, Volume 29, Issue 6, pp 1791–1804 | Cite as

Pine mortality in southeast Spain after an extreme dry and warm year: interactions among drought stress, carbohydrates and bark beetle attack

  • R. García de la Serrana
  • A. Vilagrosa
  • J. A. Alloza
Original Article
Part of the following topical collections:
  1. Drought Stress


Key message

Pine mortality was related to water stress, which caused xylem cavitation. Hydraulic failure and carbon starvation are likely interrelated, and bark beetles attacks did not seem to be directly involved.


Forests are extremely important for society given the many services they provide. Climate models reflect increases in temperature and less annual rainfall, which will generate hotter drier environments. Under these conditions, it is predicted that forest ecosystems will be severely affected, and recent studies have accumulated evidence for drought-induced tree mortality. Consequently, many studies have attempted to explain mechanisms of survival and mortality in forest species. However, the physiological mechanisms that underlie drought mortality are not completely understood. The aim of the present study was to analyse the effect of an extremely dry year on the cause of mortality of pines and on forest decline in pine forest populations in southeast Spain. Specifically, we studied the effect of drought stress that caused pine mortality, dynamics of carbohydrates reserves and bark beetle attack. The results suggest that pine mortality can be attributed to an intense drought stress level that caused xylem cavitation. The results also indicate that hydraulic failure and carbon starvation are likely interrelated, which makes separating both mechanisms very difficult. Finally, the recorded bark beetles attack did not seem to be directly involved in mortality, at least not in the forests with less intense drought conditions.


Pine mortality Xylem cavitation Carbohydrates Bark beetle infestation Drought Temperature anomalies 



We thank JA. Valiente for supplying the CEAM weather database and JM. Torres for his suggestions to improve the manuscript. This work has been carried out, thanks to Projects SURVIVE (CGL-2011-30531-CO2-02) and GRACCIE (CTM2014-59111-REDC, RED CONSOLIDER-INGENIO 2014 Programme), funded by the Spanish Government, and the PROMETEO programme (DESESTRES 2014/038), funded by Generalitat Valenciana (Regional Valencian Government). R.García de la Serrana is grateful for the Geronimo Forteza grant (FPA/2014/126), funded by Generalitat Valenciana to the SURVIVE project. CEAM is supported by the Generalitat Valenciana.

Compliance with the ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

Supplementary material

468_2015_1261_MOESM1_ESM.docx (350 kb)
Supplementary material 1 (DOCX 349 kb)


  1. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitsberger T, 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 Manage 259:660–684CrossRefGoogle Scholar
  2. Anderegg WRL (2012) Complex aspen forest carbon and root dynamics during drought. Clim Ch 111:983–991CrossRefGoogle Scholar
  3. Anderegg WRL, Anderegg LD (2013) Hydraulic and carbohydrate changes in experimental drought-induced mortality of saplings in two conifer species. Tree Physiol 33:252–260CrossRefPubMedGoogle Scholar
  4. Baquedano FJ, Valladares F, Castillo FJ (2008) Phenotypic plasticity blurs ecotypic divergence in the response of Quercus coccifera and Pinus halepensis to water stress. Eur J For Res 127:495–506CrossRefGoogle Scholar
  5. Barbéro M, Loisel R, Quezel P, Richardson DM, Romane F (1998) Pines of the Mediterranean Basin. In: Richardson DM (ed) Ecology and Biogeography of Pinus. Cambridge University Press, Cambridge, pp 153–170Google Scholar
  6. Bates BC, Kundzewicz ZW, Wu S, Palutikof JP (2008) Climate Change and Water. Technical Paper of the Intergovernmental Panel on Climate Change, pp 210Google Scholar
  7. Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584PubMedCentralCrossRefPubMedGoogle Scholar
  8. Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Berg SL (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ 26:1633–1645CrossRefGoogle Scholar
  9. Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755PubMedGoogle Scholar
  10. De Luis M, Novak K, Raventós J, Gričar J, Prislan P, Čufar K (2011) Climate factors promoting intra-annual density fluctuations in Aleppo pine (Pinus halepensis) from semiarid sites. Dendrochronologia 29:163–169CrossRefGoogle Scholar
  11. 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 Manag 310:1–9CrossRefGoogle Scholar
  12. Edwards WRN, Jarvis PG, Grace J, Moncrieff JB (1994) Reversing cavitation in tracheids of Pinus sylvestris L. under negative water potential. Plant, Cell and Environ 17:389–397CrossRefGoogle Scholar
  13. Froux F, Huc R, Ducrey M, Dreyer E (2002) Xylem hydraulic efficiency versus vulnerability in seedlings of four contrasting Mediterranean tree species (Cedrus atlantica, Cupressus sempervirens, Pinus halepensis and Pinus nigra). Ann For Sci 59:409–418CrossRefGoogle Scholar
  14. Gaylord ML, Kolb TE, Pockman WT, Ja Plaut, Ea Yepez, Macalady AK, McDowell NG (2013) Drought predisposes piñon-juniper woodlands to insect attacks and mortality. New Phytol 198:567–578CrossRefPubMedGoogle Scholar
  15. Hartmann H, Ziegler W, Trumbore S (2013) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427CrossRefGoogle Scholar
  16. Hartmann H, Adams HD, Anderegg WR, Jansen S, Zeppel MJ (2015) Research frontiers in drought-induced tree mortality: crossing scales and disciplines. New Phytol 205:965–969CrossRefPubMedGoogle Scholar
  17. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081CrossRefGoogle Scholar
  18. ICONA 1989. Técnicas de Reforestación en los Países MediterráneosGoogle Scholar
  19. IPCC (2013) Climate change 2013: the Physical Science Basis. In: Stocker TF, Qin D, Plattner GK, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 986Google Scholar
  20. Klein T, Cohen S, Yakir D (2011) Hydraulic adaptations underlying drought resistance of Pinus halepensis. Tree Physiol 31:637–648CrossRefPubMedGoogle Scholar
  21. Leuzinger S, Zotz G, Asshof R, Körner C (2005) Response of deciduous forest trees to severe drought in Central Europe. Tree Physiol 25:641–650CrossRefPubMedGoogle Scholar
  22. McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059PubMedCentralCrossRefPubMedGoogle Scholar
  23. McDowell NG, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739CrossRefPubMedGoogle Scholar
  24. McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532CrossRefPubMedGoogle Scholar
  25. Meinzer FC, Johnson DM, Lachenbruch B, Ka McCulloh, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Func Ecol 23:922–930CrossRefGoogle Scholar
  26. Mitchell PJ, O’Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA (2013) Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol 197:862–872CrossRefPubMedGoogle Scholar
  27. Netherer S, Matthews B, Katzensteiner K, Blackwell E, Henschke P, Hietz P, Schopf A (2015) Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytol 205:1128–1141PubMedCentralCrossRefPubMedGoogle Scholar
  28. Oliveras I, Martínez-Vilalta J, Jimenez-Ortiz T, Lledó MJ, Escarré A, Piñol J (2003) Hydraulic properties of Pinus halepensis, Pinus pinea and Tetraclinis articulata in a dune ecosystem of Eastern Spain. Plant Ecol 169:131–141CrossRefGoogle Scholar
  29. Palacio S, Hernández R, Maestro-Martínez M, Camarero JJ (2012) Fast replenishment of initial carbon stores after defoliation by the pine processionary moth and its relationship to the re-growth ability of trees. Trees 26:1627–1640CrossRefGoogle Scholar
  30. Pausas JG, Bladé C, Valdecantos A, Seva JP, Fuentes D, Alloza JA, Vallejo R (2004) Pines and oaks in the restoration of Mediterranean landscapes of Spain: new perspectives for an old practice a review. Plant Ecol 171:209–220CrossRefGoogle Scholar
  31. Peñuelas J, Ogaya R, Boada M, Jump AS (2007) Migration, invasion and decline: changes in recruitment and forest structure in a warming-linked shift of European beech forest in Catalonia (NE Spain). Ecography 30:829–837CrossRefGoogle Scholar
  32. Pérez Cueva AJ (1994) Atlas climático de la Comunidad Valenciana. Generalitat Valenciana, COPUT, ValenciaGoogle Scholar
  33. Quézel P (2000) Taxonomy and biogeography of Mediterranean pines (Pinus halepensis and P. brutia). In: Neeman G, Trabaud L (eds) Ecology, Biogeography and Management of Pinus halepensis and P. brutia Forest Ecosystems in the Mediterranean Basin. Backhuys Publishers, Leiden, pp 1–12Google Scholar
  34. Raffa KF (2014) Terpenes tell different tales at different scales: glimpses into the chemical ecology of conifer-bark beetle-microbial interactions. J Chem Ecol 40:1–20CrossRefPubMedGoogle Scholar
  35. Rosas T, Galiano T, Ogaya R, Peñuelas J, Martínez-Vilalta J (2013) Dynamics of non-structural carbohydrates in three Mediterranean woody species following long-term experimental drought. Front Plant Sci. 4(400)Google Scholar
  36. Sala A, Hoch G (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant, Cell & Environ 32:22–30CrossRefGoogle Scholar
  37. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought induced tree mortality are far from being resolved. New Phytol 186:274–281CrossRefPubMedGoogle Scholar
  38. Salleo S, Logullo MA, Trifilio P, Nardini A (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis. Plant, Cell Environ 27:1065–1076CrossRefGoogle Scholar
  39. Sobrado MA, Grace J, Jarvis PG (1992) The limits to xylem embolism recovery in Pinus sylvestris.L. J Exp Bot 43:831–836CrossRefGoogle Scholar
  40. Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263CrossRefPubMedGoogle Scholar
  41. Sterl AC, Severijnes C, Dijkstra H, Hazeleger W, Oldenborgh GJ, Broeke M, Burgers G, Hurk B, Leeuwen PJ, Velthoven P (2008) When can we expect extremely high surface temperatures? J Geophys Res 35:L14703Google Scholar
  42. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, BerlinGoogle Scholar
  43. Vélez R (1986) Fire prevention in Aleppo pine forests. Options Mediterraneennes, pp 167–178Google Scholar
  44. Vilagrosa A, Bellot J, Vallejo VR, Gil-Pelegrín E (2003) Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought. J Exp Bot 54:2015–2024CrossRefPubMedGoogle Scholar
  45. Vilagrosa A, Morales F, Abadía A, Bellot J, Cochard H, Gil-Pelegrin E (2010) Are symplast tolerance to intense drought conditions and xylem vulnerability to cavitation coordinated? An integrated analysis of photosynthetic, hydraulic and leaf level processes in two Mediterranean drought-resistant species. Environ Exp Bot 69:233–242CrossRefGoogle Scholar
  46. Vilagrosa A, Chirino E, Peguero-Pina JJ, Barigah TS, Cochard Gil-Pelegrín E (2012) Xylem cavitation and embolism in plants living in water-limited ecosystems. In: Aroca R (ed) 2012. Plant responses to drought stress, Springer, Berlin-Heidelberg, pp 63–109Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • R. García de la Serrana
    • 1
  • A. Vilagrosa
    • 1
  • J. A. Alloza
    • 2
  1. 1.Fundación CEAM, Joint Research Unit University of Alicante-CEAM, Univ. AlicanteAlicanteSpain
  2. 2.Fundación CEAMValenciaSpain

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