Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Differential impact of the most extreme drought event over the last half century on growth and sap flow in two coexisting Mediterranean trees

Abstract

Extreme climatic events such as intense droughts are becoming more frequent in Mediterranean regions, but our understanding of their impact on tree performance is still fragmentary. We analyzed growth and sap flow responses for a 3-year period including the most stressful drought over the last half century in the evergreen Pinus nigra and the deciduous Quercus faginea, two dominant tree species in the continental plateau of the Iberian Peninsula. Our aim was to quantify the differential impacts of this event on the performance of both species and their modulation by local microclimate. Growth was registered with digital dendrometers, and water use was assessed by continuously recording sap flow in 8–9 coexisting adult individuals of each species in two sites. Q. faginea spring growth rate decreased by 60 % during the dry year at the dry site, while the decrease in P. nigra was around 36 %. P. nigra exhibited larger sap flow reductions during the dry season and also larger decreases during the extreme year, but in contrast to Q. faginea, it was able to recover growth and sap flow values after the extreme drought. Minor microclimatic differences between sites had significant effects on growth and water use, with slightly more mesic conditions significantly attenuating the impact of drought on both species. Findings suggest that the study species were near to their tolerance thresholds, so that even moderate increases in the intensity and frequency of unusual droughts have important consequences for individual tree performance, and eventually species coexistence and ecosystem processes.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality: implications for regional die-off under global-change-type drought. P Natl Acad Sci USA 106:7063–7066

  2. Alexander LV, Zhang X, Peterson TC, Caesar J, Gleason B, Klein Tank AMG, Haylock M, Collins D, Trewin B, Rahimzadeh F, Tagipour A, Rupa Kumar K, Revadekar J, Griffiths G, Vincent L, Stephenson DB, Burn J, Aguilar E, Brunet M, Taylor M, New M, Zhai P, Rusticucci M, Vazquez-Aguirre JL (2006) Global observed changes in daily climate extremes of temperature and precipitation. J Geophys Res Atmos 111(D5). doi:10.1029/2005jd006290

  3. Allen CD, Breshears DD (1998) Drought-induced shift of a forest–woodland ecotone: rapid landscape response to climate variation. Proc Natl Acad Sci Biol 95(25):14839–14842

  4. 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 J-H, 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 Manage 259(4):660–684

  5. Anderegg WL, Anderegg LL, Berry J, Field C (2014) Loss of whole-tree hydraulic conductance during severe drought and multi-year forest die-off. Oecologia 175(1):11–23

  6. Aranda I, Gil L, Pardos JA (2005) Seasonal changes in apparent hydraulic conductance and their implications for water use of European beech (Fagus sylvatica L.) and sessile oak Quercus petraea (Matt.) Liebl in South Europe. Plant Ecol 179(2):155–167

  7. Aranda I, Forner A, Cuesta B, Valladares F (2012) Species-specific water use by forest tree species: from the tree to the stand. Agric Water Manag 114:67–77

  8. Bladé I, Castro Díez Y (2010) Atmospheric trends in the Iberian Peninsula during the instrumental period in the context of natural variability. In: Pérez FF, Boscolo R (eds) Climate in Spain: past, present and future. Ministerio de Ciencia e Innovación, pp 25–41

  9. Blondel J, Aronson J (1995) Biodiversity and ecosystem function in the Mediterranean basin: human and non-human determinants. In: Davis GW, Richardson DM (eds) Mediterranean-type ecosystems: the function of biodiversity, Springer-Verlag Berling, pp 43–105

  10. Brantley S, Ford CR, Vose JM (2013) Future species composition will affect forest water use after loss of eastern hemlock from southern Appalachian forests. Ecol Appl 23(4):777–790

  11. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63(6):625–644

  12. Brito P, Lorenzo J, González-Rodríguez Á, Morales D, Wieser G, Jimenez M (2014) Canopy transpiration of a Pinus canariensis forest at the tree line: implications for its distribution under predicted climate warming. Eur For Res 133(3):491–500

  13. Burgess SSO (2006) Measuring transpiration responses to summer precipitation in a Mediterranean climate: a simple screening tool for identifying plant water-use strategies. Physiol Plant 127:404–412

  14. Camarero JJ, Sangüesa-Barreda G, Alla AQ, González de Andrés E, Maestro-Martínez M, Vicente-Serrano SM (2012) Los precedentes y las respuestas de los árboles a sequías extremas revelan los procesos involucrados en el decaimiento de bosques mediterráneos de coníferas. Ecosistemas 21(3):22–30

  15. Campbell GS, Norman JM (1998) An introduction to environmental biophysics, 2nd edn. Springer, New York

  16. Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. PNAS 108(4):1474–1478

  17. Čermák J, Kučera J, Nadezhdina N (2004) Sap flow measurements with some thermodynamic methods, flow integration within trees and scaling up from sample trees to entire forest stands. Trees 18(5):529–546

  18. Chesson P (2000) Mechanisms of maintenance of species diversity. Ann Rev Ecol Evol Syst 31:343–366

  19. Chesson P, Huntly N (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. Am Nat 150:519–553

  20. Chirino E, Bellot J, Sánchez J (2011) Daily sap flow rate as an indicator of drought avoidance mechanisms in five Mediterranean perennial species in semi-arid southeastern Spain. Trees 25(4):593–606

  21. Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grunwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437(7058):529–533

  22. David TS, Henriques MO, Kurz-Besson C, Nunes J, Valente F, Vaz M, Pereira JS, Siegwolf R, Chaves MM, Gazarini LC, David JS (2007) Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol 27(6):793–803

  23. del Cacho M, Lloret F (2012) Resilience of Mediterranean shrubland to a severe drought episode: the role of seed bank and seedling emergence. Plant Biol 14(3):458–466

  24. Della-Marta PM, Haylock MR, Luterbacher J, Wanner H (2007) Doubled length of western European summer heat waves since 1880. J Geophys Res 112(D15). doi:10.1029/2007jd008510

  25. Drake P, Mendham D, White D, Ogden G, Dell B (2012) Water use and water-use efficiency of coppice and seedling Eucalyptus globulus Labill.: a comparison of stand-scale water balance components. Plant Soil 350(1–2):221–235

  26. Drew DM, Downes GM (2009) The use of precision dendrometers in research on daily stem size and wood property variation: a review. Dendrochronologia 27:159–172

  27. Durante P, Oyonarte C, Valladares F (2009) Influence of land-use types and climatic variables on seasonal patterns of NDVI in Mediterranean Iberian ecosystems. Appl Veg Sci 12(2):177–185

  28. Ferrero LM, Montouto O, Herranz JM (2006) Flora amenazada y protegida del Parque Natural del Alto Tajo. Junta de Comunidades de Castilla-La Mancha, Guadalajara

  29. Forrester DI, Collopy JJ, Morris JD (2010) Transpiration along an age series of Eucalyptus globulus plantations in southeastern Australia. For Ecol Manage 259(9):1754–1760

  30. Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30(1):19–30

  31. Gaultier J-P, Lorenzati S, Bigorre F, Tessier D (2000) Spatialisation du bilan de l’eau dans les sols du Dogger lorrain; influence du type de sol et de son usage. In: Hermès (ed) SIG et simulations. Géomatique, vol 10. pp 19–38

  32. Grace J (2004) Understanding and managing the global carbon cycle. J Ecol 92(2):189–202

  33. Granda E, Camarero JJ, Gimeno TE, Martinez-Fernandez J, Valladares F (2013) Intensity and timing of warming and drought differentially affect growth patterns of co-occurring Mediterranean tree species. Eur J For Res 132(3):469–480

  34. Granda E, Rossatto DR, Camareror JJ, Voltas J, Valladares F (2014) Growth and carbon isotopes of Mediterranean trees reveal contrasting responses to increased carbon dioxide and drought. Oecologia 174:307–317

  35. Granier A, Breda N (1996) Modelling canopy conductance and stand transpiration of an oak forest from sap flow measurements. Ann Sci For 53(2–3):537–546

  36. Granier A, Bréda N, Biron P, Villette S (1999) A lumped water balance model to evaluate duration and intensity of drought constraints in forest stands. Ecol Model 116:269–283

  37. Granier A, Biron P, Lemoine D (2000) Water balance, transpiration and canopy conductance in two beech stands. Agric For Meteorol 100(4):291–308

  38. Gyenge J, Fernández M, Sarasola M, Schlichter T (2011) Stand density and drought interaction on water relations of Nothofagus antarctica: contribution of forest management to climate change adaptability. Trees 25(6):1111–1120

  39. Himmelsbach W, Treviño-Garza E, González-Rodríguez H, González-Tagle M, Gómez Meza M, Aguirre Calderón O, Eduardo Estrada Castillón A, Mitlöhner R (2012) Acclimatation of three co-occurring tree species to water stress and their role as site indicators in mixed pine-oak forests in the Sierra Madre Oriental, Mexico. Eur J For Res 131(2):355–367

  40. Ibáñez I, Schupp EW, Boettinger JL (1998) Successional history of a Curleaf mountain mahogany stand: a hypothesis. In: McArthur E, et al (eds) Proceedings: shrubland ecotones. US Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Ft Collins

  41. IPCC (2012) Summary for Policymakers. In: Field CB, Barros V, Stocker TF, Qin D, Dokken DJ, Ebi KL, Mastrandrea MD (eds) Managing the risks of extreme events and disasters to advance climate change adaptation. A special report of working groups I and II of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, New York, NY, USA, pp 1–19

  42. IPCC (2013a) The physical science basis: working group I contribution to the fourth assessment report of the IPCC. Cambridge University Press, Cambridge

  43. IPCC (2013b) Summary for Policymaker. In: Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change, Cambridge, United Kingdom and New York, USA

  44. Jump AS, Hunt JM, Peñuelas J (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Glob Chang Biol 12(11):2163–2174

  45. Klein T, Shpringer I, Fikler B, Elbaz G, Cohen S, Yakir D (2013) Relationships between stomatal regulation, water-use, and water-use efficiency of two coexisting key Mediterranean tree species. For Ecol Manage 302:34–42

  46. Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7(1):69–80

  47. Köstner B, Biron P, Siegwolf R, Granier A (1996) Estimates of water vapor flux and canopy conductance of Scots Pine at the tree level utilizing different xylem sap flow methods. Theor Appl Climatol 53:105–113

  48. Kunert N, Schwendenmann L, Hölscher D (2010) Seasonal dynamics of tree sap flux and water use in nine species in Panamanian forest plantations. Agric For Meteorol 150(3):411–419

  49. Lagergren F, Lindroth A (2004) Variation in sap flow and stem growth in relation to tree size, competition and thinning in a mixed forest of pine and spruce in Sweden. For Ecol Manage 188(1–3):51–63

  50. Leuzinger S, Zotz G, Asshoff R, Körner C (2005) Responses of deciduous forest trees to severe drought in Central Europe. Tree Physiol 25:641–650

  51. Linares JC, Camarero JJ (2012) From pattern to process: linking intrinsic water-use efficiency to drought-induced forest decline. Glob Chang Biol 18(3):1000–1015

  52. 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(3):592–603

  53. Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manage 259(4):698–709

  54. Lloret F (2012) Vulnerabilidad y resiliencia de ecosistemas forestales frente a episodios extremos de sequía. Ecosistemas 21(3):85–90

  55. Lloret F, Escudero A, Iriondo JM, Martínez-Vilalta J, Valladares F (2012) Extreme climatic events and vegetation: the role of stabilizing processes. Glob Chang Biol 18(3):797–805

  56. Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20(2):131–138

  57. Martínez-Vilalta J, Piñol J (2003) Limitaciones hidráulicas al aporte de agua a las hojas y resistencia a la sequía. Ecosistemas 12(1)

  58. Martínez-Vilalta J, Prat E, Oliveras I, Piñol J (2002) Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133(1):19–29

  59. Maysek K, Hemming D, Angert A, Leavitt SW, Yakir D (2011) Increase in water-use efficiency and underlying processes in pine forests across a precipitation gradient in the dry Mediterranean region over the past 30 years. Oecologia 167:573–585

  60. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155(3):1051–1059

  61. McDowell NG, Fisher RA, Xu C, Domec JC, Hölttä T, Mackay DS, Sperry JS, Boutz A, Dickman L, Gehres N, Limousin JM, Macalady A, Martínez-Vilalta J, Mencuccini M, Plaut JA, Ogée J, Pangle RE, Rasse DP, Ryan MG, Sevanto S, Waring RH, Williams AP, Yepez EA, Pockman WT (2013) Evaluating theories of drought-induced vegetation mortality using a multimodel–experiment framework. New Phytol 200(2):304–321

  62. Morán-López T, Poyatos R, Llorens P, Sabaté S (2014) Effects of past growth trends and current water use strategies on Scots pine and pubescent oak drought sensitivity. Eur J For Res 133(2):369–382

  63. Nadal-Sala D, Sabaté S, Gracia C (2013) GOTILWA+: un modelo de procesos que evalúa efectos del cambio climático en los bosques y explora alternativas de gestión para su mitigación. Ecosistemas 22(3):29–36

  64. Ogaya R, Peñuelas J (2007) Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecol 189(2):291–299

  65. Otero I, Boada M, Badia A, Pla E, Vayreda J, Sabaté S, Gracia C, Peñuelas J (2011) Loss of water availability and stream biodiversity under land abandonment and climate change in a Mediterranean catchment (Olzinelles, NE Spain). Land Use Policy 28:207–218

  66. Penman H (1948) Natural Evaporation from Open Water, Bare Soil and Grass. Proc R Soc Lond A Math Phys 193(1032):120–145

  67. Peñuelas J, Boada M (2003) A global change-induced biome shift in the Montseny mountains (NE Spain). Glob Chang Biol 9(2):131–140

  68. Peñuelas J, Filella I, Lloret F, Piñol J, Siscart D (2000) Effects of a severe drought on water and nitrogen use by Quercus ilex and Phillyrea latifolia. Biol Plant 43(1):47–53

  69. Peñuelas J, Lloret F, Montoya R (2001) Severe drought effects on Mediterranean woody flora in Spain. Forest Sci 47(2):214–218

  70. Peñuelas J, Sardans J, Estiarte M, Ogaya R, Carnicer J, Coll M, Barbeta A, Rivas-Ubach A, Llusia J, Garbulsky M, Filella I, Jump AS (2013) Evidence of current impact of climate change on life: a walk from genes to the biosphere. Glob Chang Biol 19(8):2303–2338

  71. Pinheiro J, Bates D, DebRoy S, Sarkar D (2007) The nlme package: linear and nonlinear mixed effects models. R package version 31–108

  72. Poyatos R, Cermak J, Llorens P (2007) Variation in the radial patterns of sap flux density in pubescent oak (Quercus pubescens) and its implications for tree and stand transpiration measurements. Tree Physiol 27:537–548

  73. Poyatos R, Llorens P, Piñol J, Rubio C (2008) Response of Scots pine (Pinus sylvestris L.) and pubescent oak (Quercus pubescens Willd.) to soil and atmospheric water deficits under Mediterranean mountain climate. Ann For Sci 65(3):306

  74. Quero JL, Sterck FJ, Martinez-Vilalta J, Villar R (2011) Water-use strategies of six co-existing Mediterranean woody species during a summer drought. Oecologia 166(1):45–57

  75. Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32(6):764–775

  76. Sarris D, Christodoulakis D, KÖRner C (2007) Recent decline in precipitation and tree growth in the eastern Mediterranean. Glob Chang Biol 13(6):1187–1200

  77. Steppe K, Pauw DJW, Lemeur R, Vanrolleghem PA (2005) A mathematical model linking tree sap flow dynamics to daily stem diameter fluctuations and radial stem growth. Tree Physiol 26:257–273

  78. Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Biol 49:419–432

  79. Tognetti R, Longobucco A, Miglietta F, Raschi A (1998) Transpiration and stomatal behaviour of Quercus ilex plants during the summer in a Mediterranean carbon dioxide spring. Plant Cell Environ 21(6):613–622

  80. Voltas J, Camarero JJ, Carulla D, Aguilera M, Ortiz A, Ferrio JP (2013) A retrospective, dual-isotope approach reveals individual predispositions to winter-drought induced tree dieback in the southernmost distribution limit of Scots pine. Plant Environ 36(8):1435–1448

  81. Zapater M, Bréda N, Bonal D, Pardonnet S, Granier A (2012) Differential response to soil drought among co-occurring broad-leaved tree species growing in a 15- to 25-year-old mixed stand. Ann For Sci 70(1):31–39

  82. Zuur A, Ieno E, Smith G (2007) Analysing ecological data. Springer, New York

  83. Zweifel R, Zimmermann L, Newbery DM (2005) Modeling tree water deficit from microclimate: an approach to quantifying drought stress. Tree Physiol 25:147–156

  84. Zweifel R, Steppe K, Sterck F (2007) Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model. J Exp Bot 58(8):2113–2131

  85. Zweifel R, Rigling A, Dobbertin M (2009) Species-specific stomatal response of trees to drought-a link to vegetation dynamics? J Veg Sci 20:442–454

Download references

Acknowledgments

Authors thank the Junta de Castilla-La Mancha, Director and Park Rangers of the Alto Tajo Natural Park for the permission to carry out the study in the Park and for the information and facilities provided. Authors are very grateful to David López-Quiroga for his inestimable support in field work. We also thank to T. Morán and S. Matesanz for their help with statistical analysis and to E. Granda, A. Rey and A. Dolinger for corrections, which improved the manuscript. Meteorological data for the reference station of Molina de Aragón were provided by the Spanish Meteorological Agency (AEMET). Authors thank to M. Pollastrini for providing data of Plant Area Index (PAI) within project FunDiv Europe. A.F. was supported by JAE-predoc fellowship from the Spanish National Research Council (CSIC), co-funded by the European Union (Fondo Social Europeo). This work was supported by the Spanish Ministry of Economy and Competitiveness with the Grant VULGLO (CGL2010-22180-C03-03), the Community of Madrid Grant REMEDINAL (CM S2009/AMB-1783) and by projects ‘ECOFISEPI’ (AGL2011-25365/BOS) and SUM2008-00004-C03-01 funded by the Ministry of Science and Innovation of Spain.

Author information

Correspondence to Alicia Forner.

Additional information

Communicated by Thomas Abeli, Rodolfo Gentili and Anne Jäkäläniemi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 33 kb)

Supplementary material 2 (DOC 53 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Forner, A., Aranda, I., Granier, A. et al. Differential impact of the most extreme drought event over the last half century on growth and sap flow in two coexisting Mediterranean trees. Plant Ecol 215, 703–719 (2014). https://doi.org/10.1007/s11258-014-0351-x

Download citation

Keywords

  • Extreme drought
  • Pinus nigra
  • Quercus faginea
  • Climate change
  • Mediterranean forests