Abstract
Episodes of drought-induced tree dieback have been recently observed in many forest areas of the world, particularly at the dry edge of species distributions. Under climate change, those effects could signal potential vegetation shifts occurring over large geographical areas, with major impacts on ecosystem form and function. In this article, we studied the effect of a single drought episode, occurred which in summer 2005, on a Scots pine population in central Pyrenees (NE Spain). Our main objective was to study the environmental correlates of forest decline and vegetation change at the plot level. General and generalized linear models were used to study the relationship between canopy defoliation, mortality and recruitment, and plot characteristics. A drought-driven multifactor dieback was observed in the study forest. Defoliation and mortality were associated with the local level of drought stress estimated at each plot. In addition, stand structure, soil properties, and mistletoe infection were also associated with the observed pattern of defoliation, presumably acting as long-term predisposing factors. Recruitment of Scots pine was low in all plots. In contrast, we observed abundant recruitment of other tree species, mostly Quercus ilex and Q. humilis, particularly in plots where Scots pine showed high defoliation and mortality. These results suggest that an altitudinal upwards migration of Quercus species, mediated by the dieback of the currently dominant species, may take place in the studied slopes. Many rear-edge populations of Scots pine sheltered in the mountain environments of the Iberian Peninsula could be at risk under future climate scenarios.
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References
Allen CD, Breshears DD. 1998. Drought-induced shift of a forest-woodland ecotone: Rapid landscape response to climate variation. Ecology 95:14839–42.
Allen RG, Pereira LS, Raes D. 1998. Crop evapotranspiration—Guidelines for computing crop water requirements. FAO Irrigation and drainage paper, No. 56. Italy: Rome.
Allen CD, Macalady A, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Gonzales P, Hogg T, Rigling A, Breshears DD, Fensham R, Zhang Z, Kitzberger T, Lim JH, Castro J, Running SW, Allard G, Semerci A, Cobb N. 2010. Climate-induced forest mortality: a global overview of emerging risks. For Ecol Manag. doi:10.1016/j.foreco.2009.09.001.
Auclair AND. 1993. Extreme climatic fluctuations as a cause of forest dieback in the Pacific Rim. Water Air Soil Pollut 66:207–29.
Aukema JE, Martínez del Rio C. 2002. Where does a fruit-eating bird deposit mistletoe seeds? Seed deposition patterns and an experiment. Ecology 83(12):3489–96.
Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F. 1998. Pines of the Mediterranean Basin. In: Richardson DM, Ed. Ecology and biogeography of Pinus. Cambridge: Cambridge University Press. pp 153–70.
Beven K, Kirkby MJ. 1979. A physically based variable contributing area model of basin hydrology. Hydrol Sci Bull 24(1):43–69.
Bigler C, Bräker OU, Bugmann H, Dobbertin M, Rigling A. 2006. Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9:330–43.
Bravo-Oviedo A, Sterba H, Río M, Bravo F. 2005. Competition-induced mortality for Mediterranean Pinus pinaster Ait and Pinus sylvestris L. For Ecol Manag 222:88–98.
Bréda N, Badeau V. 2008. Forest tree responses to extreme drought and some biotic events: towards a selection according to hazard tolerance? CR Geosci 340:651–62.
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 63:625–44.
Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JH, 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 USA (PNAS) 102(42):15144–8.
Briones O, Montaña C, Ezcurra E. 1998. Competition intensity as a function of resource availability in a semiarid ecosystem. Oecologia 116:365–72.
Broadmeadow MSJ, Jackson SB. 2000. Growth responses of Quercus petraea, Fraxinus excelsior and Pinus sylvestris to elevated carbon dioxide, ozone and water supply. New Phytol 146:437–51.
Callaway RM, Walker LR. 1997. Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78(7):1958–65.
Camarero JJ, Padró A, Martín E, Gil-Peregrín E. 2002. Aproximación dendroecológica al decaimiento del abeto (Abies alba Mill.) en el Pirineo aragonés. Montes 70:26–33.
Castro J. 1999. Seed mass versus seedling performance in Scots pine: a maternally dependent trait. New Phytol 144:153–61.
Castro J, Zamora R, Hódar JA, Gómez JM. 2004. Seedling establishment of a boreal tree species (Pinus sylvestris) at its southernmost distribution limit: consequences of being in a marginal Mediterranean habitat. J Ecol 92:266–77.
Castroviejo S, Lainz M, López González G, Montserrat P, Muñoz Garmendia F, Paiva J, Villar L, Eds. 1986. Flora ibérica: plantas vasculares de la Península Ibérica e Islas Baleares, Vol. 1. Madrid: C.S.I.C.
Ceballos L, Ruiz de la Torre J. 1971. Árboles y Arbustos de la España Peninsular. Madrid: Instituto Forestal de Investigaciones y Experiencias.
Chen HYH, Fu S, Monserud RA, Gillies IC. 2008. Relative size and stand age determine Pinus banksiana mortality. For Ecol Manag 255:3980–4.
Clark PJ, Evans FC. 1954. Distances to nearest neighbour as a measure of spatial relationships in populations. Ecology 35:445–53.
Condit R. 1998. Ecological implications of changes in drought patterns: shifts in forest composition in Panama. Clim Change 39(2–3):413–27.
Connell JH. 1978. Diversity in tropical rain forests and coral reefs. Science 199(4335):1302–10.
Croisé L, Lieutier F. 1993. Effects of drought on the induced defence reaction of Scots pine to bark beetle-associated fungi. Ann Sci For 50:91–7.
Das AJ, Battles JJ, Stephenson NL, van Mantgem PJ. 2007. The relationship between tree growth patterns and likelihood of mortality: a study of two tree species in the Sierra Nevada. Can J For Res 37:580–97.
Dobbertin M. 1999. Relating defoliation and its causes to premature tree mortality. In: Forster B, Knizek M, Grodzki W, Eds. Methodology of forest insect and disease survey in Central Europe. Proceedings of the second workshop of the IUFRO WP, Sion-Chateauneuf, Switzerland. Birmensdorf: Swiss Federal Institute for Forest, Snow and Landscape (WSL). pp 215–220.
Dobbertin M, Brang P. 2001. Crown defoliation improves tree mortality models. For Ecol Manag 141(3):271–84.
Dobbertin M, Rigling A. 2006. Pine mistletoe (Viscum album ssp austriacum) contributes to Scots pine (Pinus sylvestris) mortality in the Rhone valley of Switzerland. For Pathol 36:309–22.
Dobbertin M, Wermelinger B, Bigler C, Bürgi M, Carron M, Forster B, Gimmi U, Rigling A. 2007. Linking increasing drought stress to Scots Pine mortality and bark beetle infestations. Sci World J 7(S1):231–9.
Dunn JP, Potter DA, Kimmerer TW. 1990. Carbohydrate reserves, radial growth and mechanisms of resistance of oak trees to phloem-boring insects. Oecologia 83:458–68.
Ehleringer JR, Marshall JD. 1995. Water relations. In: Press MC, Graves JD, Eds. Parasitic plants. London: Chapman & Hall.
European Environment Agency (EEA). 2008. Impacts of Europe’s changing climate—2008 indicator-based assessment. European Environment Agency summary, report No. 4. Copenhagen: European Environment Agency.
Faraway JJ. 2006. Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. Boca Raton (FL): Chapman and Hall.
Fischer JT. 1983. Water relations of mistletoes and their hosts. In: Calder M, Bernhard T, Eds. The biology of mistletoes. Sydney: Academic Press. p 163–84.
Franklin JF, Shugart HH, Harmon ME. 1987. Tree death as an ecological process: the causes, consequences and variability of tree mortality. Bio-Science 37:550–6.
García-Ruiz JM, Lasanta T, Ruiz-Flano P, Ortigosa L, White S, González C, Martí C. 1996. Land-uses changes and sustainable development in mountain areas: a case study in the Spanish Pyrenees. Landsc Ecol 11(5):267–77.
Grayson RB, Western AW, Chiew FHS, Blöschl G. 1997. Preferred states in spatial soil moisture patterns: local and nonlocal controls. Water Resour Res 33(12):2897–908.
Grayson R, Western A, Wilson D, Young R, McMahon T, Woods R, Duncan M, Blöschl G. 1999. Measurement and interpretation of soil moisture for hydrological applications. Water 99: Joint Congress. Brisbane: IE Aust. pp 5–9.
Guarín H, Taylor AH. 2005. Drought triggered tree mortality in mixed conifer forests in Yosemite National Park, California, USA. For Ecol Manag 218:229–44.
Hacke UG, Sperry JS, Ewers BE, Ellsworth DS, Schäfer KVR, Oren R. 2000. Influence of soil porosity on water use in Pinus taeda. Oecologia 124:495–505.
Hampe A, Petit RJ. 2005. Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–7.
Hargreaves GH, Samani ZA. 1985. Reference crop evapotranspiration from temperature. Appl Eng Agric 1(2):96–9.
Hegyi F. 1974. A simulation model for managing jackpine stands. In: Fries J, Ed. Growth models for tree and stand simulation. Stockholm: Royal College of Forestry. p 74–90.
Hódar JA, Castro J, Zamora R. 2003. Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biol Conserv 110:123–9.
Hubbell SP, Foster RB. 1986. Canopy gaps and the dynamics of a neotropical forest. In: Crawley MJ, Ed. Plant ecology. Oxford: Blackwell Scientific Publications. p 77–96.
Hultine KR, Koepke DF, Pockman WT, Fravolini A, Sperry JS, Williams DG. 2005. Influence of soil texture on hydraulic properties and water relations of a dominant warm-desert phreatophyte. Tree Physiol 26:313–23.
IPCC. 2007. Climate change 2007: the physical science basis. Contribution of Working Group I to the forth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press. p 1009.
Karlsson PS, Nordell KO. 1987. Growth of Betula pubescens and Pinus sylvestris seedlings in a subartic environment. Funct Ecol 1(1):37–44.
Keeley JE, Zedler PH. 1998. Evolution of life histories in Pinus. In: Richardson DM, Ed. Ecology and biogeography of Pinus. Cambridge: Cambridge University Press. p 153–70.
Kelly AE, Goulden ML. 2008. Rapid shifts in plant distribution with recent climate change. Proc Natl Acad Sci USA (PNAS) 105(33):11823–6.
Kenkel NC. 1988. Pattern of self-thinning in Jack pine: testing the random mortality hypothesis. Ecology 69(4):1017–24.
Linares JC, Camarero JJ, Carreira JA. 2009. Interacting effects of changes in climate and forest cover on mortality and growth of the southernmost European fir forests. Glob Ecol Biogeogr 18:485–97.
Lloret F, Siscart D, Dalmases C. 2004. Canopy recovery after drought dieback in holm-oak Mediterranean forests of Catalonia (NE Spain). Glob Change Biol 10:2092–9.
Manion PD. 1991. Tree disease concepts. Upper Saddle River (NJ): Prentice Hall.
Marañón T, Zamora R, Villar R, Zavala MA, Quero JL, Pérez-Ramos I, Mendoza I, Castro J. 2004. Regeneration of tree species and restoration under contrasted Mediterranean habitats: field and glasshouse experiments. Int J Ecol Environ Sci 30(3):187–96.
Martínez-García F. 1999. Los bosques de Pinus sylvestris L. del Sistema Central español. Distribución, història, composición florística y tipología. PhD thesis. Universidad Complutense de Madrid, Madrid, Spain.
Martínez-Vilalta J, Piñol J. 2002. Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For Ecol Manag 161:247–56.
Mathiasen RL, Nickrent DL, Shaw DC, Watson DM. 2008. Mistletoes: pathology, systematics, ecology and management. Plant Dis 92(7):988–1006.
Mattson WJ, Haack RA. 1987. The role of drought in outbreaks of plant-eating insects. Bioscience 37(2):110–18.
McDowell N, 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(4):719–39.
Millar CI, Stephenson NL, Stephens SL. 2007. Climate change and forests of the future: managing in the face of uncertainty. Ecol Appl 17(8):2145–51.
Mueller RC, Scudder CM, Porter ME, Trotter RTIII, Gehring CA, Whitham TG. 2005. Differential tree mortality in response to severe drought: evidence for long-term vegetation-shifts. J Ecol 93:1085–93.
Mutke S, Gordo J, Gil L. 2005. Variability of Mediterranean Stone pine cone production: yield loss as response to climate change. Agric For Meteorol 132:263–72.
Negrón JF, McMillin JD, Anhold JA, Coulson D. 2009. Bark beetle-caused mortality in a drought-affected ponderosa pine landscape in Arizona, USA. For Ecol Manag 257:1353–62.
Ninyerola M, Pons X, Roure JM. 2000. A methodological approach of climatological modelling of air temperature and precipitation through GIS techniques. Int J Climatol 20:1823–41.
O’Loughlin EM. 1986. Predictions of surface saturation zones in natural catchments by topographic analysis. Water Resour Res 22:794–804.
Oberhuber W. 2001. The role of climate in the mortality of Scots pine (Pinus sylvestris L.) exposed to soil dryness. Dendrochronologia 19:45–55.
Pedersen BS. 1998. The role of stress in the mortality of Midwestern oaks as indicated by growth prior to death. Ecology 79:79–93.
Peet RK, Christensen NL. 1987. Competition and tree death. Bioscience 37(8):586–95.
Peñuelas J, Boada M. 2003. A global change-induced biome shift in the Montseny mountains (NE Spain). Glob Change Biol 9:131–40.
Pigott CD, Pigott S. 1993. Water as a determinant of the distribution of trees at the boundary of the Mediterranean zone. J Ecol 81:557–66.
Pons X. 1996. Estimación de la Radiación Solar a partir de modelos digitales de elevaciones. Propuesta metodológica. In: Juaristi J, Moro I, Eds. VII Coloquio de Geografía Cuantitativa, Sistemas de Información Geográfica y Teledetección. Spain: Vitoria-Gasteiz.
Poyatos R, Latron J, Llorens P. 2003. Land use and land cover change after agricultural abandonment. The case of a Mediterranean Mountain area (Catalan Pre-Pyrenees). Mt Res Dev 23(4):362–8.
Press MC, Graves JD, Stewart GR. 1988. Transpiration and carbon acquisition in root hemiparasitic angiosperms. J Exp Bot 39(8):1009–14.
Pugnaire FI, Armas C, Tirado R. 2000. Balance de las interacciones entre plantas en ambientes mediterráneos. In: Zamora R, Pugnaire FI, Eds. Ecosistemas mediterráneos Análisis funcional. Granada: C.S.I.C.-A.E.E.T. p 213–35.
Rebetez M, Dobbertin M. 2004. Climate change may already threaten Scots pine stands in the Swiss Alps. Theor Appl Climatol 79:1–9.
Reich PB, Oleksyn J, Tjoelker MG. 1994. Seed mass effects on germination and growth of diverse European Scots pine populations. Can J For Res 24:306–20.
Rice KJ, Matzner SL, Byer W, Brown JR. 2004. Patterns of tree dieback in Queensland, Australia: the importance of drought stress and the role of resistance to cavitation. Oecologia 139:190–8.
Sack L, Grubb PJ. 2002. The combined impacts of deep shade and drought on the growth and biomass allocation of shade-tolerant woody seedlings. Oecologia 131:175–85.
Saxton KE, Rawls WJ, Romberger JS, Papendick RI. 1986. Estimating generalized soil-water characteristics from texture. Soil Sci Soc Am J 50:1031–6.
Schaffer B, Hawksworth FG, Jacobi WR. 1983. Effects of Comandra Blister Rust and Dwarf Mistletoe on cone and seed production of Lodgepole Pine. Plant Dis 67:215–17.
Schultz RC, Gatherum GE. 1971. Photosynthesis and distribution of assimilate of Scotch pine seedlings in relation to soil moisture and provenance. Bot Gazette 132(2):91–6.
Singh P, Carew GC. 1989. Impact of eastern dwarf mistletoe in black spruce forests of Newfoundland. Eur J For Pathol 19(5–6):305–22.
Slik JWF. 2004. El Niño droughts and their effects on tree species composition and diversity in tropical rain forests. Oecologia 141:114–20.
Smith TF, Rizzo DM, North M. 2005. Patterns of mortality in an old-growth mixed-conifer forest of the southern Sierra Nevada, California. For Sci 51(3):266–75.
Sperry JS, Hacke UG. 2002. Desert shrub water relations with respect to soil characteristics and plant functional type. Funct Ecol 16:367–78.
Sperry JS, Adler FR, Campbell GS, Comstock JP. 1998. Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ 21:347–59.
Stephenson NL. 1990. Climatic control of vegetation distribution: the role of water balance. Am Nat 135:649–70.
Strong GL, Bannister P. 2002. Water relations of temperate mistletoes on various hosts. Funct Plant Biol 29(1):89–96.
Suarez ML, Kitzberger T. 2008. Recruitment patterns following a severe drought: long-term compositional shifts in Patagonian forests. Can J For Res 38:3002–10.
Van Mantgem PJ, Stephenson NL. 2007. Apparent climatically induced increase of tree mortality rates in a temperate forest. Ecol Lett 10:909–16.
Van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fulé PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH, Veblen TT. 2009. Widespread increase of tree mortality rates in the western United States. Science 323:521–4.
Waring RH. 1987. Characteristics of trees predisposed to die. Bioscience 37(8):569–74.
Western AW, Grayson RB, Blöschl G. 2002. Scaling of soil moisture: a hydraulic perspective. Annu Rev Earth Planet Sci 30:149–80.
White GC, Bennetts RE. 1996. Analysis of frequency count data using the negative binomial distribution. Ecology 77(8):2549–57.
Williams DW, Liebhold AM. 2002. Climate change and the outbreak ranges of two North American bark beetles. Agric For Entomol 4:87–99.
Williamson GB, Laurance WF, Oliveira AA, Delamonica P, Gascon C, Lovejoy TE, Pohl L. 2000. Amazonia tree mortality during the 1997 El Niño drought. Conserv Biol 14:1538–42.
Worldwide Bioclimatic Classification System. 1996–2009. S.Rivas-Martinez & S.Rivas-Saenz, Phytosociological Research Center, Spain. http://www.globalbioclimatics.org.
Zlotin RI, Parmenter RR. 2008. Patterns of mast production in pinyon and juniper woodlands along a precipitation gradient in central New Mexico (Sevilleta National Wildlife Refuge). J Arid Environ 72(9):1562–72.
Acknowledgments
We would like to thank the Catalan Forest Service, and especially Carles Fañanàs Aguilera, for facilitating our field work and for their generous comments. We are also indebted to all the undergraduate students (Miriam, Albert, Nil, Joan) that were involved in this study. We appreciate helpful comments from Bernat Claramunt, Javier Retana, and Jofre Carnicer on the earlier version of the manuscript. This study was supported by the Spanish Ministry of Education and Sciences via competitive projects CGL2006-01293, CGL2007-60120, and CSD2008-0004. LG was supported by an FPI scholarship from the Spanish Ministry of Education and Sciences.
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Lucía Galiano conceived of or designed study, performed research, analyzed data, contributed new methods or models, wrote the paper; Jordi Martínez-Vilalta conceived of or designed study, contributed new methods or models; Francisco Lloret conceived of or designed study, contributed new methods or models.
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Supplementary Figure s1
Size (DBH) class distribution of the studied Scots pine population. N = 1002 (Tif 8940 kb)
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Average seedling abundance of all species found in the study at the plot level (Tif 8904 kb)
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Galiano, L., Martínez-Vilalta, J. & Lloret, F. 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 (2010). https://doi.org/10.1007/s10021-010-9368-8
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DOI: https://doi.org/10.1007/s10021-010-9368-8