Frontiers in Plant Science (Jan 2019)
Early-Warning Signals of Individual Tree Mortality Based on Annual Radial Growth
- Maxime Cailleret,
- Maxime Cailleret,
- Vasilis Dakos,
- Steven Jansen,
- Elisabeth M. R. Robert,
- Elisabeth M. R. Robert,
- Elisabeth M. R. Robert,
- Tuomas Aakala,
- Mariano M. Amoroso,
- Mariano M. Amoroso,
- Joe A. Antos,
- Christof Bigler,
- Harald Bugmann,
- Marco Caccianaga,
- Jesus-Julio Camarero,
- Paolo Cherubini,
- Marie R. Coyea,
- Katarina Čufar,
- Adrian J. Das,
- Hendrik Davi,
- Guillermo Gea-Izquierdo,
- Sten Gillner,
- Laurel J. Haavik,
- Laurel J. Haavik,
- Henrik Hartmann,
- Ana-Maria Hereş,
- Ana-Maria Hereş,
- Kevin R. Hultine,
- Pavel Janda,
- Jeffrey M. Kane,
- Viachelsav I. Kharuk,
- Viachelsav I. Kharuk,
- Thomas Kitzberger,
- Thomas Kitzberger,
- Tamir Klein,
- Tom Levanic,
- Juan-Carlos Linares,
- Fabio Lombardi,
- Harri Mäkinen,
- Ilona Mészáros,
- Juha M. Metsaranta,
- Walter Oberhuber,
- Andreas Papadopoulos,
- Any Mary Petritan,
- Any Mary Petritan,
- Brigitte Rohner,
- Gabriel Sangüesa-Barreda,
- Jeremy M. Smith,
- Amanda B. Stan,
- Dejan B. Stojanovic,
- Maria-Laura Suarez,
- Miroslav Svoboda,
- Volodymyr Trotsiuk,
- Volodymyr Trotsiuk,
- Volodymyr Trotsiuk,
- Ricardo Villalba,
- Alana R. Westwood,
- Peter H. Wyckoff,
- Jordi Martínez-Vilalta,
- Jordi Martínez-Vilalta
Affiliations
- Maxime Cailleret
- Department of Environmental Systems Science, Forest Ecology, Institute of Terrestrial Ecosystems, ETH Zürich, Zurich, Switzerland
- Maxime Cailleret
- Swiss Federal Institute for Forest, Snow and Landscape Research – WSL, Birmensdorf, Switzerland
- Vasilis Dakos
- CNRS, IRD, EPHE, ISEM, Université de Montpellier, Montpellier, France
- Steven Jansen
- Institute of Systematic Botany and Ecology, Ulm University, Ulm, Germany
- Elisabeth M. R. Robert
- CREAF, Cerdanyola del Vallès, Catalonia, Spain
- Elisabeth M. R. Robert
- Ecology and Biodiversity, Vrije Universiteit Brussel, Brussels, Belgium
- Elisabeth M. R. Robert
- Laboratory of Wood Biology and Xylarium, Royal Museum for Central Africa, Tervuren, Belgium
- Tuomas Aakala
- Department of Forest Sciences, University of Helsinki, Helsinki, Finland
- Mariano M. Amoroso
- Consejo Nacional de Investigaciones Científicas y Técnicas, CCT Patagonia Norte, Río Negro, Argentina
- Mariano M. Amoroso
- 0Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural, Sede Andina, Universidad Nacional de Río Negro, Río Negro, Argentina
- Joe A. Antos
- 1Department of Biology, University of Victoria, Victoria, BC, Canada
- Christof Bigler
- Department of Environmental Systems Science, Forest Ecology, Institute of Terrestrial Ecosystems, ETH Zürich, Zurich, Switzerland
- Harald Bugmann
- Department of Environmental Systems Science, Forest Ecology, Institute of Terrestrial Ecosystems, ETH Zürich, Zurich, Switzerland
- Marco Caccianaga
- 2Dipartimento di Bioscienze, Università degli Studi di Milano, Milan, Italy
- Jesus-Julio Camarero
- 3Instituto Pirenaico de Ecología (IPE-CSIC), Zaragoza, Spain
- Paolo Cherubini
- Swiss Federal Institute for Forest, Snow and Landscape Research – WSL, Birmensdorf, Switzerland
- Marie R. Coyea
- 4Centre for Forest Research, Département des Sciences du Bois et de la Forêt, Faculté de Foresterie, de Géographie et de Géomatique, Université Laval, Québec, QC, Canada
- Katarina Čufar
- 5Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia
- Adrian J. Das
- 6United States Geological Survey, Western Ecological Research Center, Sequoia and Kings Canyon Field Station, Three Rivers, CA, United States
- Hendrik Davi
- 7Ecologie des Forêts Méditerranéennes (URFM), Institut National de la Recherche Agronomique, Avignon, France
- Guillermo Gea-Izquierdo
- 8Centro de Investigación Forestal (CIFOR), Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Madrid, Spain
- Sten Gillner
- 9Institute of Forest Botany and Forest Zoology, TU Dresden, Dresden, Germany
- Laurel J. Haavik
- 0USDA Forest Service, Forest Health Protection, Saint Paul, MN, United States
- Laurel J. Haavik
- 1Department of Entomology, University of Arkansas, Fayetteville, AR, United States
- Henrik Hartmann
- 2Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Jena, Germany
- Ana-Maria Hereş
- 3Department of Forest Sciences, Transilvania University of Brasov, Brașov, Romania
- Ana-Maria Hereş
- 4BC3 – Basque Centre for Climate Change, Leioa, Spain
- Kevin R. Hultine
- 5Department of Research, Conservation and Collections, Desert Botanical Garden, Phoenix, AZ, United States
- Pavel Janda
- 6Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Prague, Czechia
- Jeffrey M. Kane
- 7Department of Forestry and Wildland Resources, Humboldt State University, Arcata, CA, United States
- Viachelsav I. Kharuk
- 8Sukachev Institute of Forest, Siberian Division of the Russian Academy of Sciences, Krasnoyarsk, Russia
- Viachelsav I. Kharuk
- 9Siberian Federal University, Krasnoyarsk, Russia
- Thomas Kitzberger
- 0Department of Ecology, Universidad Nacional del Comahue, Río Negro, Argentina
- Thomas Kitzberger
- 1Instituto de Investigaciones en Biodiversidad y Medioambiente, Consejo Nacional de Investigaciones Científicas y Técnicas, Río Negro, Argentina
- Tamir Klein
- 2Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
- Tom Levanic
- 3Department of Yield and Silviculture, Slovenian Forestry Institute, Ljubljana, Slovenia
- Juan-Carlos Linares
- 4Department of Physical, Chemical and Natural Systems, Pablo de Olavide University, Seville, Spain
- Fabio Lombardi
- 5Department of Agricultural Science, Mediterranean University of Reggio Calabria, Reggio Calabria, Italy
- Harri Mäkinen
- 6Natural Resources Institute Finland (Luke), Espoo, Finland
- Ilona Mészáros
- 7Department of Botany, Faculty of Science and Technology, University of Debrecen, Debrecen, Hungary
- Juha M. Metsaranta
- 8Northern Forestry Centre, Canadian Forest Service, Natural Resources Canada, Edmonton, AB, Canada
- Walter Oberhuber
- 9Department of Botany, University of Innsbruck, Innsbruck, Austria
- Andreas Papadopoulos
- 0Department of Forestry and Natural Environment Management, Technological Educational Institute of Stereas Elladas, Karpenisi, Greece
- Any Mary Petritan
- Swiss Federal Institute for Forest, Snow and Landscape Research – WSL, Birmensdorf, Switzerland
- Any Mary Petritan
- 1National Institute for Research and Development in Forestry “Marin Dracea”, Voluntari, Romania
- Brigitte Rohner
- Swiss Federal Institute for Forest, Snow and Landscape Research – WSL, Birmensdorf, Switzerland
- Gabriel Sangüesa-Barreda
- 2Departamento de Ciencias Agroforestales, EiFAB, iuFOR – University of Valladolid, Soria, Spain
- Jeremy M. Smith
- 3Department of Geography, University of Colorado, Boulder, CO, United States
- Amanda B. Stan
- 4Department of Geography, Planning and Recreation, Northern Arizona University, Flagstaff, AZ, United States
- Dejan B. Stojanovic
- 5Institute of Lowland Forestry and Environment, University of Novi Sad, Novi Sad, Serbia
- Maria-Laura Suarez
- 6Grupo Ecología Forestal, CONICET – INTA, EEA Bariloche, Bariloche, Argentina
- Miroslav Svoboda
- 6Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Prague, Czechia
- Volodymyr Trotsiuk
- Swiss Federal Institute for Forest, Snow and Landscape Research – WSL, Birmensdorf, Switzerland
- Volodymyr Trotsiuk
- 6Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Prague, Czechia
- Volodymyr Trotsiuk
- 7Department of Environmental Systems Science, Institute of Agricultural Sciences, ETH Zürich, Zurich, Switzerland
- Ricardo Villalba
- 8Laboratorio de Dendrocronología e Historia Ambiental, Instituto Argentino de Nivología, Glaciología y Ciencias Ambientales, CCT CONICET Mendoza, Mendoza, Argentina
- Alana R. Westwood
- 9Boreal Avian Modelling Project, Department of Renewable Resources, University of Alberta, Edmonton, AB, Canada
- Peter H. Wyckoff
- 0Department of Biology, University of Minnesota, Morris, Morris, MN, United States
- Jordi Martínez-Vilalta
- CREAF, Cerdanyola del Vallès, Catalonia, Spain
- Jordi Martínez-Vilalta
- 1Departament de Biologia Animal, de Biologia Vegetal i d’Ecologia, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain
- DOI
- https://doi.org/10.3389/fpls.2018.01964
- Journal volume & issue
-
Vol. 9
Abstract
Tree mortality is a key driver of forest dynamics and its occurrence is projected to increase in the future due to climate change. Despite recent advances in our understanding of the physiological mechanisms leading to death, we still lack robust indicators of mortality risk that could be applied at the individual tree scale. Here, we build on a previous contribution exploring the differences in growth level between trees that died and survived a given mortality event to assess whether changes in temporal autocorrelation, variance, and synchrony in time-series of annual radial growth data can be used as early warning signals of mortality risk. Taking advantage of a unique global ring-width database of 3065 dead trees and 4389 living trees growing together at 198 sites (belonging to 36 gymnosperm and angiosperm species), we analyzed temporal changes in autocorrelation, variance, and synchrony before tree death (diachronic analysis), and also compared these metrics between trees that died and trees that survived a given mortality event (synchronic analysis). Changes in autocorrelation were a poor indicator of mortality risk. However, we found a gradual increase in inter-annual growth variability and a decrease in growth synchrony in the last ∼20 years before mortality of gymnosperms, irrespective of the cause of mortality. These changes could be associated with drought-induced alterations in carbon economy and allocation patterns. In angiosperms, we did not find any consistent changes in any metric. Such lack of any signal might be explained by the relatively high capacity of angiosperms to recover after a stress-induced growth decline. Our analysis provides a robust method for estimating early-warning signals of tree mortality based on annual growth data. In addition to the frequently reported decrease in growth rates, an increase in inter-annual growth variability and a decrease in growth synchrony may be powerful predictors of gymnosperm mortality risk, but not necessarily so for angiosperms.
Keywords