{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T20:58:43Z","timestamp":1778619523241,"version":"3.51.4"},"reference-count":53,"publisher":"Proceedings of the National Academy of Sciences","issue":"22","license":[{"start":{"date-parts":[[2020,11,11]],"date-time":"2020-11-11T00:00:00Z","timestamp":1605052800000},"content-version":"vor","delay-in-days":184,"URL":"https:\/\/www.pnas.org\/site\/aboutpnas\/licenses.xhtml"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["DFG RE 603\/25-1"],"award-info":[{"award-number":["DFG RE 603\/25-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008398","name":"Villum Fonden","doi-asserted-by":"publisher","award":["16549"],"award-info":[{"award-number":["16549"]}],"id":[{"id":"10.13039\/100008398","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2020,6,2]]},"abstract":"<jats:p>Late-spring frosts (LSFs) affect the performance of plants and animals across the world\u2019s 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\u2019 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\u2019 innate resistance strategies, we estimate that \u223c35% of the European and \u223c26% of the Asian temperate forest area, but only \u223c10% 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.<\/jats:p>","DOI":"10.1073\/pnas.1920816117","type":"journal-article","created":{"date-parts":[[2020,5,12]],"date-time":"2020-05-12T00:24:58Z","timestamp":1589243098000},"page":"12192-12200","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":248,"title":["Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia"],"prefix":"10.1073","volume":"117","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8302-4854","authenticated-orcid":false,"given":"Constantin M.","family":"Zohner","sequence":"first","affiliation":[{"name":"Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;"}]},{"given":"Lidong","family":"Mo","sequence":"additional","affiliation":[{"name":"Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3704-0703","authenticated-orcid":false,"given":"Susanne S.","family":"Renner","sequence":"additional","affiliation":[{"name":"Systematic Botany and Mycology, Department of Biology, Ludwig Maximilian University of Munich, 80638 Munich, Germany;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3415-0862","authenticated-orcid":false,"given":"Jens-Christian","family":"Svenning","sequence":"additional","affiliation":[{"name":"Center for Biodiversity Dynamics in a Changing World (BIOCHANGE), Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;"},{"name":"Section for Ecoinformatics and Biodiversity, Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7454-505X","authenticated-orcid":false,"given":"Yann","family":"Vitasse","sequence":"additional","affiliation":[{"name":"Swiss Federal Institute for Forest, Snow and Landscape Research WSL, CH-8903 Birmensdorf, Switzerland;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5105-7232","authenticated-orcid":false,"given":"Blas M.","family":"Benito","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Bergen, 5020 Bergen, Norway;"}]},{"given":"Alejandro","family":"Ordonez","sequence":"additional","affiliation":[{"name":"Center for Biodiversity Dynamics in a Changing World (BIOCHANGE), Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;"},{"name":"Section for Ecoinformatics and Biodiversity, Department of Biology, Aarhus University, DK-8000 Aarhus C, Denmark;"},{"name":"Copernicus Institute of Sustainable Development, University of Utrecht, 3584 CS Utrecht, The Netherlands;"}]},{"given":"Frederik","family":"Baumgarten","sequence":"additional","affiliation":[{"name":"Swiss Federal Institute for Forest, Snow and Landscape Research WSL, CH-8903 Birmensdorf, Switzerland;"}]},{"given":"Jean-Fran\u00e7ois","family":"Bastin","sequence":"additional","affiliation":[{"name":"Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;"},{"name":"Computational and Applied Vegetation Ecology Lab, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, Ghent 9000, Belgium;"}]},{"given":"Veronica","family":"Sebald","sequence":"additional","affiliation":[{"name":"Systematic Botany and Mycology, Department of Biology, Ludwig Maximilian University of Munich, 80638 Munich, Germany;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4424-662X","authenticated-orcid":false,"given":"Peter B.","family":"Reich","sequence":"additional","affiliation":[{"name":"Department of Forest Resources, University of Minnesota, St. Paul, MN 55108;"},{"name":"Hawkesbury Institute for the Environment, Western Sydney University, Penrith NSW 2753, Australia;"}]},{"given":"Jingjing","family":"Liang","sequence":"additional","affiliation":[{"name":"Lab of Forest Advanced Computing and Artificial Intelligence, Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907;"}]},{"given":"Gert-Jan","family":"Nabuurs","sequence":"additional","affiliation":[{"name":"Wageningen Environmental Research, Wageningen University and Research, 6700AA, Wageningen, The Netherlands;"},{"name":"Forest Ecology and Forest Management, Wageningen University and Research, 6700AA, Wageningen, The Netherlands;"}]},{"given":"Sergio","family":"de-Miguel","sequence":"additional","affiliation":[{"name":"Department of Crop and Forest Sciences, University of Lleida, E25198 Lleida, Spain;"},{"name":"Joint Research Unit, Forest Science and Technology Centre of Catalonia CTFC\u2013Centre for Research in Agrotechnology, E25280, Solsona, Spain;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2422-3009","authenticated-orcid":false,"given":"Giorgio","family":"Alberti","sequence":"additional","affiliation":[{"name":"Department of Agricultural, Food, Environmental and Animal Sciences, University of Udine, 33100 Udine, Italy;"},{"name":"Institute of BioEconomy, National Research Council, 50019 Florence, Italy;"}]},{"given":"Clara","family":"Ant\u00f3n-Fern\u00e1ndez","sequence":"additional","affiliation":[{"name":"Division of Forestry and Forest Resources NIBIO, Norwegian Institute of Bioeconomy Research, NO-1431 \u00c5s, Norway;"}]},{"given":"Radomir","family":"Balazy","sequence":"additional","affiliation":[{"name":"Department of Geomatics, Forest Research Institute, Sekocin Stary, 05-090 Raszyn, Poland;"}]},{"given":"Urs-Beat","family":"Br\u00e4ndli","sequence":"additional","affiliation":[{"name":"Swiss National Forest Inventory, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, CH-8903 Birmensdorf, Switzerland;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9477-5541","authenticated-orcid":false,"given":"Han Y. H.","family":"Chen","sequence":"additional","affiliation":[{"name":"Faculty of Natural Resources Management, Lakehead University, Thunder Bay, ON P7B 5E1, Canada;"},{"name":"Key Laboratory for Humid Subtropical Eco-geographical Processes of the Ministry of Education, School of Geographical Sciences, Fujian Normal University, 350117 Fujian, China;"}]},{"given":"Chelsea","family":"Chisholm","sequence":"additional","affiliation":[{"name":"Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), 8092 Zurich, Switzerland;"}]},{"given":"Emil","family":"Cienciala","sequence":"additional","affiliation":[{"name":"Institute of Forest Ecosystem Research IFER, CZ 254 01 Jilove u Prahy, Czech Republic;"},{"name":"Global Change Research Institute, Czech Academy of Sciences, CZ 603 00 Brno, Czech Republic;"}]},{"given":"Selvadurai","family":"Dayanandan","sequence":"additional","affiliation":[{"name":"Centre for Structural and Functional Genomics, Biology Department, Concordia University, Montreal, QC H4B 1R6, Canada;"},{"name":"Quebec Centre for Biodiversity Science, Biology Department, Concordia University, Montreal, QC H4B 1R6, Canada;"}]},{"given":"Tom M.","family":"Fayle","sequence":"additional","affiliation":[{"name":"Biology Centre of the Czech Academy of Sciences, Institute of Entomology, 370 05 Ceske Budejovice, Czech Republic;"},{"name":"Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, 88400 Kota Kinabalu, Sabah, Malaysia;"}]},{"given":"Lorenzo","family":"Frizzera","sequence":"additional","affiliation":[{"name":"Department of Sustainable Agro-ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, 38010 San Michele all\u2019Adige, Trentino, Italy;"}]},{"given":"Damiano","family":"Gianelle","sequence":"additional","affiliation":[{"name":"Department of Sustainable Agro-ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund Mach, 38010 San Michele all\u2019Adige, Trentino, Italy;"}]},{"given":"Andrzej M.","family":"Jagodzinski","sequence":"additional","affiliation":[{"name":"Institute of Dendrology, Polish Academy of Sciences, PL-62-035 K\u00f3rnik, Poland;"},{"name":"Faculty of Forestry, Department of Game Management and Forest Protection, Poznan University of Life Sciences, PL-60-625 Poznan, Poland;"}]},{"given":"Bogdan","family":"Jaroszewicz","sequence":"additional","affiliation":[{"name":"Bia\u0142owie\u017ca Geobotanical Station, Faculty of Biology, University of Warsaw, PL-17-230 Bialowieza, Poland;"}]},{"given":"Tommaso","family":"Jucker","sequence":"additional","affiliation":[{"name":"School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ United Kingdom;"}]},{"given":"Sebastian","family":"Kepfer-Rojas","sequence":"additional","affiliation":[{"name":"Department of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg C 1958, Denmark;"}]},{"given":"Mohammed Latif","family":"Khan","sequence":"additional","affiliation":[{"name":"Department of Botany, Dr. Harisingh Gour Vishwavidyalaya University, Sagar, Madhya Pradesh 470003, India;"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3440-6071","authenticated-orcid":false,"given":"Hyun Seok","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Forest Sciences, Seoul National University, 08826 Seoul, Republic of Korea;"},{"name":"Interdisciplinary Program in Agricultural and Forest Meteorology, Seoul National University, 08826 Seoul, Republic of Korea;"},{"name":"National Center for Agro Meteorology, 08826 Seoul, Republic of Korea;"},{"name":"Research Institute for Agriculture and Life Sciences, Seoul National University, 08826 Seoul, Republic of Korea;"}]},{"given":"Henn","family":"Korjus","sequence":"additional","affiliation":[{"name":"Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, Estonia;"}]},{"given":"Vivian Kvist","family":"Johannsen","sequence":"additional","affiliation":[{"name":"Department of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg C 1958, Denmark;"}]},{"given":"Diana","family":"Laarmann","sequence":"additional","affiliation":[{"name":"Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, Estonia;"}]},{"given":"Mait","family":"Lang","sequence":"additional","affiliation":[{"name":"Institute of Forestry and Rural Engineering, Estonian University of Life Sciences, 51006 Tartu, Estonia;"},{"name":"Tartu Observatory, University of Tartu, 61602 T\u00f5ravere, Estonia;"}]},{"given":"Tomasz","family":"Zawila-Niedzwiecki","sequence":"additional","affiliation":[{"name":"Coordination Centre for Environmental Projects, Polish State Forests, 02-362 Warsaw, Poland;"}]},{"given":"Pascal A.","family":"Niklaus","sequence":"additional","affiliation":[{"name":"Department of Evolutionary Biology and Environmental 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