, Volume 180, Issue 4, pp 961–973 | Cite as

Climatic events inducing die-off in Mediterranean shrublands: are species’ responses related to their functional traits?

  • Francisco LloretEmail author
  • Enrique G. de la Riva
  • Ignacio M. Pérez-Ramos
  • Teodoro Marañón
  • Sandra Saura-Mas
  • Ricardo Díaz-Delgado
  • Rafael Villar
Special Topic on Functional Traits


Extreme climatic episodes, likely associated with climate change, often result in profound alterations of ecosystems and, particularly, in drastic events of vegetation die-off. Species attributes are expected to explain different biological responses to these environmental alterations. Here we explored how changes in plant cover and recruitment in response to an extreme climatic episode of drought and low temperatures were related to a set of functional traits (of leaves, roots and seeds) in Mediterranean shrubland species of south-west Spain. Remaining aerial green cover 2 years after the climatic event was positively related to specific leaf area (SLA), and negatively to leaf water potential, stable carbon isotope ratio and leaf proline content. However, plant cover resilience, i.e. the ability to attain pre-event values, was positively related to a syndrome of traits distinguished by a higher efficiency of water use and uptake. Thus, higher SLA and lower water-use efficiency characterized species that were able to maintain green biomass for a longer period of time but were less resilient in the medium term. There was a negative relationship between such syndromes and the number of emerging seedlings. Species with small seeds produced more seedlings per adult. Overall, recruitment was positively correlated with species die-off. This study demonstrates the relationship between plant traits and strong environmental pulses related to climate change, providing a functional interpretation of the recently reported episodes of climate-induced vegetation die-off. Our findings reveal the importance of selecting meaningful traits to interpret post-event resilience processes, particularly when combined with demographic attributes.


Climate change Drought Extreme climate episode Recruitment Resilience 



This study was supported by the projects CGL2009-08101, CGL2010-16373, CGL2012-32965, DIVERBOS (CGL2011-30285-C02-01 and C02-02), AGAUR 2009-SGR-00247 and 2014-SGR-00453, ICTS-RBD 38/2007, 27/2009 and 11/2013, ECO-MEDIT (CGL2014-53236-R), and by European FEDER funds. Personnel from the ICTS-RBD kindly supported the fieldwork. We thank C. Padilla, C. Navarro and M. Olmo for help during field sampling and trait measurements. Seed mass data were kindly provided by the Jardín Botánico de Córdoba (Francisca Herrera). Isotopic analysis was carried out in the Laboratorio de Isótopos Estables (LIE) de la Estación Biológica de Doñana, the Consejo Superior de Investigaciones Científicas, and leaf nitrogen measurement at the Servicio Central de Apoyo a la Investigación of the University of Córdoba.

Author contribution statement

F. L. conceived and designed the study. F. L., S. S.-M. and R. D.-D. performed the demographic surveys and E. G. R., I. M. P.-R., T. M. and R. V. carried out the measurements of plant functional traits. F. L. and E. G. R. analysed the data. F. L. and E. G. R. wrote the manuscript; other authors contributed to the discussion and interpretation of data and provided editorial advice.

Supplementary material

442_2016_3550_MOESM1_ESM.docx (4.3 mb)
Supplementary material 1 (DOCX 4431 kb)


  1. Ackerly DD (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecol Monogr 74:25–44CrossRefGoogle Scholar
  2. Ain-Lhout F, Zunzunegui M, Díaz-Barradas MC, Tirado R, Clavijo A, García-Novo F (2001) Comparison of proline accumulation in two Mediterranean shrubs subjected to natural and experimental water deficit. Plant Soil 230:175–183CrossRefGoogle Scholar
  3. Albert CH, Grassein F, Schurr FM et al (2011) When and how should intraspecific variability be considered in trait-based plant ecology? Perspect Plant Ecol Evol Syst 13:217–235CrossRefGoogle Scholar
  4. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowelll N, Vennetier M, Kitzberger T, Rigling A, Breshears D, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Limm 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 Manage 259:660–684CrossRefGoogle Scholar
  5. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109:233–237CrossRefPubMedPubMedCentralGoogle Scholar
  6. Breshears DD, Cobb NS, Rich PM et al (2005) Regional vegetation die-off in response to global-change-type drought. Proc Natl Acad Sci USA 102:15144–15148CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cavender-Bares J, Cortes P, Rambal S, Joffre R, Miles B, Rocheteau A (2005) Summer and winter sensitivity of leaves and xylem to minimum freezing temperatures: a comparison of cooccurring Mediterranean oaks that differ in leaf lifespan. New Phytol 168:597–612CrossRefPubMedGoogle Scholar
  8. Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Let 12:693–715CrossRefGoogle Scholar
  9. Chapin FS III (2003) Effects of plant traits on ecosystem and regional processes: a conceptual framework for predicting the consequences of global change. Ann Bot 91:455–463CrossRefPubMedPubMedCentralGoogle Scholar
  10. Davis SD, Ewers FW, Pratt RB, Brown PL, Bowen TJ (2005) Interactive effects of freezing and drought on long distance transport: a case study of chaparral shrubs of California. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier, Burlington, pp 425–435CrossRefGoogle Scholar
  11. de la Riva EG, Pérez-Ramos IM, Tosto A, Navarro-Fernández CM, Olmo M, Marañón T, Villar R (2015) Disentangling the relative importance of species occurrence, abundance and intraspecific variability in community assembly: a trait-based approach at the whole-plant level in Mediterranean forests. Oikos. doi: 10.1111/oik.01875
  12. del Cacho M, Lloret F (2012) Resilience of Mediterranean shrubland to severe drought episode: the role of seed bank and seedling establishment. Plant Biol 14:458–466CrossRefPubMedGoogle Scholar
  13. Diaz Barradas MC, Zunzunegui M, Tirado R, Ain-Lhout F, García Novo F (1999) Plant functional types and ecosystem function in Mediterranean shrubland. J Veg Sci 10:719–726Google Scholar
  14. Diaz S, Cabido M, Casanoves F (1998) Plant functional traits and environmental filters at a regional scale. J Veg Sci 9:113–122CrossRefGoogle Scholar
  15. Diaz S, Hodgson JG, Thompson K (2014) The plant traits that drive ecosystems: evidence from three continents. J Veg Sci 15:295–304CrossRefGoogle Scholar
  16. Díaz-Delgado R (2006) Evento de mortalidad en la vegetación terrestre del Parque Nacional de Doñana. Estación Biológica de Doñana, CSIC, SevillaGoogle Scholar
  17. Domínguez MT, Aponte C, Pérez-Ramos IM, García LV, Villar R, Marañón T (2012) Relationships between leaf morphological traits, nutrient concentrations and isotopic signatures for Mediterranean woody plant species and communities. Plant Soil 357:407–424CrossRefGoogle Scholar
  18. Easterling D, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modelling, and impacts. Science 289:2068–2074CrossRefPubMedGoogle Scholar
  19. Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782CrossRefGoogle Scholar
  20. Esther A, Groeneveld J, Enright NJ, Miller BP, Lamont BB, Perry GLW, Blank FB, Jeltsch F (2010) Sensitivity of plant functional types to climate change: classification tree analysis of a simulation model. J Veg Sci 21:447–461CrossRefGoogle Scholar
  21. Farquhar GD, Learyb MHO, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137CrossRefGoogle Scholar
  22. García Murillo P, Sousa Martín A (1999) El paisaje vegetal de la zona oeste del Parque Natural de Doñana (Huelva). Lagascalia 21:11–132Google Scholar
  23. García C, Moracho E, Díaz-Delgado R, Jordano P (2014) Long-term expansion of juniper populations in managed landscapes: patterns in space and time. J Ecol 102:1562–1571CrossRefGoogle Scholar
  24. Granda E, Scoffoni C, Rubio-Casal AE, Sack L, Valladares F (2014) Leaf and stem physiological responses to summer and winter extremes of woody species across temperate ecosystems. Oikos 123:1281–1290CrossRefGoogle Scholar
  25. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553CrossRefGoogle Scholar
  26. Hernandez EI, Pausas JG, Vilagrosa A (2011) Leaf physiological traits in relation to resprouter ability in the Mediterranean Basin. Plant Ecol 212:1959–1966CrossRefGoogle Scholar
  27. IPCC (2013) Climate change 2013: the physical scientific basis. WMO, UNEPGoogle Scholar
  28. Karavatas S, Manetas Y (1999) Seasonal patterns of photosystem II photochemical efficiency in evergreen sclerophylls and drought semi-deciduous shrubs under Mediterranean field conditions. Photosynthetica 36:41–49CrossRefGoogle Scholar
  29. Kichenin E, Wardle DA, Peltzer DA, Morse CW, Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along and environmental gradient. Funct Ecol 27:1254–1261CrossRefGoogle Scholar
  30. Koepke DF, Kolb TE, Adams HD (2010) Variation in woody plant mortality and dieback from severe drought among soils, plant groups, and species within a northern Arizona ecotone. Oecologia 163:1079–1090CrossRefPubMedGoogle Scholar
  31. Lagan SJ, Ewers FW, Davis SD (1997) Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs. Plant Cell Environ 20:425–437CrossRefGoogle Scholar
  32. Larcher W (1981) Low temperature effects on Mediterranean sclerophylls: an unconventional viewpoint. In: Margaris NS, Mooney HA (eds) Components of productivity of Mediterranean-climate regions—basic and applied aspects. Junk, the Hague, pp 259–266CrossRefGoogle Scholar
  33. Leishman MR (2001) Does the seed size/number trade-off model determine plant community structure? An assessment of the model mechanisms and their generality. Oikos 93:294–302CrossRefGoogle Scholar
  34. Lloret F (1998) Fire, canopy cover and seedling dynamics in Mediterranean shrubland of northeastern Spain. J Veg Sci 9:417–430CrossRefGoogle Scholar
  35. Lloret F, Granzow-de la Cerda I (2013) Plant competition and facilitation after extreme drought episodes in Mediterranean shrubland: does damage to vegetation cover trigger replacement by juniper woodland? J Veg Sci 24:1020–1032CrossRefGoogle Scholar
  36. Lloret F, Casanovas C, Peñuelas J (1999) Seedling survival of Mediterranean shrubland species in relation to root:shoot ratio, seed size and water and nitrogen use. Funct Ecol 13:210–216CrossRefGoogle Scholar
  37. Lloret F, Keeling E, Sala A (2011) Components of tree resilience: effects of successive low-growth episodes in old ponderosa pine forests. Oikos 120:1909–1920CrossRefGoogle Scholar
  38. 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 18:797–805CrossRefGoogle Scholar
  39. Lloret F, Martínez-Vilalta J, Serra-Díaz J, Ninyerola M (2013) Relationship between projected changes in climatic suitability and demographic and functional traits of forest tree species in Spain. Clim Change 120:449–462CrossRefGoogle Scholar
  40. Logullo MA, Salleo S (1993) Different vulnerabilities of Quercus ilex L. to freeze-and summer drought-induced xylem embolism: an ecological interpretation. Plant Cell Environ 16:511–519CrossRefGoogle Scholar
  41. Martínez F, Merino O, Martín A, García Martín D, Merino J (1998) Belowground structure and production in a Mediterranean sand dune shrub community. Plant Soil 201:209–216CrossRefGoogle Scholar
  42. Martínez-Vilalta J, Mencuccini M, Vayreda J, Retana J (2010) Interspecific variation in functional traits, not climatic differences among species ranges, determines demographic rates across 44 temperate and Mediterranean tree species. J Ecol 98:1462–1475CrossRefGoogle Scholar
  43. Martínez-Vilalta J, Breshears DD, Lloret F (2012) Drought-induced forest decline: causes, scope and implications. Biol Lett 8:689–691CrossRefPubMedPubMedCentralGoogle Scholar
  44. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195:823–831CrossRefGoogle Scholar
  45. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mitrakos K (1980) A theory for Mediterranean plant life. Acta Oecol Oecol Plant 1:245–252Google Scholar
  47. Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113:91–105CrossRefGoogle Scholar
  48. Muller-Landau HC (2010) The tolerance-fecundity trade-off and the maintenance of diversity in seed size. Proc Natl Acad Sci USA 107:4242–4247CrossRefPubMedPubMedCentralGoogle Scholar
  49. Oliveira G, Peñuelas J (2004) Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L. Plant Ecol 175:179–191CrossRefGoogle Scholar
  50. Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JL, de Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Bonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234Google Scholar
  51. Pérez-Ramos IM, Roumet C, Cruz P, Blanchard A, Autran P, Garnier E (2012) Evidence for a “plant community economics spectrum” driven by nutrient and water limitations in a Mediterranean rangeland of southern France. J Ecol 100:1315–1327CrossRefGoogle Scholar
  52. Pérez-Ramos IM, Volaire F, Fattet M, Blanchard A, Roumet C (2013) Tradeoffs between functional strategies for resource-use and drought-survival in Mediterranean rangeland species. Environ Exp Bot 87:126–136CrossRefGoogle Scholar
  53. Pivovaroff AL, Sack L, Santiago LS (2014) Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis. New Phytol 302:842–850CrossRefGoogle Scholar
  54. Pratt RB, Ewers FW, Lawson MC, Jacobsen AL, Brediger MM, Davis SD (2005) Mechanisms for tolerating freeze-thaw stress of two evergreen chaparral species: Rhus ovata and Malosma laurina (Anacardiaceae). Am J Bot 92:1102–1113CrossRefPubMedGoogle Scholar
  55. Pratt RB, Jacobsen AL, Mohla R, Ewers FW, Davis SD (2008) Linkage between water stress tolerance and life history type in seedlings of nine chaparral species (Rhamnaceae). J Ecol 96:1252–1265CrossRefGoogle Scholar
  56. Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL, Mao Z, Pierret A, Portillo N, Roupsard O, Thammahacksa C, Stokes A (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103:361–373CrossRefGoogle Scholar
  57. Reich PB, Walters MB, Ellsworth DS, Vose JM, Volin JC, Gresham C, Bowman WD (1998) Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114:471–482CrossRefGoogle Scholar
  58. Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra and strategy. Int J Plant Sci 164(S3):S143–S164CrossRefGoogle Scholar
  59. Reyer CPO, Leuzinger S, Rammig A, Wolf A, Bartholomeus RP, Bonfante A, De Lorenzi F, Dury M, Glonig P, Jaoudé RA, Klein T, Kuster TM, Martins M, Niedrist G, Riccardi M, Wohlfahrt G, De Angelis P, de Dato G, François L, Menzel A, Pereira M (2013) A plant’s perspective of extremes: terrestrial plant responses to changing climatic variability. Glob Change Biol 19:75–89CrossRefGoogle Scholar
  60. Royer PD, Cobb NS, Clifford MJ, Huang CY, Breshears DD, Adams HD, Villegas JC (2011) Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. J Ecol 99:714–723CrossRefGoogle Scholar
  61. Saura-Mas S, Lloret F (2007) Leaf and shoot water content and leaf dry matter content of Mediterranean woody species with different post-fire regenerative strategies. Ann Bot 99:545–554CrossRefPubMedPubMedCentralGoogle Scholar
  62. Saura-Mas S, Lloret F (2014) Adult root structure of Mediterran shrubs: relationship with post-fire regenerative syndrome. Plant Biol 16:147–154CrossRefPubMedGoogle Scholar
  63. Shih-Chieh K, Ganguly AR (2011) Intensity, duration, and frequency of precipitation extremes under 21st-century warming scenarios. J Geol Res Atmos 112:D16119Google Scholar
  64. Smith SD, Herr CA, Leary KL, Piorkowski JM (1995) Soil-plant water relations in a Mojave Desert mixed shrub community: a comparison of three geomorphic surfaces. J Arid Environ 29:339–351CrossRefGoogle Scholar
  65. Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 15:1736–1752CrossRefGoogle Scholar
  66. Suding KN, Lavorel S, Chapin FS, Cornelissen JHS, Diaz S, Garnier E, Goldberg D, Hooper D, Jackson S, Navas ML (2008) Scaling environmental change through the community-level: a trait-based response and -effect framework for plants. Glob Change Biol 14:1125–1140CrossRefGoogle Scholar
  67. Thuillier W, Lavorel S, Sykes MT, Araujo MB (2006) Using niche-based modelling to assess the impact of climate change on tree functional diversity in Europe. Div Distrib 12:49–60CrossRefGoogle Scholar
  68. Verdú M, Pausas JG (2007) Fire drives phylogenetic clustering in Mediterranean Basin woody plants communities. J Ecol 95:1316–1323CrossRefGoogle Scholar
  69. Villar R, Merino JA (2001) Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytol 151:213–226CrossRefGoogle Scholar
  70. Villar R, Ruiz-Robleto J, de Yong Y, Poorter H (2006) Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant Cell Environ 29:1629–1643CrossRefPubMedGoogle Scholar
  71. Wahl S, Ryser P (2000) Root tissue structure is linked to ecological strategies of grasses. New Phytol 148:459–471CrossRefGoogle Scholar
  72. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159CrossRefGoogle Scholar
  73. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827CrossRefPubMedGoogle Scholar
  74. Zunzunegui M, Barradas MD, Ain-Lhout F, Clavijo A, Novo FG (2005) To live or to survive in Doñana dunes: adaptive responses of woody species under a Mediterranean climate. Plant Soil 273:77–89CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Francisco Lloret
    • 1
    Email author
  • Enrique G. de la Riva
    • 2
  • Ignacio M. Pérez-Ramos
    • 3
  • Teodoro Marañón
    • 3
  • Sandra Saura-Mas
    • 1
  • Ricardo Díaz-Delgado
    • 4
  • Rafael Villar
    • 2
  1. 1.CREAF and Unitat d’Ecologia, Department of Biologia Animal, Biologia Vegetal i EcologiaUniversitat Autònoma BarcelonaCerdanyola del VallèsSpain
  2. 2.Área de Ecología, Facultad de CienciasUniversidad de CórdobaCórdobaSpain
  3. 3.IRNAS, CSICSevilleSpain
  4. 4.EBD, CSICSevilleSpain

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