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Research Article

Forest and woodland replacement patterns following drought-related mortality

View ORCID ProfileEnric Batllori, View ORCID ProfileFrancisco Lloret, View ORCID ProfileTuomas Aakala, View ORCID ProfileWilliam R. L. Anderegg, View ORCID ProfileErmias Aynekulu, View ORCID ProfileDevin P. Bendixsen, Abdallah Bentouati, View ORCID ProfileChristof Bigler, C. John Burk, View ORCID ProfileJ. Julio Camarero, View ORCID ProfileMichele Colangelo, View ORCID ProfileJonathan D. Coop, Roderick Fensham, View ORCID ProfileM. Lisa Floyd, View ORCID ProfileLucía Galiano, View ORCID ProfileJoseph L. Ganey, View ORCID ProfilePatrick Gonzalez, View ORCID ProfileAnna L. Jacobsen, View ORCID ProfileJeffrey Michael Kane, View ORCID ProfileThomas Kitzberger, View ORCID ProfileJuan C. Linares, Suzanne B. Marchetti, View ORCID ProfileGeorge Matusick, Michael Michaelian, View ORCID ProfileRafael M. Navarro-Cerrillo, View ORCID ProfileRobert Brandon Pratt, View ORCID ProfileMiranda D. Redmond, View ORCID ProfileAndreas Rigling, View ORCID ProfileFrancesco Ripullone, View ORCID ProfileGabriel Sangüesa-Barreda, View ORCID ProfileYamila Sasal, Sandra Saura-Mas, View ORCID ProfileMaria Laura Suarez, View ORCID ProfileThomas T. Veblen, Albert Vilà-Cabrera, View ORCID ProfileCaroline Vincke, and View ORCID ProfileBen Zeeman
PNAS November 24, 2020 117 (47) 29720-29729; first published November 2, 2020; https://doi.org/10.1073/pnas.2002314117
Enric Batllori
aCentre de Recerca Ecològica i Aplicacions Forestals (CREAF), 08193 Cerdanyola del Vallès, Barcelona, Spain;
bUnitat de Botànica, Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Universitat de Barcelona, 08028 Barcelona, Spain;
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  • ORCID record for Enric Batllori
  • For correspondence: enric.batllori@gmail.com francisco.lloret@uab.cat
Francisco Lloret
aCentre de Recerca Ecològica i Aplicacions Forestals (CREAF), 08193 Cerdanyola del Vallès, Barcelona, Spain;
cUnitat d’Ecologia, Departament de Biologia Animal, Biologia Vegetal i Ecologia, Universitat Autònoma Barcelona, 08193 Barcelona, Spain;
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  • ORCID record for Francisco Lloret
  • For correspondence: enric.batllori@gmail.com francisco.lloret@uab.cat
Tuomas Aakala
dDepartment of Forest Sciences, University of Helsinki, FI-00014 Helsinki, Finland;
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  • ORCID record for Tuomas Aakala
William R. L. Anderegg
eSchool of Biological Sciences, University of Utah, Salt Lake City, UT 84112;
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  • ORCID record for William R. L. Anderegg
Ermias Aynekulu
fWorld Agroforestry Centre (ICRAF), Nairobi, 00100, Kenya;
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  • ORCID record for Ermias Aynekulu
Devin P. Bendixsen
gDepartment of Natural Resource Ecology and Management, Oklahoma State University, Stillwater, OK 74074;
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  • ORCID record for Devin P. Bendixsen
Abdallah Bentouati
hInstitut des Sciences Vétérinaires et des Sciences Agronomiques, Université El Hadj Lakhdar, 05000 Batna, Algérie;
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Christof Bigler
iForest Ecology, Department of Environmental Systems Science, ETH Zürich, CH-8092 Zürich, Switzerland;
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  • ORCID record for Christof Bigler
C. John Burk
jDepartment of Biological Sciences, Smith College, Northampton, MA 01066;
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J. Julio Camarero
kInstituto Pirenaico de Ecología (IPE-CSIC), Consejo Superior de Investigaciones Científicas, 50059 Zaragoza, Spain;
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  • ORCID record for J. Julio Camarero
Michele Colangelo
kInstituto Pirenaico de Ecología (IPE-CSIC), Consejo Superior de Investigaciones Científicas, 50059 Zaragoza, Spain;
lSchool of Agricultural, Forest, Food and Environmental Sciences, University of Basilicata, 85100 Potenza, Italy;
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  • ORCID record for Michele Colangelo
Jonathan D. Coop
mSchool of Environment and Sustainability, Western Colorado University, Gunnison, CO 81231;
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  • ORCID record for Jonathan D. Coop
Roderick Fensham
nQueensland Herbarium (DES), Toowong, QLD 4066, Australia;
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M. Lisa Floyd
oNatural History Institute, Prescott, AZ 86301;
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  • ORCID record for M. Lisa Floyd
Lucía Galiano
aCentre de Recerca Ecològica i Aplicacions Forestals (CREAF), 08193 Cerdanyola del Vallès, Barcelona, Spain;
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  • ORCID record for Lucía Galiano
Joseph L. Ganey
pRocky Mountain Research Station, United States Department of Agriculture (USDA) Forest Service, Flagstaff, AZ 86001;
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  • ORCID record for Joseph L. Ganey
Patrick Gonzalez
qDepartment of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720;
rInstitute for Parks, People, and Biodiversity, University of California, Berkeley, CA 94720;
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  • ORCID record for Patrick Gonzalez
Anna L. Jacobsen
sDepartment of Biology, California State University, Bakersfield, CA 93311;
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  • ORCID record for Anna L. Jacobsen
Jeffrey Michael Kane
tDepartment of Forestry and Wildland Resources, Humboldt State University, Arcata, CA 95521;
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  • ORCID record for Jeffrey Michael Kane
Thomas Kitzberger
uDepartamento de Ecología, Universidad Nacional del Comahue (UN Comahue), 8400 Bariloche, Río Negro, Argentina;
vLaboratorio Ecotono, Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), Consejo Nacional de Ciencia y Tecnología (CONICET)-UN Comahue, 8400 Bariloche, Río Negro, Argentina;
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  • ORCID record for Thomas Kitzberger
Juan C. Linares
wDepartamento Sistemas Físicos, Químicos y Naturales, Universidad Pablo de Olavide, 41013 Sevilla, Spain;
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  • ORCID record for Juan C. Linares
Suzanne B. Marchetti
xGunnison Service Center, USDA Forest Service, Gunnison, CO 81230;
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George Matusick
ySchool of Veterinary and Life Sciences, Murdoch University, Murdoch, WA 6150, Australia;
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  • ORCID record for George Matusick
Michael Michaelian
zNatural Resources Canada, Canadian Forest Service, Edmonton, AB T6H 3S5, Canada;
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Rafael M. Navarro-Cerrillo
aaDepartment of Forest Engineering, Laboratory of Dendrochronology, Silviculture and Global Change (DendrodatLab-ERSAF), University of Córdoba, 14071 Córdoba, Spain;
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  • ORCID record for Rafael M. Navarro-Cerrillo
Robert Brandon Pratt
sDepartment of Biology, California State University, Bakersfield, CA 93311;
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  • ORCID record for Robert Brandon Pratt
Miranda D. Redmond
bbDepartment of Forest and Rangeland Stewardship, Colorado State University, Fort Collins, CO 80523;
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  • ORCID record for Miranda D. Redmond
Andreas Rigling
ccSwiss Federal Institute for Forest, Snow and Landscape Research (WSL), CH-8903 Birmensdorf, Switzerland;
ddInstitute of Terrestrial Ecology, Department of Environmental Sciences, Swiss Federal Institute Technology, ETH Zürich, CH-8092 Zürich, Switzerland;
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  • ORCID record for Andreas Rigling
Francesco Ripullone
lSchool of Agricultural, Forest, Food and Environmental Sciences, University of Basilicata, 85100 Potenza, Italy;
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  • ORCID record for Francesco Ripullone
Gabriel Sangüesa-Barreda
eeDepartamento de Ciencias Agroforestales, Escuela de Ingeniería de Soria (EiFAB), Instituto Universitario de Investigación Gestión Forestal Sostenible (iuFOR), Universidad de Valladolid, 42004 Soria, Spain;
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  • ORCID record for Gabriel Sangüesa-Barreda
Yamila Sasal
vLaboratorio Ecotono, Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), Consejo Nacional de Ciencia y Tecnología (CONICET)-UN Comahue, 8400 Bariloche, Río Negro, Argentina;
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  • ORCID record for Yamila Sasal
Sandra Saura-Mas
aCentre de Recerca Ecològica i Aplicacions Forestals (CREAF), 08193 Cerdanyola del Vallès, Barcelona, Spain;
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Maria Laura Suarez
vLaboratorio Ecotono, Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), Consejo Nacional de Ciencia y Tecnología (CONICET)-UN Comahue, 8400 Bariloche, Río Negro, Argentina;
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  • ORCID record for Maria Laura Suarez
Thomas T. Veblen
ffDepartment of Geography, University of Colorado Boulder, Boulder, CO 80301;
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  • ORCID record for Thomas T. Veblen
Albert Vilà-Cabrera
ggBiological and Environmental Sciences, Faculty of Natural Sciences, University of Stirling, Stirling FK9 4LA, Scotland, United Kingdom;
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Caroline Vincke
hhFaculty of Bioscience Engineering, Université Catholique de Louvain,1348 Louvain-la-Neuve, Belgium;
iiEarth and Life Institute, Université Catholique de Louvain,1348 Louvain-la-Neuve, Belgium;
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  • ORCID record for Caroline Vincke
Ben Zeeman
jjDepartment of Ecology, Environment and Evolution, La Trobe University, Bundoora, VIC 3086, Australia
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  • ORCID record for Ben Zeeman
  1. Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved September 29, 2020 (received for review February 6, 2020)

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    Fig. 1.

    Location of the 131 field sites (Dataset S1) for which this research assessed tree species replacement patterns after mortality concomitant with drought. The analysis considers forest and woodland sites across Earth’s forested biomes, excluding species-rich tropical biomes (gray areas in the map). Global forest cover is based on Global Forest Watch (http://globalforestwatch.org). Biome classification (61): BorF, boreal forests/taiga; Des, deserts and xeric shrublands; MedF, Mediterranean forests, woodlands, and scrub; MnG, montane grasslands; TeBF, temperate broadleaf and mixed forests; TeCF, temperate conifer forests; TeG, temperate grasslands, savannas, and shrublands; TrG, tropical and subtropical grasslands, savannas, and shrublands. Photos exemplifying the four replacement processes considered are as follows. (A) Self-replacement; E. marginata, Northern Jarrah Forest, Australia (G.M., 2014). (B) Replacement by another tree species; Cedrus atlantica, Middle Atlas, Morocco (E.B., 2017). (C) Replacement by shrub species; Abies pinsapo, Sierra de las Nieves, Spain (E.B., 2017). (D) No replacement by woody vegetation; P. edulis, New Mexico, USA (F.L., 2012).

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    Fig. 2.

    Postdrought replacement patterns by vegetation replacement type (NR, no replacement by woody vegetation; Self, self-replacement; Shrub, replacement by shrublands; Tree, replacement by other tree species) and by tree genus. In A, each bar depicts the possible combinations of replacement by the different types (e.g., Self + Tree corresponds to sites in which self-replacement and replacement by other tree species are observed), whereas the proportion of each replacement type across all sites is depicted by the size of the gray dots. The overall proportion of sites showing a given replacement type is shown (Right). Colors depict major replacing categories in which trees (green), shrubs (violet), or lack of replacement by woody vegetation (brown) dominate. In B, outer-level colored bars show the dominant (predrought) genus and the most important replacing woody genera (NR, lack of replacement by woody vegetation; Shrub, replacement by shrub species; Tree_other, replacement by other scarcely represented tree genera: Acer, Arbutus, Austrocedrus, Betula, Carya, Dasyphyllum, Fagus, Ilex, Lomatia, Sorbus, Ulmus, Weinmannia). Inner links are directional, joinning predrought dominant genera (flat ends) and postdrought replacing genera (arrow ends). The inner links depict replacement proportions, so link width is proportional to the number of cases showing any given replacement pattern.

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    Fig. 3.

    Effects of drought conditions before (pre), during, and after (post) tree mortality on the reported replacement patterns. The panels show the results of a beta regression model where replacement pattern (included in the model as the community resemblance index) is the dependent variable and drought conditions are the explanatory variables. The CRI is a joint compositional and structural index that quantifies the vegetation-type change in initial tree forest composition. CRI = 0 reflects no change in composition or structure (complete self-replacement by neighboring canopy trees) and CRI = 1 corresponds to the maximum possible change (no woody replacement). (A) The model’s coefficient estimates. (B) Influence of the difference between postmortality and during-mortality drought conditions on CRI; larger values correspond thus to more favorable conditions after mortality. (C) Influence of the interaction between during-mortality drought and the difference between postmortality and during-mortality drought conditions on CRI. Model pseudo-R2 = 0.274.

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    Fig. 4.

    Postdrought replacement patterns in relation to management, management intensity, and biotic disturbances. The CRI is a joint compositional and structural index that quantifies the vegetation-type change in initial tree forest composition (Fig. 3). The symbols (Top Right) in each plot show significant differences among the different classes in each panel: +P < 0.05, ++P < 0.01.

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    Fig. 5.

    Community bioclimatic shift as a result of forest mortality associated with drought. (Left) Relative change within the environmental space defined by precipitation regime and aridity. Environmental axes 1 and 2 encompass 82.4% of the variability of individual variables (PCA-derived axes). Each arrow represents the bioclimatic shift for a given forest site computed as the difference between the bioclimatic centroids of the dominant (predrought) and the replacing woody species weighted by the relative abundance of each species at the site. Orange and blue arrows illustrate shifts toward more xeric and more mesic communities, respectively. (Right) From A to E are examples of bioclimatic niches of the predrought dominant (blue) and postdrought replacing (red) species. Solid lines show the abundance and distribution range of each species along environmental axis 1, whereas the dotted vertical lines correspond to the species’ bioclimatic optima (center of mass of the distribution).

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    Fig. 6.

    Contribution of (A) the bioclimatic characteristics of the study sites, (B) the dry bioclimatic edge of the replacing species (Rep_sp), (C) the range of the bioclimatic distribution of the replacing woody species, and (D) the successional index of the replacing species versus the dominant (predrought) species on the bioclimatic shift index. ICBS is the difference between the bioclimatic optima of the replacing woody species and the bioclimatic optima of the dominant (predrought) species along environmental axis 1 (Fig. 4). Positive ICBS values indicate shifts toward more xeric communities, whereas negative values indicate shifts toward more mesic communities. A shows a linear fit and B–D depict the component smooth functions of a generalized additive model fitted using the four variables depicted here; model R2 = 0.612, explained deviance = 67.2%; all variables are significant at P < 0.05.

Data supplements

  • Supporting Information

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    • Download Dataset_S01 (XLSX)
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    • Download Dataset_S03 (XLSX)
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Forest and woodland replacement patterns following drought-related mortality
Enric Batllori, Francisco Lloret, Tuomas Aakala, William R. L. Anderegg, Ermias Aynekulu, Devin P. Bendixsen, Abdallah Bentouati, Christof Bigler, C. John Burk, J. Julio Camarero, Michele Colangelo, Jonathan D. Coop, Roderick Fensham, M. Lisa Floyd, Lucía Galiano, Joseph L. Ganey, Patrick Gonzalez, Anna L. Jacobsen, Jeffrey Michael Kane, Thomas Kitzberger, Juan C. Linares, Suzanne B. Marchetti, George Matusick, Michael Michaelian, Rafael M. Navarro-Cerrillo, Robert Brandon Pratt, Miranda D. Redmond, Andreas Rigling, Francesco Ripullone, Gabriel Sangüesa-Barreda, Yamila Sasal, Sandra Saura-Mas, Maria Laura Suarez, Thomas T. Veblen, Albert Vilà-Cabrera, Caroline Vincke, Ben Zeeman
Proceedings of the National Academy of Sciences Nov 2020, 117 (47) 29720-29729; DOI: 10.1073/pnas.2002314117

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Forest and woodland replacement patterns following drought-related mortality
Enric Batllori, Francisco Lloret, Tuomas Aakala, William R. L. Anderegg, Ermias Aynekulu, Devin P. Bendixsen, Abdallah Bentouati, Christof Bigler, C. John Burk, J. Julio Camarero, Michele Colangelo, Jonathan D. Coop, Roderick Fensham, M. Lisa Floyd, Lucía Galiano, Joseph L. Ganey, Patrick Gonzalez, Anna L. Jacobsen, Jeffrey Michael Kane, Thomas Kitzberger, Juan C. Linares, Suzanne B. Marchetti, George Matusick, Michael Michaelian, Rafael M. Navarro-Cerrillo, Robert Brandon Pratt, Miranda D. Redmond, Andreas Rigling, Francesco Ripullone, Gabriel Sangüesa-Barreda, Yamila Sasal, Sandra Saura-Mas, Maria Laura Suarez, Thomas T. Veblen, Albert Vilà-Cabrera, Caroline Vincke, Ben Zeeman
Proceedings of the National Academy of Sciences Nov 2020, 117 (47) 29720-29729; DOI: 10.1073/pnas.2002314117
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    • Forest and Woodland Replacement Patterns
    • Vegetation Dynamics and Bioclimate
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