Contrasting impacts of continuous moderate drought and episodic severe droughts on the aboveground‐biomass increment and litterfall of three coexisting Mediterranean woody species

Climate change is predicted to increase the aridity in the Mediterranean Basin and severely affect forest productivity and composition. The responses of forests to different timescales of drought, however, are still poorly understood because extreme and persistent moderate droughts can produce nonlinear responses in plants. We conducted a rainfall-manipulation experiment in a Mediterranean forest dominated by Quercus ilex, Phillyrea latifolia, and Arbutus unedo in the Prades Mountains in southern Catalonia from 1999 to 2014. The experimental drought significantly decreased forest aboveground-biomass increment (ABI), tended to increase the litterfall, and decreased aboveground net primary production throughout the 15 years of the study. The responses to the experimental drought were highly species-specific. A. unedo suffered a significant reduction in ABI, Q. ilex experienced a decrease during the early experiment (1999-2003) and in the extreme droughts of 2005-2006 and 2011-2012, and P. latifolia was unaffected by the treatment. The drought treatment significantly increased branch litterfall, especially in the extremely dry year of 2011, and also increased overall leaf litterfall. The drought treatment reduced the fruit production of Q. ilex, which affected seedling recruitment. The ABIs of all species were highly correlated with SPEI in early spring, whereas the branch litterfalls were better correlated with summer SPEIs and the leaf and fruit litterfalls were better correlated with autumn SPEIs. These species-specific responses indicated that the dominant species (Q. ilex) could be partially replaced by the drought-resistant species (P. latifolia). However, the results of this long-term study also suggest that the effect of drought treatment has been dampened over time, probably due to a combination of demographic compensation, morphological and physiological acclimation, and epigenetic changes. However, the structure of community (e.g., species composition, dominance, and stand density) may be reordered when a certain drought threshold is reached.

[1]  Influence of drought on tree rings and tracheid features of Pinus nigra and Pinus sylvestris in a mesic Mediterranean forest , 2012, European Journal of Forest Research.

[2]  S. Zegelin,et al.  Improved field probes for soil water content and electrical conductivity measurement using time domain reflectometry , 1989 .

[3]  S. Rambal,et al.  Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought , 2011, Oecologia.

[4]  J. Peñuelas,et al.  Comparative study of diurnal and nocturnal sap flow of Quercus ilex and Phillyrea latifolia in a Mediterranean holm oak forest in Prades (Catalonia, NE Spain) , 2012, Trees.

[5]  J. Peñuelas,et al.  Responses of terrestrial ecosystems to temperature and precipitation change: a meta‐analysis of experimental manipulation , 2011 .

[6]  J. Peñuelas,et al.  Large-scale recruitment limitation in Mediterranean pines: the role of Quercus ilex and forest successional advance as key regional drivers , 2014 .

[7]  Marianne E. Porter,et al.  Differential tree mortality in response to severe drought: evidence for long‐term vegetation shifts , 2005 .

[8]  S. Rambal,et al.  Long‐term transpiration change with rainfall decline in a Mediterranean Quercus ilex forest , 2009 .

[9]  S. Vicente‐Serrano,et al.  A Multiscalar Drought Index Sensitive to Global Warming: The Standardized Precipitation Evapotranspiration Index , 2009 .

[10]  J. Peñuelas,et al.  Foliar CO₂ in a holm oak forest subjected to 15 years of climate change simulation. , 2014, Plant science : an international journal of experimental plant biology.

[11]  J. Peñuelas,et al.  Species-specific drought effects on flower and fruit production in a Mediterranean holm oak forest , 2007 .

[12]  Marco A. Lara,et al.  Climate extremes initiate ecosystem‐regulating functions while maintaining productivity , 2011 .

[13]  F. Bussotti,et al.  Leaf shedding, crown condition and element return in two mixed holm oak forests in Tuscany, central Italy , 2003 .

[14]  W. Davis,et al.  The Combined Effects of , 1957 .

[15]  P. Ciais,et al.  Europe-wide reduction in primary productivity caused by the heat and drought in 2003 , 2005, Nature.

[16]  C. Beierkuhnlein,et al.  Effects of Extreme Weather Events on Plant Productivity and Tissue Die-Back are Modified by Community Composition , 2008, Ecosystems.

[17]  Jeffrey Q. Chambers,et al.  TROPICAL FORESTS : AN EVALUATION AND SYNTHESIS OF EXISTING FIELD DATA , 2022 .

[18]  Michael Obersteiner,et al.  Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe , 2013, Nature Communications.

[19]  J. Espelta,et al.  Increased drought reduces acorn production in Quercus ilex coppices: thinning mitigates this effect but only in the short term , 2011 .

[20]  J. Peñuelas,et al.  Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought , 2011, Proceedings of the National Academy of Sciences.

[21]  K. Price,et al.  Regional vegetation die-off in response to global-change-type drought. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  I. Oliveras,et al.  Xylem hydraulic properties of roots and stems of nine Mediterranean woody species , 2002, Oecologia.

[23]  Jordi Sardans,et al.  Evidence of current impact of climate change on life: a walk from genes to the biosphere , 2013, Global change biology.

[24]  Rasmus Fensholt,et al.  Drought footprint on European ecosystems between 1999 and 2010 assessed by remotely sensed vegetation phenology and productivity , 2014, Global change biology.

[25]  R. R. Odriguez-Cortin.  Long-term transpiration change with rainfall decline in a Mediterranean Quercus ilex forest , 2009 .

[26]  J. Peñuelas,et al.  Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. , 2014, Plant biology.

[27]  J. Peñuelas,et al.  The combined effects of a long‐term experimental drought and an extreme drought on the use of plant‐water sources in a Mediterranean forest , 2015, Global change biology.

[28]  Sara Taskinen,et al.  smatr 3– an R package for estimation and inference about allometric lines , 2012 .

[29]  Peter A. Troch,et al.  Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought , 2009, Proceedings of the National Academy of Sciences.

[30]  Josep Peñuelas,et al.  Complex spatiotemporal phenological shifts as a response to rainfall changes. , 2004, The New phytologist.

[31]  C. Field,et al.  The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off , 2011, Proceedings of the National Academy of Sciences.

[32]  E. García,et al.  Resource manipulation reveals flexible allocation rules to growth and reproduction in a Mediterranean evergreen oak , 2014 .

[33]  F. Chapin,et al.  The impacts of climate change on ecosystem structure and function , 2013 .

[34]  D. Clark,et al.  Field‐quantified responses of tropical rainforest aboveground productivity to increasing CO2 and climatic stress, 1997–2009 , 2013 .

[35]  Stewart J. Cohen,et al.  Climate Change 2014: Impacts,Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change , 2014 .

[36]  B. Emmett,et al.  Response of plant species richness and primary productivity in shrublands along a north–south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003 , 2007 .

[37]  N. McDowell,et al.  Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? , 2008, The New phytologist.

[38]  S. Rambal,et al.  Phenological responses to extreme droughts in a Mediterranean forest , 2011 .

[39]  S. Vicca,et al.  Do global change experiments overestimate impacts on terrestrial ecosystems? , 2011, Trends in ecology & evolution.

[40]  V. Potop.  Evolution of drought severity and its impact on corn in the Republic of Moldova , 2011 .

[41]  Markus Reichstein,et al.  The European carbon balance. Part 3: forests , 2010 .

[42]  Y. Malhi,et al.  The allocation of ecosystem net primary productivity in tropical forests , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[43]  C. Wirth,et al.  Reconciling Carbon-cycle Concepts, Terminology, and Methods , 2006, Ecosystems.

[44]  S. Seneviratne,et al.  Drought and ecosystem carbon cycling , 2011 .

[45]  J. Lopez-Bustins,et al.  Future variability of droughts in three Mediterranean catchments , 2013, Natural Hazards.

[46]  S. Running,et al.  Impacts of climate change on natural forest productivity – evidence since the middle of the 20th century , 2006 .

[47]  B. Emmett,et al.  Nonintrusive Field Experiments Show Different Plant Responses to Warming and Drought Among Sites, Seasons, and Species in a North–South European Gradient , 2004, Ecosystems.

[48]  C. Azorín-Molina,et al.  Performance of Drought Indices for Ecological, Agricultural, and Hydrological Applications , 2012 .

[49]  J. Peñuelas,et al.  Leaf mass per area ratio in Quercus ilex leaves under a wide range of climatic conditions. The importance of low temperatures , 2007 .

[50]  J. Peñuelas,et al.  Dampening effects of long‐term experimental drought on growth and mortality rates of a Holm oak forest , 2013, Global change biology.

[51]  Xiao Zhang,et al.  Impacts of Climate Change , 2007 .

[52]  Mark C. Vanderwel,et al.  Methods to estimate aboveground wood productivity from long-term forest inventory plots , 2014 .

[53]  Forest Isbell,et al.  Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory , 2012, Proceedings of the National Academy of Sciences.

[54]  Xavier Pons,et al.  Reassessing global change research priorities in mediterranean terrestrial ecosystems: how far have we come and where do we go from here? , 2015 .

[55]  A. Nardini,et al.  Global convergence in the vulnerability of forests to drought , 2012, Nature.

[56]  F. D. Pineda,et al.  Forest composition in Mediterranean mountains is projected to shift along the entire elevational gradient under climate change , 2012 .

[57]  Anja Rammig,et al.  A plant's perspective of extremes: terrestrial plant responses to changing climatic variability , 2013, Global change biology.

[58]  M. Battaglia,et al.  Wood properties in a long-lived conifer reveal strong climate signals where ring-width series do not. , 2013, Tree physiology.

[59]  Kevin Marsh,et al.  Erratum: Corrigendum: The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody , 2013 .

[60]  Josep Peñuelas,et al.  Comparative field study of Quercus ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions , 2003 .

[61]  M. Estiarte,et al.  Experimental evidence of reduced diversity of seedlings due to climate modification in a Mediterranean‐type community , 2004 .

[62]  A. Dai.  Increasing drought under global warming in observations and models , 2013 .

[63]  Maosheng Zhao,et al.  Drought-Induced Reduction in Global Terrestrial Net Primary Production from 2000 Through 2009 , 2010, Science.

[64]  S. Rambal,et al.  Mast seeding under increasing drought: results from a long-term data set and from a rainfall exclusion experiment. , 2010, Ecology.

[65]  J. Peñuelas,et al.  Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought , 2007, Plant Ecology.

[66]  J. Peñuelas,et al.  Contrasting foliar responses to drought in Quercus ilex and Phillyrea latifolia , 2006, Biologia Plantarum.

[67]  Jianping Huang,et al.  Evolution of land surface air temperature trend , 2014 .

[68]  Thomas Wohlgemuth,et al.  Precipitation manipulation experiments--challenges and recommendations for the future. , 2012, Ecology letters.

[69]  S. Rambal,et al.  The temporal response to drought in a Mediterranean evergreen tree: comparing a regional precipitation gradient and a throughfall exclusion experiment , 2013, Global change biology.

[70]  W. R. Whalley.  Considerations on the use of time‐domain reflectometry (TDR) for measuring soil water content , 1993 .

[71]  Sergio M. Vicente-Serrano,et al.  Response of vegetation to drought time-scales across global land biomes , 2012, Proceedings of the National Academy of Sciences.

[72]  J. Peñuelas,et al.  Sap flow of three co-occurring Mediterranean woody species under varying atmospheric and soil water conditions. , 2003, Tree physiology.

[73]  J. Iriondo,et al.  Extreme climatic events and vegetation: the role of stabilizing processes , 2012 .