Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population

10.24072/pcjournal.60 - Peer Community Journal, Volume 1 (2021), article no. e55.

Get full text PDF Peer reviewed and recommended by PCI

Since several studies have been reporting an increase in the decline of forests, a major issue in ecology is to better understand and predict tree mortality. The interactions between the different factors and the physiological processes giving rise tree mortality, as well as the inter-individual variability in mortality risk, still need to be better assessed. This study investigates mortality in a rear-edge population of European beech (Fagus sylvatica L.) using a combination of statistical and process-based modelling approaches. Based on a survey of 4323 adult beeches since 2002 within a natural reserve, we first used statistical models to quantify the effects of competition, tree growth, size, defoliation and fungi presence on mortality. Secondly, we used an ecophysiological process-based model (PBM) to separate out the different mechanisms giving rise to temporal and inter-individual variations in mortality by simulating depletion of carbon stocks, loss of hydraulic conductance and damage due to late frosts in response to climate. The combination of all these simulated processes was associated with the temporal variations in the population mortality rate. The individual probability of mortality decreased with increasing mean growth, and increased with increasing crown defoliation, earliness of budburst, fungi presence and increasing competition, in the statistical model. Moreover, the interaction between tree size and defoliation was significant, indicating a stronger increase in mortality associated to defoliation in smaller than larger trees. Finally, the PBM predicted a higher conductance loss together with a higher level of carbon reserves for trees with earlier budburst, while the ability to defoliate the crown was found to limit the impact of hydraulic stress at the expense of the accumulation of carbon reserves. We discuss the convergences and divergences obtained between statistical and process-based approaches and we highlight the importance of combining them to characterize the different processes underlying mortality, and the factors modulating individual vulnerability to mortality.

Published online:
DOI: 10.24072/pcjournal.60
Petit-Cailleux, Cathleen 1; Davi, Hendrik 1; Lefèvre, François 1; Garrigue, Joseph 2; Magdalou, Jean-André 2; Hurson, Christophe 3, 2; Magnanou, Elodie 2, 4; Oddou-Muratorio, Sylvie 1

1 INRAE, URFM, Avignon, France
2 Réserve Naturelle Nationale de la Forêt de la Massane, France
3 Fédération des Réserves Naturelles Catalanes, Prades, France
4 Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, F-66650 Banyuls-sur-Mer, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Petit-Cailleux, Cathleen and Davi, Hendrik and Lef\`evre, Fran\c{c}ois and Garrigue, Joseph and Magdalou, Jean-Andr\'e and Hurson, Christophe and Magnanou, Elodie and Oddou-Muratorio, Sylvie},
     title = {Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population},
     journal = {Peer Community Journal},
     eid = {e55},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.60},
     url = {}
AU  - Petit-Cailleux, Cathleen
AU  - Davi, Hendrik
AU  - Lefèvre, François
AU  - Garrigue, Joseph
AU  - Magdalou, Jean-André
AU  - Hurson, Christophe
AU  - Magnanou, Elodie
AU  - Oddou-Muratorio, Sylvie
TI  - Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population
JO  - Peer Community Journal
PY  - 2021
DA  - 2021///
VL  - 1
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.60
ID  - 10_24072_pcjournal_60
ER  - 
%0 Journal Article
%A Petit-Cailleux, Cathleen
%A Davi, Hendrik
%A Lefèvre, François
%A Garrigue, Joseph
%A Magdalou, Jean-André
%A Hurson, Christophe
%A Magnanou, Elodie
%A Oddou-Muratorio, Sylvie
%T Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.60
%F 10_24072_pcjournal_60
Petit-Cailleux, Cathleen; Davi, Hendrik; Lefèvre, François; Garrigue, Joseph; Magdalou, Jean-André; Hurson, Christophe; Magnanou, Elodie; Oddou-Muratorio, Sylvie. Comparing statistical and mechanistic models to identify the drivers of mortality within a rear-edge beech population. Peer Community Journal, Volume 1 (2021), article  no. e55. doi : 10.24072/pcjournal.60.

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100070

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Adams, H. D.; Zeppel, M. J. B.; Anderegg, W. R. L.; Hartmann, H.; Landhäusser, S. M.; Tissue, D. T.; Huxman, T. E.; Hudson, P. J.; Franz, T. E.; Allen, C. D.; Anderegg, L. D. L.; Barron-Gafford, G. A.; Beerling, D. J.; Breshears, D. D.; Brodribb, T. J.; Bugmann, H.; Cobb, R. C.; Collins, A. D.; Dickman, L. T.; Duan, H.; Ewers, B. E.; Galiano, L.; Galvez, D. A.; Garcia-Forner, N.; Gaylord, M. L.; Germino, M. J.; Gessler, A.; Hacke, U. G.; Hakamada, R.; Hector, A.; Jenkins, M. W.; Kane, J. M.; Kolb, T. E.; Law, D. J.; Lewis, J. D.; Limousin, J.-M.; Love, D. M.; Macalady, A. K.; Martínez-Vilalta, J.; Mencuccini, M.; Mitchell, P. J.; Muss, J. D.; O’Brien, M. J.; O’Grady, A. P.; Pangle, R. E.; Pinkard, E. A.; Piper, F. I.; Plaut, J. A.; Pockman, W. T.; Quirk, J.; Reinhardt, K.; Ripullone, F.; Ryan, M. G.; Sala, A.; Sevanto, S.; Sperry, J. S.; Vargas, R.; Vennetier, M.; Way, D. A.; Xu, C.; Yepez, E. A.; McDowell, N. G. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality, Nature Ecology & Evolution, Volume 1 (2017) no. 9, pp. 1285-1291 | DOI

[2] Akaike, H. Factor Analysis and AIC, Springer Series in Statistics, Springer New York, New York, NY, 1987, pp. 371-386 | DOI

[3] Allen, C. D.; Macalady, A. K.; Chenchouni, H.; Bachelet, D.; McDowell, N.; Vennetier, M.; Kitzberger, T.; Rigling, A.; Breshears, D. D.; Hogg, E. (.; Gonzalez, P.; Fensham, R.; Zhang, Z.; Castro, J.; Demidova, N.; Lim, J.-H.; Allard, G.; Running, S. W.; Semerci, A.; Cobb, N. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests, Forest Ecology and Management, Volume 259 (2010) no. 4, pp. 660-684 | DOI

[4] Anderegg, W. R. L.; Berry, J. A.; Smith, D. D.; Sperry, J. S.; Anderegg, L. D. L.; Field, C. B. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off, Proceedings of the National Academy of Sciences, Volume 109 (2012) no. 1, pp. 233-237 | DOI

[5] Anderegg, W. R. L.; Hicke, J. A.; Fisher, R. A.; Allen, C. D.; Aukema, J.; Bentz, B.; Hood, S.; Lichstein, J. W.; Macalady, A. K.; McDowell, N.; Pan, Y.; Raffa, K.; Sala, A.; Shaw, J. D.; Stephenson, N. L.; Tague, C.; Zeppel, M. Tree mortality from drought, insects, and their interactions in a changing climate, New Phytologist, Volume 208 (2015) no. 3, pp. 674-683 | DOI

[6] Anderegg, W. R. L. Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation, New Phytologist, Volume 205 (2015) no. 3, pp. 1008-1014 | DOI

[7] Archambeau, J.; Ruiz-Benito, P.; Ratcliffe, S.; Fréjaville, T.; Changenet, A.; Muñoz Castañeda, J. M.; Lehtonen, A.; Dahlgren, J.; Zavala, M. A.; Benito Garzón, M. Similar patterns of background mortality across Europe are mostly driven by drought in European beech and a combination of drought and competition in Scots pine, Agricultural and Forest Meteorology, Volume 280 (2020) | DOI

[8] Arnold, T. W. Uninformative Parameters and Model Selection Using Akaike's Information Criterion, The Journal of Wildlife Management, Volume 74 (2010) no. 6, pp. 1175-1178 | DOI

[9] Augspurger, C. K. Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest, Functional Ecology, Volume 23 (2009) no. 6, pp. 1031-1039 | DOI

[10] Ball, J. T.; Woodrow, I. E.; Berry, J. A. A Model Predicting Stomatal Conductance and its Contribution to the Control of Photosynthesis under Different Environmental Conditions, Progress in Photosynthesis Research, Springer Netherlands, Dordrecht, 1987, pp. 221-224 | DOI

[11] Barnier, J.; Briatte, F.; Larmarange, J. Questionr: Functions to Make Surveys Processing Easier, (2018)

[12] Bartoń, K. MuMIn: Multi-Model Inference. R package version 1.43.17., (2020)

[13] Bauch, J. Characteristics and Response of Wood in Declining Trees from Forests Affected by Pollution, IAWA Journal, Volume 7 (1986) no. 4, pp. 269-276 | DOI

[14] Beguería, S.; Vicente-Serrano, S. M. SPEI: Calculation of the Standardised Precipitation-Evapotranspiration Index, (2017)

[15] Benito Garzón, M.; González Muñoz, N.; Wigneron, J.-P.; Moisy, C.; Fernández-Manjarrés, J.; Delzon, S. The legacy of water deficit on populations having experienced negative hydraulic safety margin, Global Ecology and Biogeography, Volume 27 (2018) no. 3, pp. 346-356 | DOI

[16] Berzaghi, F.; Wright, I. J.; Kramer, K.; Oddou-Muratorio, S.; Bohn, F. J.; Reyer, C. P.; Sabaté, S.; Sanders, T. G.; Hartig, F. Towards a New Generation of Trait-Flexible Vegetation Models, Trends in Ecology & Evolution, Volume 35 (2020) no. 3, pp. 191-205 | DOI

[17] Bigler, C.; Bugmann, H. Climate-induced shifts in leaf unfolding and frost risk of European trees and shrubs, Scientific Reports, Volume 8 (2018) no. 1 | DOI

[18] Brando, P. M.; Balch, J. K.; Nepstad, D. C.; Morton, D. C.; Putz, F. E.; Coe, M. T.; Silverio, D.; Macedo, M. N.; Davidson, E. A.; Nobrega, C. C.; Alencar, A.; Soares-Filho, B. S. Abrupt increases in Amazonian tree mortality due to drought-fire interactions, Proceedings of the National Academy of Sciences, Volume 111 (2014) no. 17, pp. 6347-6352 | DOI

[19] Bréda, N.; Huc, R.; Granier, A.; Dreyer, E. Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences, Annals of Forest Science, Volume 63 (2006) no. 6, pp. 625-644 | DOI

[20] Brier, G. W. Verification of forecasts expressed in terms of probability, Monthly Weather Review, Volume 78 (1950) no. 1, pp. 1-3 | DOI

[21] Cailleret, M.; Bircher, N.; Hartig, F.; Hülsmann, L.; Bugmann, H. Bayesian calibration of a growth‐dependent tree mortality model to simulate the dynamics of European temperate forests, Ecological Applications, Volume 30 (2019) no. 1 | DOI

[22] Cailleret, M.; Davi, H. Effects of climate on diameter growth of co-occurring Fagus sylvatica and Abies alba along an altitudinal gradient, Trees, Volume 25 (2011) no. 2, pp. 265-276 | DOI

[23] Cailleret, M.; Jansen, S.; Robert, E. M. R.; Desoto, L.; Aakala, T.; Antos, J. A.; Beikircher, B.; Bigler, C.; Bugmann, H.; Caccianiga, M.; Čada, V.; Camarero, J. J.; Cherubini, P.; Cochard, H.; Coyea, M. R.; Čufar, K.; Das, A. J.; Davi, H.; Delzon, S.; Dorman, M.; Gea‐Izquierdo, G.; Gillner, S.; Haavik, L. J.; Hartmann, H.; Hereş, A.; Hultine, K. R.; Janda, P.; Kane, J. M.; Kharuk, V. I.; Kitzberger, T.; Klein, T.; Kramer, K.; Lens, F.; Levanic, T.; Linares Calderon, J. C.; Lloret, F.; Lobo‐Do‐Vale, R.; Lombardi, F.; López Rodríguez, R.; Mäkinen, H.; Mayr, S.; Mészáros, I.; Metsaranta, J. M.; Minunno, F.; Oberhuber, W.; Papadopoulos, A.; Peltoniemi, M.; Petritan, A. M.; Rohner, B.; Sangüesa‐Barreda, G.; Sarris, D.; Smith, J. M.; Stan, A. B.; Sterck, F.; Stojanović, D. B.; Suarez, M. L.; Svoboda, M.; Tognetti, R.; Torres‐Ruiz, J. M.; Trotsiuk, V.; Villalba, R.; Vodde, F.; Westwood, A. R.; Wyckoff, P. H.; Zafirov, N.; Martínez‐Vilalta, J. A synthesis of radial growth patterns preceding tree mortality, Global Change Biology, Volume 23 (2017) no. 4, pp. 1675-1690 | DOI

[24] Campbell, G. S. A simple method for determining unsaturated conductivity from moisture retention data, Soil Science, Volume 117 (1974) no. 6, pp. 311-314 | DOI

[25] Carnicer, J.; Coll, M.; Ninyerola, M.; Pons, X.; Sanchez, G.; Penuelas, J. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 4, pp. 1474-1478 | DOI

[26] Cavin, L.; Jump, A. S. Highest drought sensitivity and lowest resistance to growth suppression are found in the range core of the tree Fagus sylvatica L. not the equatorial range edge, Global Change Biology, Volume 23 (2017) no. 1, pp. 362-379 | DOI

[27] Cheaib, A.; Badeau, V.; Boe, J.; Chuine, I.; Delire, C.; Dufrêne, E.; François, C.; Gritti, E. S.; Legay, M.; Pagé, C.; Thuiller, W.; Viovy, N.; Leadley, P. Climate change impacts on tree ranges: model intercomparison facilitates understanding and quantification of uncertainty, Ecology Letters, Volume 15 (2012) no. 6, pp. 533-544 | DOI

[28] Choat, B.; Brodribb, T. J.; Brodersen, C. R.; Duursma, R. A.; López, R.; Medlyn, B. E. Triggers of tree mortality under drought, Nature, Volume 558 (2018) no. 7711, pp. 531-539 | DOI

[29] Chuine, I.; Cour, P.; Rousseau, D. D. Selecting models to predict the timing of flowering of temperate trees: implications for tree phenology modelling, Plant, Cell and Environment, Volume 22 (1999) no. 1, pp. 1-13 | DOI

[30] Clark, J. S.; Bell, D. M.; Hersh, M. H.; Kwit, M. C.; Moran, E.; Salk, C.; Stine, A.; Valle, D.; Zhu, K. Individual-scale variation, species-scale differences: inference needed to understand diversity, Ecology Letters, Volume 14 (2011) no. 12, pp. 1273-1287 | DOI

[31] Collet, C.; Le Moguedec, G. Individual seedling mortality as a function of size, growth and competition in naturally regenerated beech seedlings, Forestry, Volume 80 (2007) no. 4, pp. 359-370 | DOI

[32] Cowan, I. R.; Farquhar, G. D. Stomatal function in relation to leaf metabolism and environment, Symposia of the Society for Experimental Biology, Volume 31 (1977), pp. 471-505

[33] Cribari-Neto, F.; Zeileis, A. Beta Regression inR, Journal of Statistical Software, Volume 34 (2010) no. 2, pp. 1-24 | DOI

[34] Davi, H.; Barbaroux, C.; Francois, C.; Dufrene, E. The fundamental role of reserves and hydraulic constraints in predicting LAI and carbon allocation in forests, Agricultural and Forest Meteorology, Volume 149 (2009) no. 2, pp. 349-361 | DOI

[35] Davi, H.; Cailleret, M. Assessing drought-driven mortality trees with physiological process-based models, Agricultural and Forest Meteorology, Volume 232 (2017), pp. 279-290 | DOI

[36] Davi, H.; Dufrêne, E.; Granier, A.; Le Dantec, V.; Barbaroux, C.; François, C.; Bréda, N. Modelling carbon and water cycles in a beech forest, Ecological Modelling, Volume 185 (2005) no. 2-4, pp. 387-405 | DOI

[37] De Cáceres, M.; Martin-StPaul, N.; Turco, M.; Cabon, A.; Granda, V. Estimating daily meteorological data and downscaling climate models over landscapes, Environmental Modelling & Software, Volume 108 (2018), pp. 186-196 | DOI

[38] De Vries, F.; Brunsting, A.; Van Laar, H. Products, requirements and efficiency of biosynthesis a quantitative approach, Journal of Theoretical Biology, Volume 45 (1974) no. 2, pp. 339-377 | DOI

[39] Dittmar, C.; Zech, W.; Elling, W. Growth variations of Common beech (Fagus sylvatica L.) under different climatic and environmental conditions in Europe—a dendroecological study, Forest Ecology and Management, Volume 173 (2003) no. 1-3, pp. 63-78 | DOI

[40] Dobbertin, M.; Brang, P. Crown defoliation improves tree mortality models, Forest Ecology and Management, Volume 141 (2001) no. 3, pp. 271-284 | DOI

[41] Dufrêne, E.; Davi, H.; François, C.; Maire, G. l.; Dantec, V. L.; Granier, A. Modelling carbon and water cycles in a beech forest, Ecological Modelling, Volume 185 (2005) no. 2-4, pp. 407-436 | DOI

[42] Durand-Gillmann, M.; Cailleret, M.; Boivin, T.; Nageleisen, L.-M.; Davi, H. Individual vulnerability factors of Silver fir (Abies alba Mill.) to parasitism by two contrasting biotic agents: mistletoe (Viscum album L. ssp. abietis) and bark beetles (Coleoptera: Curculionidae: Scolytinae) during a decline process, Annals of Forest Science, Volume 71 (2012) no. 6, pp. 659-673 | DOI

[43] Farquhar, G. D.; von Caemmerer, S.; Berry, J. A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species, Planta, Volume 149 (1980) no. 1, pp. 78-90 | DOI

[44] Feng, X.; Ackerly, D. D.; Dawson, T. E.; Manzoni, S.; Skelton, R. P.; Vico, G.; Thompson, S. E. The ecohydrological context of drought and classification of plant responses, Ecology Letters, Volume 21 (2018) no. 11, pp. 1723-1736 | DOI

[45] Gao, S.; Liu, R.; Zhou, T.; Fang, W.; Yi, C.; Lu, R.; Zhao, X.; Luo, H. Dynamic responses of tree‐ring growth to multiple dimensions of drought, Global Change Biology, Volume 24 (2018) no. 11, pp. 5380-5390 | DOI

[46] García-Plazaola, J. I.; Esteban, R.; Hormaetxe, K.; Fernández-Marín, B.; Becerril, J. M. Photoprotective responses of Mediterranean and Atlantic trees to the extreme heat-wave of summer 2003 in Southwestern Europe, Trees, Volume 22 (2008) no. 3, pp. 385-392 | DOI

[47] Gauzere, J.; Delzon, S.; Davi, H.; Bonhomme, M.; Garcia de Cortazar-Atauri, I.; Chuine, I. Integrating interactive effects of chilling and photoperiod in phenological process-based models. A case study with two European tree species: Fagus sylvatica and Quercus petraea, Agricultural and Forest Meteorology, Volume 244-245 (2017), pp. 9-20 | DOI

[48] Gillner, S.; Rüger, N.; Roloff, A.; Berger, U. Low relative growth rates predict future mortality of common beech (Fagus sylvatica L.), Forest Ecology and Management, Volume 302 (2013), pp. 372-378 | DOI

[49] Granier, A.; Biron, P.; Lemoine, D. Water balance, transpiration and canopy conductance in two beech stands, Agricultural and Forest Meteorology, Volume 100 (2000) no. 4, pp. 291-308 | DOI

[50] Greenwood, S.; Ruiz-Benito, P.; Martínez-Vilalta, J.; Lloret, F.; Kitzberger, T.; Allen, C. D.; Fensham, R.; Laughlin, D. C.; Kattge, J.; Bönisch, G.; Kraft, N. J. B.; Jump, A. S. Tree mortality across biomes is promoted by drought intensity, lower wood density and higher specific leaf area, Ecology Letters, Volume 20 (2017) no. 4, pp. 539-553 | DOI

[51] Hawkes, C. Woody plant mortality algorithms: description, problems and progress, Ecological Modelling, Volume 126 (2000) no. 2-3, pp. 225-248 | DOI

[52] Heinze, G.; Wallisch, C.; Dunkler, D. Variable selection - A review and recommendations for the practicing statistician, Biometrical Journal, Volume 60 (2018) no. 3, pp. 431-449 | DOI

[53] Hesse, B. D.; Goisser, M.; Hartmann, H.; Grams, T. E. E. Repeated summer drought delays sugar export from the leaf and impairs phloem transport in mature beech, Tree Physiology, Volume 39 (2018) no. 2, pp. 192-200 | DOI

[54] Hijmans, R. J.; Phillips, S.; Leathwick, J.; Elith, J.; Hijmans, M. R. J. Package ‘dismo’, Circles, Volume 9 (2017) no. 1, pp. 1-68

[55] Hosmer, D. W.; Lemeshow, S. Applied Logistic Regression, John Wiley & Sons, Inc., Hoboken, NJ, USA, 2000 | DOI

[56] Hülsmann, L.; Bugmann, H. K. M.; Commarmot, B.; Meyer, P.; Zimmermann, S.; Brang, P. Does one model fit all? Patterns of beech mortality in natural forests of three European regions, Ecological Applications, Volume 26 (2016) no. 8, pp. 2465-2479 | DOI

[57] Hülsmann, L.; Bugmann, H.; Brang, P. How to predict tree death from inventory data — lessons from a systematic assessment of European tree mortality models, Canadian Journal of Forest Research, Volume 47 (2017) no. 7, pp. 890-900 | DOI

[58] Hülsmann, L.; Bugmann, H.; Cailleret, M.; Brang, P. How to kill a tree: empirical mortality models for 18 species and their performance in a dynamic forest model, Ecological Applications, Volume 28 (2018) no. 2, pp. 522-540 | DOI

[59] Jump, A. S.; Hunt, J. M.; Penuelas, J. Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica, Global Change Biology, Volume 12 (2006) no. 11, pp. 2163-2174 | DOI

[60] Kneeshaw, D. D.; Kobe, R. K.; Coates, K. D.; Messier, C. Sapling size influences shade tolerance ranking among southern boreal tree species, Journal of Ecology, Volume 94 (2006) no. 2, pp. 471-480 | DOI

[61] Knutzen, F.; Dulamsuren, C.; Meier, I. C.; Leuschner, C. Recent Climate Warming-Related Growth Decline Impairs European Beech in the Center of Its Distribution Range, Ecosystems, Volume 20 (2017) no. 8, pp. 1494-1511 | DOI

[62] Kramer, K.; Degen, B.; Buschbom, J.; Hickler, T.; Thuiller, W.; Sykes, M. T.; de Winter, W. Modelling exploration of the future of European beech (Fagus sylvatica L.) under climate change—Range, abundance, genetic diversity and adaptive response, Forest Ecology and Management, Volume 259 (2010) no. 11, pp. 2213-2222 | DOI

[63] Lebourgeois, F.; Bréda, N.; Ulrich, E.; Granier, A. Climate-tree-growth relationships of European beech (Fagus sylvatica L.) in the French Permanent Plot Network (RENECOFOR), Trees, Volume 19 (2005) no. 4, pp. 385-401 | DOI

[64] Lederer, D. J.; Bell, S. C.; Branson, R. D.; Chalmers, J. D.; Marshall, R.; Maslove, D. M.; Ost, D. E.; Punjabi, N. M.; Schatz, M.; Smyth, A. R.; Stewart, P. W.; Suissa, S.; Adjei, A. A.; Akdis, C. A.; Azoulay, É.; Bakker, J.; Ballas, Z. K.; Bardin, P. G.; Barreiro, E.; Bellomo, R.; Bernstein, J. A.; Brusasco, V.; Buchman, T. G.; Chokroverty, S.; Collop, N. A.; Crapo, J. D.; Fitzgerald, D. A.; Hale, L.; Hart, N.; Herth, F. J.; Iwashyna, T. J.; Jenkins, G.; Kolb, M.; Marks, G. B.; Mazzone, P.; Moorman, J. R.; Murphy, T. M.; Noah, T. L.; Reynolds, P.; Riemann, D.; Russell, R. E.; Sheikh, A.; Sotgiu, G.; Swenson, E. R.; Szczesniak, R.; Szymusiak, R.; Teboul, J.-L.; Vincent, J.-L. Control of Confounding and Reporting of Results in Causal Inference Studies. Guidance for Authors from Editors of Respiratory, Sleep, and Critical Care Journals, Annals of the American Thoracic Society, Volume 16 (2019) no. 1, pp. 22-28 | DOI

[65] Lenz, A.; Hoch, G.; Vitasse, Y.; Körner, C. European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients, New Phytologist, Volume 200 (2013) no. 4, pp. 1166-1175 | DOI

[66] Lines, E. R.; Coomes, D. A.; Purves, D. W. Influences of Forest Structure, Climate and Species Composition on Tree Mortality across the Eastern US, PLoS ONE, Volume 5 (2010) no. 10 | DOI

[67] Long JA, (2020)

[68] Lorenz, M. a. B. G., (2012)

[69] Loustau, D.; Granier, A.; El Hadj Moussa, F.; Sartore, M.; Guedon, M. Evolution saisonnière du flux de sève dans un peuplement de pins maritimes, Annales des Sciences Forestières, Volume 47 (1990) no. 6, pp. 599-618 | DOI

[70] Maraun, M.; Salamon, J.-A.; Schneider, K.; Schaefer, M.; Scheu, S. Oribatid mite and collembolan diversity, density and community structure in a moder beech forest (Fagus sylvatica): effects of mechanical perturbations, Soil Biology and Biochemistry, Volume 35 (2003) no. 10, pp. 1387-1394 | DOI

[71] Martin, G.; Ek, A. R. A Comparison of Competition Measures and Growth Models for Predicting Plantation Red Pine Diameter and Height Growth, Forest Science, Volume 30 (1984) no. 3, pp. 731-743 | DOI

[72] McDowell, N. G.; Beerling, D. J.; Breshears, D. D.; Fisher, R. A.; Raffa, K. F.; Stitt, M. The interdependence of mechanisms underlying climate-driven vegetation mortality, Trends in Ecology & Evolution, Volume 26 (2011) no. 10, pp. 523-532 | DOI

[73] McDowell, N. G.; Fisher, R. A.; Xu, C.; Domec, J. C.; Hölttä, T.; Mackay, D. S.; Sperry, J. S.; Boutz, A.; Dickman, L.; Gehres, N.; Limousin, J. M.; Macalady, A.; Martínez‐Vilalta, J.; Mencuccini, M.; Plaut, J. A.; Ogée, J.; Pangle, R. E.; Rasse, D. P.; Ryan, M. G.; Sevanto, S.; Waring, R. H.; Williams, A. P.; Yepez, E. A.; Pockman, W. T. Evaluating theories of drought‐induced vegetation mortality using a multimodel–experiment framework, New Phytologist, Volume 200 (2013) no. 2, pp. 304-321 | DOI

[74] Meir, P.; Mencuccini, M.; Dewar, R. C. Drought‐related tree mortality: addressing the gaps in understanding and prediction, New Phytologist, Volume 207 (2015) no. 1, pp. 28-33 | DOI

[75] Menzel, A.; Helm, R.; Zang, C. Patterns of late spring frost leaf damage and recovery in a European beech (Fagus sylvatica L.) stand in south-eastern Germany based on repeated digital photographs, Frontiers in Plant Science, Volume 6 (2015) | DOI

[76] Monserud, R. A. Simulation of forest tree mortality, Forest Science, Volume 22 (1976) no. 4, pp. 438-444 | DOI

[77] Monteith, J. L. Evaporation and environment. The state and movement of water in living organisms, Symposium of the Society of Experimental Biology, Volume 19 (1965), pp. 205-234

[78] Mueller, R. C.; Scudder, C. M.; Porter, M. E.; Talbot Trotter, R.; Gehring, C. A.; Whitham, T. G. Differential tree mortality in response to severe drought: evidence for long-term vegetation shifts, Journal of Ecology, Volume 93 (2005) no. 6, pp. 1085-1093 | DOI

[79] Niinemets, Ü. Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: Past stress history, stress interactions, tolerance and acclimation, Forest Ecology and Management, Volume 260 (2010) no. 10, pp. 1623-1639 | DOI

[80] Nourtier, M.; Chanzy, A.; Cailleret, M.; Yingge, X.; Huc, R.; Davi, H. Transpiration of silver Fir (Abies alba mill.) during and after drought in relation to soil properties in a Mediterranean mountain area, Annals of Forest Science, Volume 71 (2012) no. 6, pp. 683-695 | DOI

[81] O'Brien, M. J.; Engelbrecht, B. M. J.; Joswig, J.; Pereyra, G.; Schuldt, B.; Jansen, S.; Kattge, J.; Landhäusser, S. M.; Levick, S. R.; Preisler, Y.; Väänänen, P.; Macinnis-Ng, C. A synthesis of tree functional traits related to drought-induced mortality in forests across climatic zones, Journal of Applied Ecology, Volume 54 (2017) no. 6, pp. 1669-1686 | DOI

[82] O’Brien, M. J.; Leuzinger, S.; Philipson, C. D.; Tay, J.; Hector, A. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels, Nature Climate Change, Volume 4 (2014) no. 8, pp. 710-714 | DOI

[83] Pammenter, N. W.; Van der Willigen, C. A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation, Tree Physiology, Volume 18 (1998) no. 8-9, pp. 589-593 | DOI

[84] Peñuelas, J.; Boada, M. A global change-induced biome shift in the Montseny mountains (NE Spain), Global Change Biology, Volume 9 (2003) no. 2, pp. 131-140 | DOI

[85] Percie du Sert, T. Relations Entre La Phenologie et La Morphologie Du Hêtre Dans Le Massif Des Albères, Réserve Naturelle de La Massane, Travaux, Volume 12 (1982), pp. 1-73

[86] Pretzsch, H. Growth Trends of Forests in Southern Germany, Growth Trends in European Forests, Springer Berlin Heidelberg, Berlin, Heidelberg, 1996, pp. 107-131 | DOI

[87] Robson, T. M.; Rasztovits, E.; Aphalo, P. J.; Alia, R.; Aranda, I. Flushing phenology and fitness of European beech (Fagus sylvatica L.) provenances from a trial in La Rioja, Spain, segregate according to their climate of origin, Agricultural and Forest Meteorology, Volume 180 (2013), pp. 76-85 | DOI

[88] Ryan, M. G. Effects of Climate Change on Plant Respiration, Ecological Applications, Volume 1 (1991) no. 2, pp. 157-167 | DOI

[89] Sala, A.; Tenhunen, J. Simulations of canopy net photosynthesis and transpiration in Quercus ilex L. under the influence of seasonal drought, Agricultural and Forest Meteorology, Volume 78 (1996) no. 3-4, pp. 203-222 | DOI

[90] Schielzeth, H. Simple means to improve the interpretability of regression coefficients, Methods in Ecology and Evolution, Volume 1 (2010) no. 2, pp. 103-113 | DOI

[91] Seidl, R.; Fernandes, P. M.; Fonseca, T. F.; Gillet, F.; Jönsson, A. M.; Merganičová, K.; Netherer, S.; Arpaci, A.; Bontemps, J.-D.; Bugmann, H.; González-Olabarria, J. R.; Lasch, P.; Meredieu, C.; Moreira, F.; Schelhaas, M.-J.; Mohren, F. Modelling natural disturbances in forest ecosystems: a review, Ecological Modelling, Volume 222 (2011) no. 4, pp. 903-924 | DOI

[92] Senf, C.; Pflugmacher, D.; Zhiqiang, Y.; Sebald, J.; Knorn, J.; Neumann, M.; Hostert, P.; Seidl, R. Canopy mortality has doubled in Europe’s temperate forests over the last three decades, Nature Communications, Volume 9 (2018) no. 1 | DOI

[93] Sevanto, S.; McDowell, N. G.; Dickman, L. T.; Pangle, R.; Pockman, W. T. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses, Plant, Cell & Environment, Volume 37 (2013) no. 1, pp. 153-161 | DOI

[94] Stadt, K. J.; Huston, C.; Coates, K. D.; Feng, Z.; Dale, M. R.; Lieffers, V. J. Evaluation of competition and light estimation indices for predicting diameter growth in mature boreal mixed forests, Annals of Forest Science, Volume 64 (2007) no. 5, pp. 477-490 | DOI

[95] Thuiller, W.; Lavorel, S.; Araujo, M. B.; Sykes, M. T.; Prentice, I. C. Climate change threats to plant diversity in Europe, Proceedings of the National Academy of Sciences, Volume 102 (2005) no. 23, pp. 8245-8250 | DOI

[96] Tyree, M. T.; Sperry, J. S. Vulnerability of Xylem to Cavitation and Embolism, Annual Review of Plant Physiology and Plant Molecular Biology, Volume 40 (1989) no. 1, pp. 19-36 | DOI

[97] van Mantgem, P. J.; Stephenson, N. L.; Byrne, J. C.; Daniels, L. D.; Franklin, J. F.; Fulé, P. Z.; Harmon, M. E.; Larson, A. J.; Smith, J. M.; Taylor, A. H.; Veblen, T. T. Widespread Increase of Tree Mortality Rates in the Western United States, Science, Volume 323 (2009) no. 5913, pp. 521-524 | DOI

[98] Vanoni, M.; Bugmann, H.; Nötzli, M.; Bigler, C. Drought and frost contribute to abrupt growth decreases before tree mortality in nine temperate tree species, Forest Ecology and Management, Volume 382 (2016), pp. 51-63 | DOI

[99] Vidal, J.-P.; Martin, E.; Franchistéguy, L.; Baillon, M.; Soubeyroux, J.-M. A 50-year high-resolution atmospheric reanalysis over France with the Safran system, International Journal of Climatology, Volume 30 (2009) no. 11, pp. 1627-1644 | DOI

[100] Vitasse, Y.; Delzon, S.; Dufrêne, E.; Pontailler, J.-Y.; Louvet, J.-M.; Kremer, A.; Michalet, R. Leaf phenology sensitivity to temperature in European trees: Do within-species populations exhibit similar responses?, Agricultural and Forest Meteorology, Volume 149 (2009) no. 5, pp. 735-744 | DOI

Cited by Sources: