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Research Article

Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia

View ORCID ProfileConstantin M. Zohner, Lidong Mo, View ORCID ProfileSusanne S. Renner, View ORCID ProfileJens-Christian Svenning, View ORCID ProfileYann Vitasse, View ORCID ProfileBlas M. Benito, Alejandro Ordonez, Frederik Baumgarten, Jean-François Bastin, Veronica Sebald, View ORCID ProfilePeter B. Reich, Jingjing Liang, Gert-Jan Nabuurs, Sergio de-Miguel, View ORCID ProfileGiorgio Alberti, Clara Antón-Fernández, Radomir Balazy, Urs-Beat Brändli, View ORCID ProfileHan Y. H. Chen, Chelsea Chisholm, Emil Cienciala, Selvadurai Dayanandan, Tom M. Fayle, Lorenzo Frizzera, Damiano Gianelle, Andrzej M. Jagodzinski, Bogdan Jaroszewicz, Tommaso Jucker, Sebastian Kepfer-Rojas, Mohammed Latif Khan, View ORCID ProfileHyun Seok Kim, Henn Korjus, Vivian Kvist Johannsen, Diana Laarmann, Mait Lang, Tomasz Zawila-Niedzwiecki, Pascal A. Niklaus, Alain Paquette, Hans Pretzsch, Purabi Saikia, Peter Schall, Vladimír Šebeň, Miroslav Svoboda, Elena Tikhonova, Helder Viana, Chunyu Zhang, Xiuhai Zhao, and Thomas W. Crowther
PNAS June 2, 2020 117 (22) 12192-12200; first published May 11, 2020; https://doi.org/10.1073/pnas.1920816117
Constantin M. Zohner
aInstitute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;
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  • ORCID record for Constantin M. Zohner
  • For correspondence: constantin.zohner@t-online.de
Lidong Mo
aInstitute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;
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Susanne S. Renner
bSystematic Botany and Mycology, Department of Biology, Ludwig Maximilian University of Munich, 80638 Munich, Germany;
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Jens-Christian Svenning
cCenter for Biodiversity Dynamics in a Changing World (BIOCHANGE), Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;
dSection for Ecoinformatics and Biodiversity, Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;
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Yann Vitasse
eSwiss Federal Institute for Forest, Snow and Landscape Research WSL, CH-8903 Birmensdorf, Switzerland;
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Blas M. Benito
fDepartment of Biological Sciences, University of Bergen, 5020 Bergen, Norway;
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Alejandro Ordonez
cCenter for Biodiversity Dynamics in a Changing World (BIOCHANGE), Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;
dSection for Ecoinformatics and Biodiversity, Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;
gCopernicus Institute of Sustainable Development, University of Utrecht, 3584 CS Utrecht, The Netherlands;
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Frederik Baumgarten
eSwiss Federal Institute for Forest, Snow and Landscape Research WSL, CH-8903 Birmensdorf, Switzerland;
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Jean-François Bastin
aInstitute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;
hComputational and Applied Vegetation Ecology Lab, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, Ghent 9000, Belgium;
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Veronica Sebald
bSystematic Botany and Mycology, Department of Biology, Ludwig Maximilian University of Munich, 80638 Munich, Germany;
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Peter B. Reich
iDepartment of Forest Resources, University of Minnesota, St. Paul, MN 55108;
jHawkesbury Institute for the Environment, Western Sydney University, Penrith NSW 2753, Australia;
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Jingjing Liang
kLab of Forest Advanced Computing and Artificial Intelligence, Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907;
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Gert-Jan Nabuurs
lWageningen Environmental Research, Wageningen University and Research, 6700AA, Wageningen, The Netherlands;
mForest Ecology and Forest Management, Wageningen University and Research, 6700AA, Wageningen, The Netherlands;
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Sergio de-Miguel
nDepartment of Crop and Forest Sciences, University of Lleida, E25198 Lleida, Spain;
oJoint Research Unit, Forest Science and Technology Centre of Catalonia CTFC–Centre for Research in Agrotechnology, E25280, Solsona, Spain;
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Giorgio Alberti
pDepartment of Agricultural, Food, Environmental and Animal Sciences, University of Udine, 33100 Udine, Italy;
qInstitute of BioEconomy, National Research Council, 50019 Florence, Italy;
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Clara Antón-Fernández
rDivision of Forestry and Forest Resources NIBIO, Norwegian Institute of Bioeconomy Research, NO-1431 Ås, Norway;
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Radomir Balazy
sDepartment of Geomatics, Forest Research Institute, Sekocin Stary, 05-090 Raszyn, Poland;
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Urs-Beat Brändli
tSwiss National Forest Inventory, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, CH-8903 Birmensdorf, Switzerland;
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Han Y. H. Chen
uFaculty of Natural Resources Management, Lakehead University, Thunder Bay, ON P7B 5E1, Canada;
vKey Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, 350117 Fujian, China;
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Chelsea Chisholm
aInstitute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;
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Emil Cienciala
wInstitute of Forest Ecosystem Research IFER, CZ 254 01 Jilove u Prahy, Czech Republic;
xGlobal Change Research Institute, Czech Academy of Sciences, CZ 603 00 Brno, Czech Republic;
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Selvadurai Dayanandan
yCentre for Structural and Functional Genomics, Biology Department, Concordia University, Montreal, QC H4B 1R6, Canada;
zQuebec Centre for Biodiversity Science, Biology Department, Concordia University, Montreal, QC H4B 1R6, Canada;
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Tom M. Fayle
aaBiology Centre of the Czech Academy of Sciences, Institute of Entomology, 370 05 Ceske Budejovice, Czech Republic;
bbInstitute for Tropical Biology and Conservation, Universiti Malaysia Sabah, 88400 Kota Kinabalu, Sabah, Malaysia;
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Lorenzo Frizzera
ccDepartment of Sustainable Agro-ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, 38010 San Michele all’Adige, Trentino, Italy;
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Damiano Gianelle
ccDepartment of Sustainable Agro-ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, 38010 San Michele all’Adige, Trentino, Italy;
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Andrzej M. Jagodzinski
ddInstitute of Dendrology, Polish Academy of Sciences, PL-62-035 Kórnik, Poland;
eeFaculty of Forestry, Department of Game Management and Forest Protection, Poznan University of Life Sciences, PL-60-625 Poznan, Poland;
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Bogdan Jaroszewicz
ffBiałowieża Geobotanical Station, Faculty of Biology, University of Warsaw, PL-17-230 Bialowieza, Poland;
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Tommaso Jucker
ggSchool of Biological Sciences, University of Bristol, Bristol, BS8 1TQ United Kingdom;
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Sebastian Kepfer-Rojas
hhDepartment of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg C 1958, Denmark;
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Mohammed Latif Khan
iiDepartment of Botany, Dr. Harisingh Gour Vishwavidyalaya University, Sagar, Madhya Pradesh 470003, India;
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Hyun Seok Kim
jjDepartment of Forest Sciences, Seoul National University, 08826 Seoul, Republic of Korea;
kkInterdisciplinary Program in Agricultural and Forest Meteorology, Seoul National University, 08826 Seoul, Republic of Korea;
llNational Center for Agro Meteorology, 08826 Seoul, Republic of Korea;
mmResearch Institute for Agriculture and Life Sciences, Seoul National University, 08826 Seoul, Republic of Korea;
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Henn Korjus
nnInstitute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, Estonia;
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Vivian Kvist Johannsen
hhDepartment of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg C 1958, Denmark;
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Diana Laarmann
nnInstitute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, Estonia;
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Mait Lang
nnInstitute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, Estonia;
ooTartu Observatory, University of Tartu, 61602 Tõravere, Estonia;
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Tomasz Zawila-Niedzwiecki
ppCoordination Centre for Environmental Projects, Polish State Forests, 02-362 Warsaw, Poland;
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Pascal A. Niklaus
qqDepartment of Evolutionary Biology and Environmental Studies, University of Zurich, 8057 Zurich, Switzerland;
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Alain Paquette
rrCentre for Forest Research, Université du Québec à Montréal, Montreal, H3C 3P8 Canada;
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Hans Pretzsch
ssSchool of Life Sciences Weihenstephan, Technical University of Munich, 85354 Freising, Germany;
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Purabi Saikia
ttDepartment of Environmental Sciences, Central University of Jharkhand, Brambe, Ranchi, Jharkhand 835205, India;
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Peter Schall
uuSilviculture and Forest Ecology of the Temperate Zones, University of Göttingen, 37077 Göttingen, Germany;
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Vladimír Šebeň
vvNational Forest Centre, 96001 Zvolen, Slovak Republic;
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Miroslav Svoboda
wwFaculty of Forestry and Wood Sciences, Czech University of Life Sciences in Prague, Praha 6 Suchdol, 16521, Czech Republic;
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Elena Tikhonova
xxCenter for Forest Ecology and Productivity, Russian Academy of Sciences, 117997 Moscow, Russian Federation;
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Helder Viana
yyAgricultural High School, Polytechnic Institute of Viseu, 3500-606 Viseu, Portugal;
zzCentre for the Research and Technology of Agro-Environmental and Biological Sciences, Universidade de Trás-os-Montes e Alto Douro, Quinta de Prados, 5000-801 Vila Real, Portugal;
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Chunyu Zhang
aaaResearch Center of Forest Management Engineering of State Forestry and Grassland Administration, Beijing Forestry University, 100083 Beijing, China
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Xiuhai Zhao
aaaResearch Center of Forest Management Engineering of State Forestry and Grassland Administration, Beijing Forestry University, 100083 Beijing, China
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Thomas W. Crowther
aInstitute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;
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  1. Edited by Thomas J. Givnish, University of Wisconsin–Madison, Madison, WI, and accepted by Editorial Board Member Robert E. Dickinson March 30, 2020 (received for review November 29, 2019)

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Significance

Frost in late spring causes severe ecosystem damage in temperate and boreal regions. We here analyze late-spring frost occurrences between 1959 and 2017 and woody species’ resistance strategies to forecast forest vulnerability under climate change. Leaf-out phenology and leaf-freezing resistance data come from up to 1,500 species cultivated in common gardens. The greatest increase in leaf-damaging spring frost has occurred in Europe and East Asia, where species are more vulnerable to spring frost than in North America. The data imply that 35 and 26% of Europe’s and Asia’s forests are increasingly threatened by frost damage, while this is only true for 10% of North America. Phenological strategies that helped trees tolerate past frost frequencies will thus be increasingly mismatched to future conditions

Abstract

Late-spring frosts (LSFs) affect the performance of plants and animals across the world’s temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees’ adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species’ innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.

  • climate change
  • phenology
  • spring leaf-out
  • late frost
  • freezing damage

Footnotes

  • ↵1C.M.Z. and L.M. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: constantin.zohner{at}t-online.de.
  • Author contributions: C.M.Z. conceived and developed the study with input from S.S.R. and J.-C.S.; C.M.Z. and L.M. performed research; L.M., B.M.B., and A.O. computed the frost risk maps; C.M.Z. and V.S. collected the phenology and leaf freezing resistance data; C.M.Z. wrote the manuscript with assistance from S.S.R. and T.W.C.; Y.V., B.M.B., A.O., F.B., J.-F.B., V.S., P.B.R., and J.L. provided input on the manuscript text; P.B.R., G.-J.N., S.d.-M., G.A., C.A.-F., R.B., U.-B.B., H.Y.H.C., C.C., E.C., S.D., T.M.F., L.F., D.G., A.M.J., B.J., T.J., S.K.-R., M.L.K., H.S.K., H.K., V.K.J., D.L., M.L., T.Z.-N., P.A.N., A.P., H.P., P. Saikia, P. Schall, V.Š., M.S., E.T., H.V., C.Z., and X.Z. contributed forest inventory data; and all authors reviewed the manuscript.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission. T.J.G. is a guest editor invited by the Editorial Board.

  • Data deposition: All source code, models, and raw data have been deposited in GitHub (https://github.com/LidongMo/FrostRiskProject) and Datasets S1–S3.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1920816117/-/DCSupplemental.

Published under the PNAS license.

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Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia
Constantin M. Zohner, Lidong Mo, Susanne S. Renner, Jens-Christian Svenning, Yann Vitasse, Blas M. Benito, Alejandro Ordonez, Frederik Baumgarten, Jean-François Bastin, Veronica Sebald, Peter B. Reich, Jingjing Liang, Gert-Jan Nabuurs, Sergio de-Miguel, Giorgio Alberti, Clara Antón-Fernández, Radomir Balazy, Urs-Beat Brändli, Han Y. H. Chen, Chelsea Chisholm, Emil Cienciala, Selvadurai Dayanandan, Tom M. Fayle, Lorenzo Frizzera, Damiano Gianelle, Andrzej M. Jagodzinski, Bogdan Jaroszewicz, Tommaso Jucker, Sebastian Kepfer-Rojas, Mohammed Latif Khan, Hyun Seok Kim, Henn Korjus, Vivian Kvist Johannsen, Diana Laarmann, Mait Lang, Tomasz Zawila-Niedzwiecki, Pascal A. Niklaus, Alain Paquette, Hans Pretzsch, Purabi Saikia, Peter Schall, Vladimír Šebeň, Miroslav Svoboda, Elena Tikhonova, Helder Viana, Chunyu Zhang, Xiuhai Zhao, Thomas W. Crowther
Proceedings of the National Academy of Sciences Jun 2020, 117 (22) 12192-12200; DOI: 10.1073/pnas.1920816117

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Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia
Constantin M. Zohner, Lidong Mo, Susanne S. Renner, Jens-Christian Svenning, Yann Vitasse, Blas M. Benito, Alejandro Ordonez, Frederik Baumgarten, Jean-François Bastin, Veronica Sebald, Peter B. Reich, Jingjing Liang, Gert-Jan Nabuurs, Sergio de-Miguel, Giorgio Alberti, Clara Antón-Fernández, Radomir Balazy, Urs-Beat Brändli, Han Y. H. Chen, Chelsea Chisholm, Emil Cienciala, Selvadurai Dayanandan, Tom M. Fayle, Lorenzo Frizzera, Damiano Gianelle, Andrzej M. Jagodzinski, Bogdan Jaroszewicz, Tommaso Jucker, Sebastian Kepfer-Rojas, Mohammed Latif Khan, Hyun Seok Kim, Henn Korjus, Vivian Kvist Johannsen, Diana Laarmann, Mait Lang, Tomasz Zawila-Niedzwiecki, Pascal A. Niklaus, Alain Paquette, Hans Pretzsch, Purabi Saikia, Peter Schall, Vladimír Šebeň, Miroslav Svoboda, Elena Tikhonova, Helder Viana, Chunyu Zhang, Xiuhai Zhao, Thomas W. Crowther
Proceedings of the National Academy of Sciences Jun 2020, 117 (22) 12192-12200; DOI: 10.1073/pnas.1920816117
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Proceedings of the National Academy of Sciences: 117 (22)
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  • Article
    • Abstract
    • Geographic Variation in Late-Spring Frosts
    • Biogeographic Variation in Plant Traits That Govern Frost Susceptibility
    • Spatiotemporal Projections of Late-Spring Frost
    • Methods
    • Acknowledgments
    • Footnotes
    • References
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