in

Alpine shrub growth follows bimodal seasonal patterns across biomes – unexpected environmental controls

  • IPCC. Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change (2021).

  • Giorgi, F. & Lionello, P. Climate change projections for the Mediterranean region. Glob. Planet. Change 63, 90–104 (2008).

    Article 

    Google Scholar 

  • Post, E. et al. The polar regions in a 2 °C warmer world. Sci. Adv. 5, eaaw9883 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Körner, C. Alpine Plant Life (Springer International Publishing, 2021).

  • Graven, H. D. et al. Enhanced seasonal exchange of CO2 by northern ecosystems since 1960. Science 341, 1085–1089 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Myers-Smith, I. H. et al. Complexity revealed in the greening of the Arctic. Nat. Clim. Change 10, 106–117 (2020).

    Article 

    Google Scholar 

  • Gamm, C. M. et al. Declining growth of deciduous shrubs in the warming climate of continental western Greenland. J. Ecol. 106, 640–654 (2018).

    CAS 
    Article 

    Google Scholar 

  • AMAP. Arctic Climate Change Update 2021: Key Trends and Impacts. Arctic Monitoring and Assessment Programme (2021).

  • Elmendorf, S. C. et al. Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nat. Clim. Change 2, 453–457 (2012).

    Article 

    Google Scholar 

  • Bjorkman, A. D. et al. Plant functional trait change across a warming tundra biome. Nature 562, 57–62 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Zhang, W. et al. Self‐amplifying feedbacks accelerate greening and warming of the arctic. Geophys. Res. Lett. 45, 7102–7111 (2018).

    Article 

    Google Scholar 

  • Körner, C. Treelines will be understood once the functional difference between a tree and a shrub is. Ambio 41, 197–206 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Pellizzari, E. et al. Diverging shrub and tree growth from the Polar to the Mediterranean biomes across the European continent. Glob. Change Biol. 23, 3169–3180 (2017).

    Article 

    Google Scholar 

  • Dobbert, S., Pape, R. & Löffler, J. How does spatial heterogeneity affect inter‐ and intraspecific growth patterns in tundra shrubs. J. Ecol. 7, 1 (2021).

    Google Scholar 

  • Ackerman, D., Griffin, D., Hobbie, S. E. & Finlay, J. C. Arctic shrub growth trajectories differ across soil moisture levels. Glob. Change Biol. 23, 4294–4302 (2017).

    Article 

    Google Scholar 

  • Stendel, M., Christensen, J. H. & Petersen, D. in High-Arctic Ecosystem Dynamics in a Changing Climate (eds. Meltofte, H.) 13–43 (Elsevier, 2008).

  • Prislan, P. et al. Annual cambial rhythm in Pinus halepensis and Pinus sylvestris as indicator for climate adaptation. Front. Plant Sci. 7, 1923 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Gazol, A. & Camarero, J. J. Mediterranean dwarf shrubs and coexisting trees present different radial-growth synchronies and responses to climate. Plant Ecol. 213, 1687–1698 (2012).

    Article 

    Google Scholar 

  • Olano, J. M., Almería, I., Eugenio, M. & Arx, G. V. Under pressure: how a Mediterranean high-mountain forb coordinates growth and hydraulic xylem anatomy in response to temperature and water constraints. Funct. Ecol. 27, 1295–1303 (2013).

    Article 

    Google Scholar 

  • Voltas, J. et al. A retrospective, dual-isotope approach reveals individual predispositions to winter-drought induced tree dieback in the southernmost distribution limit of Scots pine. Plant, Cell Environ. 36, 1435–1448 (2013).

    CAS 
    Article 

    Google Scholar 

  • Hanewinkel, M., Cullmann, D. A., Schelhaas, M.-J., Nabuurs, G.-J. & Zimmermann, N. E. Climate change may cause severe loss in the economic value of European forest land. Nat. Clim. Change 3, 203–207 (2013).

    Article 

    Google Scholar 

  • Castagneri, D., Battipaglia, G., Arx, G. V., Pacheco, A. & Carrer, M. Tree-ring anatomy and carbon isotope ratio show both direct and legacy effects of climate on bimodal xylem formation in Pinus pinea. Tree Physiol. 38, 1098–1109 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cabon, A., Peters, R. L., Fonti, P., Martínez-Vilalta, J. & Cáceres, M. Temperature and water potential co-limit stem cambial activity along a steep elevational gradient. N. Phytologist 226, 1325–1340 (2020).

    CAS 
    Article 

    Google Scholar 

  • Camarero, J. J., Valeriano, C., Gazol, A., Colangelo, M. & Sánchez-Salguero, R. Climate differently impacts the growth of coexisting trees and shrubs under semi-arid mediterranean conditions. Forests 12, 381 (2021).

    Article 

    Google Scholar 

  • García-Cervigón Morales, A. I., Olano Mendoza, J. M., Eugenio Gozalbo, M. & Camarero Martínez, J. J. Arboreal and prostrate conifers coexisting in Mediterranean high mountains differ in their climatic responses. Dendrochronologia 30, 279–286 (2012).

    Article 

    Google Scholar 

  • Oladi, R., Emaminasab, M. & Eckstein, D. The dendroecological potential of shrubs in north Iranian semi-deserts. Dendrochronologia 44, 94–102 (2017).

    Article 

    Google Scholar 

  • McMahon, S. M. & Parker, G. G. A general model of intra-annual tree growth using dendrometer bands. Ecol. Evolution 5, 243–254 (2015).

    Article 

    Google Scholar 

  • Drew, D. M., Downes, G. M. & Battaglia, M. CAMBIUM, a process-based model of daily xylem development in Eucalyptus. J. Theor. Biol. 264, 395–406 (2010).

    PubMed 
    Article 

    Google Scholar 

  • Delpierre, N., Berveiller, D., Granda, E. & Dufrêne, E. Wood phenology, not carbon input, controls the interannual variability of wood growth in a temperate oak forest. N. Phytologist 210, 459–470 (2016).

    CAS 
    Article 

    Google Scholar 

  • Rathgeber, C. B. K., Cuny, H. E. & Fonti, P. Biological basis of tree-ring formation: a crash course. Front. Plant Sci. 7, 734 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Körner, C. Carbon limitation in trees. J. Ecol. 91, 4–17 (2003).

    Article 

    Google Scholar 

  • Thompson, J. D. Plant Evolution in the Mediterranean (Oxford University Press, 2005).

  • Rossi, S. et al. Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere. Glob. Change Biol. 22, 3804–3813 (2016).

    Article 

    Google Scholar 

  • Löffler, J. & Pape, R. Thermal niche predictors of alpine plant species. Ecology 101, e02891 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Zweifel, R. et al. Why trees grow at night. N. Phytologist 231, 2174–2185 (2021).

    Article 

    Google Scholar 

  • González-Rodríguez, Á. M. et al. Seasonal cycles of sap flow and stem radius variation of Spartocytisus supranubius in the alpine zone of Tenerife, Canary Islands. Alp. Bot. 127, 97–108 (2017).

    Article 

    Google Scholar 

  • Zweifel, R., Haeni, M., Buchmann, N. & Eugster, W. Are trees able to grow in periods of stem shrinkage. N. Phytologist 211, 839–849 (2016).

    Article 

    Google Scholar 

  • Rossi, S., Deslauriers, A., Anfodillo, T. & Carraro, V. Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152, 1–12 (2007).

    PubMed 
    Article 

    Google Scholar 

  • Myers-Smith, I. H. et al. Climate sensitivity of shrub growth across the tundra biome. Nat. Clim. Change 5, 887–891 (2015).

    Article 

    Google Scholar 

  • Mitrakos, K. A Theory for Mediterranean Plant Life (Acta oecologica, 1980).

  • Camarero, J. J., Olano, J. M. & Parras, A. Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. N. Phytologist 185, 471–480 (2010).

    Article 

    Google Scholar 

  • Alday, J. G., Camarero, J. J., Revilla, J. & Resco de Dios, V. Similar diurnal, seasonal and annual rhythms in radial root expansion across two coexisting Mediterranean oak species. Tree Physiol. 40, 956–968 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Lockhart, J. A. An analysis of irreversible plant cell elongation. J. Theor. Biol. 8, 264–275 (1965).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Descals, A. et al. Soil thawing regulates the spring growth onset in tundra and alpine biomes. Sci. total Environ. 742, 140637 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Morgner, E., Elberling, B., Strebel, D. & Cooper, E. J. The importance of winter in annual ecosystem respiration in the High Arctic: effects of snow depth in two vegetation types. Polar Res. 29, 58–74 (2010).

    CAS 
    Article 

    Google Scholar 

  • Weijers, S., Beckers, N. & Löffler, J. Recent spring warming limits near-treeline deciduous and evergreen alpine dwarf shrub growth. Ecosphere 9, e02328 (2018).

    Article 

    Google Scholar 

  • Bret-Harte, M. S. et al. Developmental plasticity allows Betula nana to dominate tundra subjected to an altered environment. Ecology 82, 18–32 (2001).

    Article 

    Google Scholar 

  • Wang, Y. et al. Warming‐induced shrubline advance stalled by moisture limitation on the Tibetan Plateau. Ecography 44, 1631–1641 (2021).

    Article 

    Google Scholar 

  • Tape, K. D., Hallinger, M., Welker, J. M. & Ruess, R. W. Landscape heterogeneity of shrub expansion in Arctic Alaska. Ecosystems 15, 711–724 (2012).

    CAS 
    Article 

    Google Scholar 

  • Francon, L., Corona, C., Till-Bottraud, I., Carlson, B. Z. & Stoffel, M. Some (do not) like it hot: shrub growth is hampered by heat and drought at the alpine treeline in recent decades. Am. J. Bot. 107, 607–617 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Lu, X., Liang, E., Babst, F., Camarero, J. J. & Büntgen, U. Warming-induced tipping points of Arctic and alpine shrub recruitment. Proc. Natl Acad. Sci. USA 119, e2118120119 (2022).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sabater, A. M. et al. Transpiration from subarctic deciduous woodlands: environmental controls and contribution to ecosystem evapotranspiration. Ecohydrology 13, e2190 (2019).

    Google Scholar 

  • Larson, P. R. The indirect effect of photoperiod on tracheid diameter in Pinus resinosa. Am. J. Bot. 49, 132–137 (1962).

    Article 

    Google Scholar 

  • Jackson, S. D. Plant responses to photoperiod. N. Phytologist 181, 517–531 (2009).

    CAS 
    Article 

    Google Scholar 

  • Waisel, Y. & Fahn, A. The effects of environment on wood formation and cambial activity in Robina Pseudacacia L. N. Phytologist 64, 436 (1965).

    Article 

    Google Scholar 

  • Pasho, E., Camarero, J. J. & Vicente-Serrano, S. M. Climatic impacts and drought control of radial growth and seasonal wood formation in Pinus halepensis. Trees 26, 1875–1886 (2012).

    Article 

    Google Scholar 

  • Gričar, J. et al. Plasticity in variation of xylem and phloem cell characteristics of Norway spruce under different local conditions. Front. Plant Sci. 6, 730 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Zellweger, F. et al. Forest microclimate dynamics drive plant responses to warming. Science 368, 772–775 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Oberhuber, W., Sehrt, M. & Kitz, F. Hygroscopic properties of thin dead outer bark layers strongly influence stem diameter variations on short and long time scales in Scots pine (Pinus sylvestris L.). Agric. For. Meteorol. 290, 108026 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sonntag, D. Important new values of the physical constants of 1986, vapour pressure formulations based on ITS-90, and psychrometer formulae. Z. f.ür. Meteorologie 70, 340–344 (1990).

    Google Scholar 

  • Löffler, J., Dobbert, S., Pape, R. & Wundram, D. Dendrometer measurements of arctic-alpine dwarf shrubs and micro-environmental drivers of plant growth—Dataset from long-term alpine ecosystem research in central Norway. Erdkunde 75, DP311201 (2021).

    Google Scholar 

  • Löffler, J., Albrecht, E. C., Dobbert, S., Pape, R. & Wundram, D. Dendrometer measurements of Mediterranean-alpine dwarf shrubs and micro-environmental drivers of plant growth—Dataset from long-term alpine ecosystem research in the Sierra Nevada, Spain (LTAER-ES). Erdkunde 76, DP311202 (2022).

    Article 

    Google Scholar 

  • R Core Team. A Language and Environment for Statistical Computing. https://www.R-project.org/ (2020).

  • Wood, S. N. Generalized Additive Models. An introduction with R (2nd edition) (Chapman & Hall/CRC, 2017).

  • Wood, S. N. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J. R. Stat. Soc.: Ser. B 73, 3–36 (2011).

    Article 

    Google Scholar 

  • Byun, J. G. et al. Radial growth response of Pinus densiflora and Quercus spp. to topographic and climatic factors in South Korea. J. Plant Ecol. 6, 380–392 (2013).

    Article 

    Google Scholar 

  • Yee, T. W. & Mitchell, N. D. Generalized additive models in plant ecology. J. Vegetation Sci. 2, 587–602 (1991).

    Article 

    Google Scholar 

  • Gasparrini, A., Scheipl, F., Armstrong, B. & Kenward, M. G. A penalized framework for distributed lag non-linear models. Biometrics 73, 938–948 (2017).

    PubMed 
    Article 

    Google Scholar 

  • Scott, E. R., Uriarte, M. & Bruna, E. M. Delayed effects of climate on vital rates lead to demographic divergence in Amazonian forest fragments. https://doi.org/10.1101/2021.06.28.450186 (2021).

  • Almon, S. The distributed lag between capital appropriations and expenditures. Econometrica 33, 178 (1965).

    Article 

    Google Scholar 

  • Vanoni, M., Bugmann, H., Nötzli, M. & Bigler, C. Drought and frost contribute to abrupt growth decreases before tree mortality in nine temperate tree species. For. Ecol. Manag. 382, 51–63 (2016).

    Article 

    Google Scholar 

  • Pukienė, R., Vitas, A., Kažys, J. & Rimkus, E. Four-decadal series of dendrometer measurements reveals trends in Pinus sylvestris L. inter- and intra-annual growth response to climatic conditions. Can. J. For. Res. 51, 445–454 (2020).

    Article 

    Google Scholar 

  • Gasparrini, A., Armstrong, B. & Kenward, M. G. Distributed lag non-linear models. Stat. Med. 29, 2224–2234 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Gasparrini, A. Distributed lag linear and non-linear models in R: the package dlnm. J. Stat. Softw. 43, https://doi.org/10.18637/jss.v043.i08 (2011).

  • Kartverket. Terrain Map. https://www.norgeskart.no/ (Norwegian Mapping Authority, 2008).

  • Autonomous body National Center for Geographic Information (CNIG). Digital Terrain Model – DTM25. http://centrodedescargas.cnig.es/ (2009).


  • Source: Ecology - nature.com

    Making hydropower plants more sustainable

    Nitrogen cycling and microbial cooperation in the terrestrial subsurface