Abstract
Understanding which variables affect forest resilience to extreme drought is key to predict future dynamics under ongoing climate change. In this study, we analyzed how tree resistance, recovery and resilience to drought have changed along three consecutive droughts and how they were affected by species, tree size, plot basal area (as a proxy for competition) and climate. We focused on the three most abundant pine species in the northeast Iberian Peninsula: Pinus halepensis, P. nigra and P. sylvestris during the three most extreme droughts recorded in the period 1951–2010 (occurred in 1986, 1994, and 2005–2006). We cored trees from permanent sample plots and used dendrochronological techniques to estimate resistance (ability to maintain growth level during drought), recovery (growth increase after drought) and resilience (capacity to recover pre-drought growth levels) in terms of tree stem basal area increment. Mixed-effects models were used to determine which tree- and plot-level variables were the main determinants of resistance, recovery and resilience, and to test for differences among the studied droughts. Larger trees were significantly less resistant and resilient. Plot basal area effects were only observed for resilience, with a negative impact only during the last drought. Resistance, recovery and resilience differed across the studied drought events, so that the studied populations became less resistant, less resilient and recovered worse during the last two droughts. This pattern suggests an increased vulnerability to drought after successive drought episodes.
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References
Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci 95:14839–14842. https://doi.org/10.1073/pnas.95.25.14839
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manege 259:660–684. https://doi.org/10.1016/j.foreco.2009.09.001
Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6(8):129. https://doi.org/10.1890/es15-00203.1
Anderegg WRL, Plavcocá L, Anderegg LDL, Hacke U, Berry JA, Field CB (2013) Drought’s legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Glob Change Biol 19:1188–1196. https://doi.org/10.1111/gcb.12100
Anderegg WRL, Schwalm C, Biondi F, Camarero JJ, Koch G, Litvak M, Ogle K, Shaw JD, Shevliakova E, Williams AP, Wolf A, Ziaco E, Pacala S (2015) Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349:528–531. https://doi.org/10.1126/science.aab1833
Aussenac G (2000) Interactions between forest stands and microclimate: ecophysiological aspects and consequences for silviculture. Ann For Sci 57:287–301. https://doi.org/10.1051/forest:2000119
Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ (2015) Larger trees suffer most during drought in forests worldwide. Nat Plants 1:1–5. https://doi.org/10.1038/nplants.2015.139
Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice GR, Romme WH, Kastens JD, Floyd ML, Belnap J, Anderson JJ, Myers OB, Meyer CW (2005) Regional vegetation die-off in response to global-change-type drought. Proc Natl Acad Sci 102:15144–15148. https://doi.org/10.1073/pnas.0505734102
Cailleret M, Jansen S, Robert EMR, Desoto L, Aakala T, Antos JA, Beikircher B, Bigler C, Bugmann H, Caccianga M, Cada V, Camarero JJ, Cherubini P, Cochard H, Coyea MR, Cufar K, Das AJ, Davi H, Delzon S, Dorman M, Gea-Izquierdo G, Gillner S, Haavik LJ, Hartmann H, Heres AM, Hultine KR, Janda P, Kane JM, Kharuk VI, Kitzberger T, Klein T, Kramer K, Lens F, Levanic T, Linares JC, Lloret F, Lobo-Do-Vale R, Lombardi F, López-Rodriguéz R, Mäkinen H, Mayr S, Mészáros I, Metsaranta JM, Minunno F, Oberhuber W, Papadopoulus A, Peltoniemi M, Petritan AM, Rohenr B, Sangüesa-Barreda G, Sarris D, Smith JM, Stan AB, Sterck F, Stajanovic DB, Suarez ML, Svoboda M, Tognetti R, Torres-Ruiz JM, Trotsiuk V, Villalba R, Vodde F, Westwood AR, Wyckoff PH, Zafirov N, Martínez-Vilalta J (2017) A synthesis of radial growth patterns preceding tree motality. Glob Change Biol 23:1675–1690. https://doi.org/10.1111/gcb.13535
Camarero JJ, Manzanedo RD, Sanchez-Salguero R, Navarro-Cerrillo M (2013) Growth response to climate and drought change along an aridity gradient in the southernmost Pinus nigra relict forests. Ann For Sci 70:769–780. https://doi.org/10.1007/s13595-013-0321-9
Chaparro D, Vayreda J, Vall-Llosera M, Banqué M, Piles M, Campos A, Martínez-Vilalta J (2016) The role of climatic anomalies and soil moisture in the decline of drought-prone forests. J of Sel Top in Appl Earth Obs Remote Sens 10:503–514. https://doi.org/10.1109/jstars.2016.2585505
Chen PY, Welsh C, Hamann A (2010) Geographic variation in growth response of Douglas-fir to interannual climate variability and projected climate change. Glob Change Biol 16:3374–3385. https://doi.org/10.1111/j.1365-2486.20
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755. https://doi.org/10.1038/nature11688
Coll JR, Jones PD, Aguilar E (2015) Expected changes in mean seasonal precipitation and temperature across the Iberian Peninsula for the 21st century. Idójárás 119(1):1–22
Cybis Elektronik (2010) CDendro and CooRecorder, http://www.cybis.se/forfun/dendro/index.htm
Delucia EH, Maherali H, Carey EV (2000) Climate-driven changes in biomass allocation in pines. Glob Change Biol 6:587–593. https://doi.org/10.1046/j.1365-2486.2000.00338.x
Dorman M, Svoray T, Perevolotsky A, Sarris D (2013) Forest performance during two consecutive drought periods: diverging long-term trends and short-term responses along a climatic gradient. For Ecol Manege 310:1–9. https://doi.org/10.1016/j.foreco.2013.08.009
Dorman M, Perevolotsky A, Sarris D (2015) The effect of rainfall and competition intensity on forest response to drought: lessons learned from a dry extreme. Oecologia 177:1025–1038. https://doi.org/10.1007/s00442-015-3229-2
Floyd ML, Clifford M, Cobb NS, Hanna D, Delph R, Ford P, Turner D (2009) Relationship of stand characteristics to drought-induced mortality in three southwestern piñon—juniper woodlands. Ecol Appl 19:1223–1230. https://doi.org/10.1890/08-1265.1
Fritts HC (1976) Tree rings and climate. Academic Press, London
Galiano L, Martínez-Vilalta J, Lloret F (2010) Drought-induced multifactor decline of scots pine in the pyrenees and potential vegetation change by the expansion of co-occurring oak species. Ecosystems 13:978–991. https://doi.org/10.1007/s10021-010-9368-8
Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol 190:750–759. https://doi.org/10.1111/j.1469-8137.20
Gazol A, Camarero JJ, Anderegg WRL, Vicente Serrano SM (2016) Impacts of droughts on the growth resilience of Northern Hemisphere forests. Glob Ecol Biogeogr 26:166–176. https://doi.org/10.1111/geb.12526
Greenwood DL, Weisberg PJ (2008) Density-dependent tree mortality in pinyon-juniper woodlands. For Ecol Manage 255(7):2129–2137. https://doi.org/10.1016/j.foreco.2007.12.048
Hargreaves GH, Samani ZA (1982) Estimating potential evapotranspiration. J Irrig Drain Div ASCE 108:225–230
Hereş AM, Martínez-Vilalta J, López BC (2012) Growth patterns in relation to drought-induced mortality at two Scots pine (Pinus sylvestris L.) sites in NE Iberian Peninsula. Trees Struct Funct 26:621–630. https://doi.org/10.1007/s00468-011-0628-9
Intergovernmental Panel on Climate Change (IPCC) (2013) Climate change 2013: the physical science basis: contribution of working group I to the fifth assessment report of the IPCC. Cambridge University Press, Cambridge
Lebourgeois F, Rathgeber CBK, Ulrich E (2010) Sensitivity of French temperate coniferous forests to climate variability and extreme events (Abies alba, Picea abies and Pinus sylvestris). J Veg Sci 21:364–376. https://doi.org/10.1111/j.1654-1103.2009.01148.x
Lenth RV (2016) Least-squares means: the R Package Lsmeans. J Stat Soft 69(1):1–33. https://doi.org/10.18637/jss.v069.i01
Levesque M, Rigling A, Bugmann H, Weber P, Brang P (2014) Growth response of five co-occurring conifers to drought across a wide climatic gradient in Central Europe. Agric For Meteorol 197:1–12. https://doi.org/10.1016/j.agrformet.2014.06.001
Linares JC, Camarero JJ, Carreira JA (2010) Competition modulates the adaptation capacity of forests to climatic stress: Insights from recent growth decline and death in relict stands of the Mediterranean fir Abies pinsapo. J Ecol 98:592–603. https://doi.org/10.1111/j.1365-2745.20
Lloret F, Keeling EG, Sala A (2011) Components of tree resilience: effects of successive low-growth episodes in old ponderosa pine forests. Oikos 120:1909–1920. https://doi.org/10.1111/j.1600-0706.2011.19372.x
Lloret F, Escudero A, Iriondo JM, Martínez-Vilalta J, Valladares F (2012) Extreme climatic events and vegetation: the role of stabilizing processes. Glob Change Biol 18:797–805. https://doi.org/10.1111/j.1365-2486.2011.02624.x
Martínez-Vilalta J, Lloret F (2016) Drought-induced vegetation shifts in terrestrial ecosystems: the key role of regeneration dynamics. Glob Planet Change 144:94–108. https://doi.org/10.1016/j.gloplacha.2016.07.009
Martínez-Vilalta J, Piñol J (2002) Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manege 161:247–256. https://doi.org/10.1016/s0378-1127(01)00495-9
Martinez-Vilalta J, Cochard H, Mencuccini M, Streck F, Herrero A, Korhonen JFJ, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen Zweifel R (2009) Hydraulic adjustment of Scots pine across Europe. New Phytol 184:353–364. https://doi.org/10.1111/j.1469-8137.2009.02954.x
Martínez-Vilalta J, Lopez BC, Adell N, Badiella L, Ninyerola M (2008) Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions. Glob Change Biol 14:2868–2881. https://doi.org/10.1111/j.13652486.2008.01685.x
Martínez-Vilalta J, López BC, Loepfe L, Lloret F (2012) Stand- and tree-level determinants of the drought response of Scots pine radial growth. Oecologia 168:877–888. https://doi.org/10.1007/s00442-011-2132-8
Matusick G, Ruthorf KX, Fontaine JB, Hardy GESJ (2016) Eucalyptus forest shows low structural resistance and resilience to climate change-type drought. J Veg Sci 27:493–503. https://doi.org/10.1111/jvs.12378
McIntyre PJ, Thorne JH, Dolanc CR, Flint AL, Flint LE, Kelly M, Ackerly DD (2015) Twentieth-century shifts in forest structure in California: denser forests, smaller trees, and increased dominance of oaks. Proc Natl Acad Sci USA 112(5):1458–1463. https://doi.org/10.1073/pnas.1410186112
McKee TB, Doesken NJ, Kleist J (1993) The relationship of drought frequency and duration to time scales. Preprints, Eight Conference on Applied Climatology. Anaheim, CA. American Meteor Society, pp 179–184
Mencuccini M, Martínez-Vilalta J, Vanderklein D, Hamid HA, Korakaki E, Lee S, Michiels B (2005) Size-mediated ageing reduces vigour in trees. Ecol Lett 8:1183–1190. https://doi.org/10.1111/j.1461-0248.2005.00819.x
Merlin M, Perot T, Perret S, Korboulewsky N, Vallet P (2015) Effects of stand composition and tree size on resistance and resilience to drought in sessile oak and Scots pine. For Ecol Manage 339:22–33. https://doi.org/10.1016/j.foreco.2014.11.032
Mueller RC, Scudder CM, Porter ME, Trotter T, Gehring CC, Whitman TG (2005) Differential tree mortality in response to severe drought: evidence for long-term vegetation shifts. J Ecol 93:1085–1093. https://doi.org/10.1111/j.1365-2745.2005.01042.x
Nepstad DC, Thover IM, Ray D, Mouthino P, Cardinot G (2007) Mortality of large trees and lianas following experimental drought in an amazon forest. Ecology 88:2259–2269. https://doi.org/10.1890/06-1046.1
Ninyerola M, Pons X, Roure JM (2000) A methodological approach of climatological modelling of air temperature and precipitation throughout GIS technique. Int J Clim 20:1823–1841. https://doi.org/10.1002/1097-0088(20001130)20:14<1823::AID-JOC566>3.0.CO;2-B
Pasho E, Camarero JJ, de Luis M, Vicente-Serrano M (2011) Impacts of drought at different time scales on forest growth across a wide climatic gradient in north-eastern Spain. Agric For Meteorol 151:1800–1811. https://doi.org/10.1016/j.agrformet.2011.07.018
Peltier DMP, Fell M, Ogle K (2016) Legacy effects of drought in the southwestern United States: a multi-species synthesis. Ecol Monogr 86:312–326. https://doi.org/10.1002/ecm.1219
Phillips OL, van der Heijden C, Lewis SL, López-González G, Aragão LEOC, Lloyd J, Malhi Y, Monteagudo A, Almeida S, Dávila EA, Amaral I, Andelman S, Andrade A, Arroyo L, Aymard G, Baker TR, Blanc L, Bonal D, Oliveira ACA, Chao KJ, Cardozo ND, da Costa L, Feldpausch TR, Fisher JB, Fyllas NM, Freitas MA, Galbraith D, Gloor E, Higuchi N, Honorio E, Jiménez E, Keeling H, Killen TJ, Lovett JC, Meir P, Mendoza C, Morel A, Vargas PN, Patiño S, Peh KS-H, Cruz AP, Prieto A, Quesada CA, Ramírez F, Ramírez H, Rudas A, Salamão R, Schwarz M, Silva J, Silveira M, Silk JWF, Sonké B, Thomas AS, Stropp J, Taplin JR, Vásquez R, Vilanova E (2010) Drought-mortality relationships for tropical forests. New Phytol 187:631–646. https://doi.org/10.1111/j.1469-8137.2010.03359.x
Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-128, http://CRAN.R-project.org/package=nlme
Poyatos R, Aguadé D, Galiano L, Mencuccini M, Martínez-Vilalta J (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytol 200:388–401. https://doi.org/10.1111/nph.12278
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rowland L, da Costa ACL, Galbraith DR, Rs Oliveira, Binks OJ, Oliveira AAR, Pullen AM, Doughty CE, Metcalfe DB, Vasconcelos SS, Ferreira LV, Malhi Y, Grace J, Mencuccini M, Meir P (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528:119–122. https://doi.org/10.1038/nature15539
Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth: what keeps trees from growing beyond a certain height? Bioscience 47:235–242. https://doi.org/10.2307/1313077
Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381. https://doi.org/10.1111/j.1365-3040.2005.01478.x
Schwalm CR, Anderegg WRL, Michalak AM, Fisher JB, Biondi F, Koch G, Litvak M, Ogle K, Shaw JD, Wolf A, Huntzinger DN, Schaefer K, Cook R, Wei Y, Fang Y, Hayes D, Huang M, Jain A, Tian H (2017) Global patterns of drought recovery. Nature 548:202–205. https://doi.org/10.1038/nature23021
Shi Z, Xu L, Dong L, Gao J, Yang X, Lu S, Feng Ch, Shang J, Song A, Guo H, Zhang X (2015) Growth-climate response and drought reconstruction from tree-ring of Mongolian pine in Hulunbuir, Northeast China. J Plant Ecol. https://doi.org/10.1093/jpe/rtv029
Van Gunst KJ, Weisberf PJ, Yang J, Fan Y (2016) Do denser forests have greater risk of tree mortality: a remote sensing analysis of density-dependent forest mortality. For Ecol Manege 359:19–32. https://doi.org/10.1016/j.foreco.2015.09.032
Vicente-Serrano SM, Begueria S, López-Moreno JI (2010) A multiscalar drought index sensitive to global warming: the standardized precipitation evapotranspiration index. J Clim 23:1696–1718. https://doi.org/10.1175/2009JCLI2909.1
Vilà-Cabrera A, Martínez-Vilalta J, Vayreda J, Retana J (2011) Structural and climatic determinants of demographic rates of Scots pine forests across the Iberian Peninsula. Ecol Appl 21:1162–1172. https://doi.org/10.1890/10-0647.1
Vilà-Cabrera A, Martínez-Vilalte J, Galiano L, Retana J (2013) Patterns of forest decline and regeneration across scots pine populations. Ecosystems 16:323–335. https://doi.org/10.1007/s10021-012-9615-2
Zang C, Hartl-Meier C, Dittmar C, Rothe A, Menzel A (2014) Patterns of drought tolerance in major European temperate forest trees: climatic drivers and levels of variability. Glob Change Biol 20:3767–3779. https://doi.org/10.1111/gcb.12637
Acknowledgements
We thank Núria Serra for assistance with sample, processing in the laboratory and cross-dating of dendrochronological series. We also thank Teresa Rosas and Carles Batlles for their advice and help during the development of the project. This project has been funded by the Spanish Ministry of Economy and Competitiveness through grant CGL3013-46808-R. J. Martínez-Vilalta benefits from an ICREA Academia award.
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MM and JMV conceived and designed the study. XSM performed statistical analyses. XSM, JMV and MM interpreted the data. XSM wrote the manuscript. JMV and MM critically revised the manuscript.
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Communicated by Jeremy Lichstein.
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Serra-Maluquer, X., Mencuccini, M. & Martínez-Vilalta, J. Changes in tree resistance, recovery and resilience across three successive extreme droughts in the northeast Iberian Peninsula. Oecologia 187, 343–354 (2018). https://doi.org/10.1007/s00442-018-4118-2
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DOI: https://doi.org/10.1007/s00442-018-4118-2
Keywords
- Drought
- Mediterranean
- Pinus
- BAI
- Resilience