Warming-induced phenological mismatch between trees and shrubs explains high-elevation forest expansion

ABSTRACT Despite the importance of species interaction in modulating the range shifts of plants, little is known about the responses of coexisting life forms to a warmer climate. Here, we combine long-term monitoring of cambial phenology in sympatric trees and shrubs at two treelines of the Tibetan Plateau, with a meta-analysis of ring-width series from 344 shrubs and 575 trees paired across 11 alpine treelines in the Northern Hemisphere. Under a spring warming of +1°C, xylem resumption advances by 2–4 days in trees, but delays by 3–8 days in shrubs. The divergent phenological response to warming was due to shrubs being 3.2 times more sensitive than trees to chilling accumulation. Warmer winters increased the thermal requirement for cambial reactivation in shrubs, leading to a delayed response to warmer springs. Our meta-analysis confirmed such a mechanism across continental scales. The warming-induced phenological mismatch may give a competitive advantage to trees over shrubs, which would provide a new explanation for increasing alpine treeline shifts under the context of climate change.

[1]  Intergovernmental Panel on Climate Change Climate Change 2021 – The Physical Science Basis , 2023 .

[2]  C. Körner,et al.  Chronic in situ tissue cooling does not reduce lignification at the Swiss treeline but enhances the risk of ‘blue’ frost rings , 2023, Alpine Botany.

[3]  Sara E. Kuebbing,et al.  Warmer temperatures are linked to widespread phenological mismatch among native and non‐native forest plants , 2022, Journal of Ecology.

[4]  A. Deslauriers,et al.  The early bud gets the cold: diverging spring phenology drives exposure to late frost in a Picea mariana [(Mill.) BSP] common garden. , 2022, Physiologia plantarum.

[5]  F. Sun,et al.  The continuing shrinkage of snow cover in High Mountain Asia over the last four decades. , 2022, Science bulletin.

[6]  Tao Wang,et al.  Enhanced habitat loss of the Himalayan endemic flora driven by warming-forced upslope tree expansion , 2022, Nature Ecology & Evolution.

[7]  J. Peñuelas,et al.  An earlier start of the thermal growing season enhances tree growth in cold humid areas but not in dry areas , 2022, Nature Ecology & Evolution.

[8]  J. Alexander,et al.  Competition contributes to both warm and cool range edges , 2022, bioRxiv.

[9]  P. Ciais,et al.  Deciphering the multiple effects of climate warming on the temporal shift of leaf unfolding , 2022, Nature Climate Change.

[10]  Huiying Liu,et al.  Phenological mismatches between above- and belowground plant responses to climate warming , 2021, Nature Climate Change.

[11]  A. Menzel,et al.  Diverging growth performance of co-occurring trees (Picea abies) and shrubs (Pinus mugo) at the treeline ecotone of Central European mountain ranges , 2021 .

[12]  M. Carrer,et al.  Growing faster, longer or both? Modelling plastic response of Juniperus communis growth phenology to climate change , 2021, Global Ecology and Biogeography.

[13]  I. Ibáñez,et al.  Spring phenological escape is critical for the survival of temperate tree seedlings , 2021, Functional Ecology.

[14]  G. Bonanomi,et al.  Shrub facilitation promotes advancing of the Fagus sylvatica treeline across the Apennines (Italy) , 2021, Journal of Vegetation Science.

[15]  G. Drolet,et al.  Regionwide temporal gradients of carbon allocation allow for shoot growth and latewood formation in boreal black spruce , 2021, Global Ecology and Biogeography.

[16]  M. Shen,et al.  No benefits from warming even for subnival vegetation in the central Himalayas. , 2021, Science bulletin.

[17]  Erin M. Schliep,et al.  Seasonal temperature–moisture interactions limit seedling establishment at upper treeline in the Southern Rockies , 2021, Ecosphere.

[18]  Ronggao Liu,et al.  Divergent changes of the elevational synchronicity in vegetation spring phenology in North China from 2001 to 2017 in connection with variations in chilling , 2021, International Journal of Climatology.

[19]  Mu-yi Kang,et al.  Intra-annual growth dynamics of Picea meyeri needles, shoots, and stems on Luya Mountain, North-central China , 2021 .

[20]  Alice C Hughes,et al.  The global significance of biodiversity science in China: an overview , 2021, National science review.

[21]  Eliot J. B. McIntire,et al.  Global fading of the temperature–growth coupling at alpine and polar treelines , 2021, Global change biology.

[22]  Sumit Singh Chauhan,et al.  A review on genetic algorithm: past, present, and future , 2020, Multim. Tools Appl..

[23]  D. Flynn,et al.  Winter temperatures predominate in spring phenological responses to warming , 2020, Nature Climate Change.

[24]  A. Hastings,et al.  Interspecific competition slows range expansion and shapes range boundaries , 2020, Proceedings of the National Academy of Sciences.

[25]  M. Mayfield,et al.  Beyond direct neighbourhood effects: higher-order interactions improve modelling and predicting tree survival and growth , 2020, National science review.

[26]  A. Deslauriers,et al.  Comparing the Cell Dynamics of Tree-Ring Formation Observed in Microcores and as Predicted by the Vaganov–Shashkin Model , 2020, Frontiers in Plant Science.

[27]  R. Tognetti,et al.  Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers , 2020, Proceedings of the National Academy of Sciences.

[28]  Michał Bogdziewicz,et al.  Flowering synchrony drives reproductive success in a wind-pollinated tree. , 2020, Ecology letters.

[29]  Malcolm K. Hughes,et al.  An interpreted language implementation of the Vaganov–Shashkin tree-ring proxy system model , 2019, Dendrochronologia.

[30]  V. Rudolf The role of seasonal timing and phenological shifts for species coexistence. , 2019, Ecology letters.

[31]  Václav Treml,et al.  Differences in growth between shrubs and trees: How does the stature of woody plants influence their ability to thrive in cold regions? , 2019, Agricultural and Forest Meteorology.

[32]  N. Delpierre,et al.  Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers , 2019, Global change biology.

[33]  P. Jones,et al.  An Ensemble Version of the E‐OBS Temperature and Precipitation Data Sets , 2018, Journal of Geophysical Research: Atmospheres.

[34]  Andrew Gelman,et al.  Global shifts in the phenological synchrony of species interactions over recent decades , 2018, Proceedings of the National Academy of Sciences.

[35]  N. Delpierre,et al.  Warmer winters reduce the advance of tree spring phenology induced by warmer springs in the Alps , 2018 .

[36]  R. Danby,et al.  Factors influencing the establishment and growth of tree seedlings at Subarctic alpine treelines , 2018 .

[37]  M. Carrer,et al.  Diverging shrub and tree growth from the Polar to the Mediterranean biomes across the European continent , 2017, Global change biology.

[38]  E. Vaganov,et al.  New perspective on spring vegetation phenology and global climate change based on Tibetan Plateau tree-ring data , 2017, Proceedings of the National Academy of Sciences.

[39]  C. Rixen,et al.  ‘Hearing’ alpine plants growing after snowmelt: ultrasonic snow sensors provide long-term series of alpine plant phenology , 2017, International Journal of Biometeorology.

[40]  Blas M. Benito,et al.  Day length unlikely to constrain climate-driven shifts in leaf-out times of northern woody plants , 2016 .

[41]  David Frank,et al.  Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere , 2016, Global change biology.

[42]  Guillaume Charrier,et al.  Can phenological models predict tree phenology accurately in the future? The unrevealed hurdle of endodormancy break , 2016, Global change biology.

[43]  E. Liang,et al.  Temperature thresholds for the onset of xylogenesis in alpine shrubs on the Tibetan Plateau , 2016, Trees.

[44]  C. Körner,et al.  Where, why and how? Explaining the low‐temperature range limits of temperate tree species , 2016 .

[45]  H. Mäkinen,et al.  Fine-scale distribution of treeline trees and the nurse plant facilitation on the eastern Tibetan Plateau , 2016 .

[46]  Yafeng Wang,et al.  Species interactions slow warming-induced upward shifts of treelines on the Tibetan Plateau , 2016, Proceedings of the National Academy of Sciences.

[47]  Cyrille B K Rathgeber,et al.  Woody biomass production lags stem-girth increase by over one month in coniferous forests , 2015, Nature Plants.

[48]  R. Tognetti,et al.  Synchronisms and correlations of spring phenology between apical and lateral meristems in two boreal conifers. , 2015, Tree physiology.

[49]  Philippe Ciais,et al.  Declining global warming effects on the phenology of spring leaf unfolding , 2015, Nature.

[50]  H. Fowler,et al.  Elevation-dependent warming in mountain regions of the world , 2015 .

[51]  S. Huang,et al.  Half-century evidence from western Canada shows forest dynamics are primarily driven by competition followed by climate , 2015, Proceedings of the National Academy of Sciences.

[52]  C. Pickering,et al.  Shrub facilitation is an important driver of alpine plant community diversity and functional composition , 2015, Biodiversity and Conservation.

[53]  Wilfried Thuiller,et al.  The influence of interspecific interactions on species range expansion rates , 2014, Ecography.

[54]  Melanie Smith,et al.  Alpine Treelines: Functional Ecology of the Global High Elevation Tree Limits , 2013 .

[55]  J. Cornelissen,et al.  Shrub-tree interactions and environmental changes drive treeline dynamics in the Subarctic. , 2012 .

[56]  G. Elliott Extrinsic regime shifts drive abrupt changes in regeneration dynamics at upper treeline in the Rocky Mountains, U.S.A. , 2012, Ecology.

[57]  Forrest M Hoffman,et al.  Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling , 2012, Proceedings of the National Academy of Sciences.

[58]  A. Deslauriers,et al.  Xylem phenology and wood production: resolving the chicken-or-egg dilemma. , 2010, Plant, cell & environment.

[59]  A. Deslauriers,et al.  Critical temperatures for xylogenesis in conifers of cold climates , 2008 .

[60]  J. Peñuelas,et al.  Migration, invasion and decline: changes in recruitment and forest structure in a warming‐linked shift of European beech forest in Catalonia (NE Spain) , 2007 .

[61]  Philippe Ciais,et al.  Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades , 2007 .

[62]  G. Miehe,et al.  Highest Treeline in the Northern Hemisphere Found in Southern Tibet , 2007 .

[63]  Koen Kramer,et al.  Selecting a model to predict the onset of growth of Fagus sylvatica , 1994 .

[64]  R. Pape,et al.  Thermal niche predictors of alpine plant species. , 2019, Ecology.