Petzoldt, T. , Fritz, S. , Isaac, N. , and Pearse, W. (2013). The caper package: Comparative analysis of phylogenetics and evolution in R. R package version 0.5.2. 1–36.

Pastorczyk, M. , Giełwanowska, I. , and Lahuta, L.B. (2014). Changes in soluble carbohydrates in polar Caryophyllaceae and Poaceae plants in response to chilling. Acta Physiol. Plant. 36: 1771–1780.

Preston, K.A. , Cornwell, W.K. , and DeNoyer, J.L. (2006). Wood density and vessel traits as distinct correlates of ecological strategy in 51 California coast range angiosperms. New Phytol. 170: 807–818. PubMed

Rai, S. , Breme, N. , Jandová, V. , Lanta, V. , Altman, J. , Ruka, A.T. , Rixen, C. , and Doležal, J. (2024). Growth dynamics and climate sensitivities in alpine cushion plants: Insights from

Ratier‐Backes, A. , Römermann, C. , Alexander, J.M. , Arévalo, J.R. , Keil, P. , Padrón‐Mederos, M.A. , et al. (2023). Mechanisms behind elevational plant species richness patterns revealed by a trait‐based approach. J. Veg. Sci. 34: e13171.

Revell, L.J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3: 217–223.

Robinson, D. (2001). δ PubMed

Rosbakh, S. , and Poschlod, P. (2018). Killing me slowly: Harsh environment extends plant maximum life span. Basic Appl. Ecol. 28: 17–26.

Rosell, J.A. , Olson, M.E. , Anfodillo, T. , and Martínez‐Méndez, N. (2017). Exploring the bark thickness–stem diameter relationship: Clues from lianas, successive cambia, monocots and gymnosperms. New Phytol, 215(2): 569–581. PubMed

Schenk, H.J. , and Jackson, R.B. (2002). Rooting depths, lateral root spreads and below‐ground/above‐ground allometries of plants in water‐limited ecosystems. J. Ecol. 90: 480–494.

Schweingruber, F.H. , Dvorský, M. , Börner, A. , Doležal, J. (2020). Atlas of Stem Anatomy of Arctic and Alpine Plants Around the Globe. Springer, Cham, Switzerland.

Schweingruber, F.H. , Poschlod, P. , and la Neige et le Paysage (Birmensdorf) Institut Fédéral de Recherches sur la Forêt . (2005). Growth rings in herbs and shrubs: life span, age determination and stem anatomy.

Sigdel, S.R. , Liang, E. , Rokaya, M.B. , Rai, S. , Dyola, N. , Sun, J. , Zhang, L. , Zhu, H. , Chettri, N. , Chaudhary, R.P. , et al. (2023). Functional traits of a plant species fingerprint ecosystem productivity along broad elevational gradients in the Himalayas. Funct. Ecol. 37: 383–394.

Sklenář, P. , Kučerová, A. , Macková, J. , and Romoleroux, K. (2016). Temperature microclimates of plants in a tropical alpine environment: How much does growth form matter? Arct. Antarct. Alp. Res. 48: 61–78.

Sperry, J.S. (2003). Evolution of water transport and xylem structure. Int. J. Plant Sci. 164: S115–S127.

Stahl, U. , Reu, B. , and Wirth, C. (2014). Predicting species' range limits from functional traits for the tree flora of North America. Proc. Natl. Acad. Sci. U. S. A. 111: 13739–13744. PubMed PMC

Steinbauer, M.J. , Grytnes, J.‐A. , Jurasinski, G. , Kulonen, A. , Lenoir, J. , Pauli, H. , and Wipf, S. (2018). Accelerated increase in plant species richness on mountain summits is linked to warming. Nature 556: 231–234. PubMed

Tang, L. , Morris, W.K. , Zhang, M. , et al. (2022). Exploring how functional traits modulate species distributions along topographic gradients in Baxian Mountain, North China. Sci. Rep. 12: 994. PubMed PMC

Trifilò, P. , Kiorapostolou, N. , Petruzzellis, F. , Vitti, S. , Petit, G. , Gullo, M.A.L. , and Casolo, V. (2019). Hydraulic recovery from xylem embolism in excised branches of twelve woody species: Relationships with parenchyma cells and non‐structural carbohydrates. Plant Physiol. Biochem. 139: 513–520. PubMed

Venturas, M.D. , Sperry, J.S. , and Hacke, U.G. (2017). Plant xylem hydraulics: What we understand, current research, and future challenges. J. Integr. Plant Biol. 59: 356–389. PubMed

Vijn, I. , and Smeekens, S. (1999). Fructan: More than a reserve carbohydrate? Plant Physiol. 120: 351–360. PubMed PMC

von Arx, G. , Edwards, P.J. , and Dietz, H. (2006). Evidence for life history changes in high‐altitude populations of three perennial forbs. Ecology 87: 665–674. PubMed

Westoby, M. , Falster, D.S. , Moles, A.T. , Vesk, P.A. , and Wright, I.J. (2002). Plant ecological strategies: Some leading dimensions of variation between species. Annu. Rev. Ecol. Syst. 33: 125–159.

Whittaker, R.H. (1967). Gradient analysis of vegetation. Biol. Rev. Camb. Philos. Soc. 42: 207–264. PubMed

Wilson, P.J. , Thompson, K.E.N. , and Hodgson, J.G. (1999). Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytol. 143: 155–162.

Yoshida, M. (2021). Fructan structure and metabolism in overwintering plants. Plants 10: 933. PubMed PMC

Zhang, Y. , Li, C. , and Wang, M. (2019). Linkages of C:N:P stoichiometry between soil and leaf and their response to climatic factors along altitudinal gradients. J. Soils Sediments 19: 1820–1829.

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...