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Physiological and structural changes in response to altered precipitation regimes in a Mediterranean macchia ecosystem

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Abstract

Significant decrease in precipitation up to 15–20% has been observed in the Mediterranean area in the last two decades as a consequence of climate change. To simulate an analogous scenario, the precipitation regime was altered in replicated experimental plots in a Mediterranean macchia dominated by Arbutus unedo L. species. Two different levels of soil water content (SWC) were obtained during the summer: a mean value of 7% was obtained in water-depleted (D) plots by a partial (−20%) rain exclusion treatment using rain gutters; while a mean value of 14% in SWC was obtained in watered (W) plots supplying water by a sprinkler net. The physiological and structural changes were investigated over the course of two consecutive years by measurement of water potential, gas exchange leaf carbon isotopes, leaf pigments and growth. Apart from short-term responses, mainly related to the elastic response of stomatal conductance to soil water, a more long-lasting and significant acclimation to water availability was observed as a result of the increase in hydraulic resistance in the soil–plant continuum, which persisted even after the return to full water availability during the fall and winter. This response involved the permanent down-regulation of stomatal conductance and photosynthesis, accumulation of photo-protective pigments, as well as a reduction in shoot growth, leaf area index and an increase in shoot-bearing flowers in D plots. This acclimation response prevented the onset of any run-away damage thereby reducing the forest vulnerability to drought. Furthermore, the imposed drought induced a slight increase or no change in intrinsic water-use efficiency (WUEint), as a result of the parallel increase in stomatal and non-stomatal limitations; conversely integrated WUE (i.e., estimated from leaf carbon isotopes) was not affected by drought.

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References

  • Acherar M, Rambal S, Lepart J (1991) Évolution du potentiel hydrique foliaire et de la conductance stomatique de quatre chênes méditerranéens lors d’une période de dessèchement. Ann Sci For 48(5):561–573. doi:10.1051/forest:19910506

    Article  Google Scholar 

  • Aussenac G, Valette JC (1982) Comportement hydrique estival de Cedrus atlantica Manetti, Quercus ilex L., Quercus pubescens Willd. et de divers pins dans le Mont Ventoux. Ann Sci For 39(1):41–62. doi:10.1051/forest:19820103

    Article  Google Scholar 

  • Baraldi R, Canaccini F, Cortes S, Magnani F, Rapparini F, Zamboni A, Raddi S (2008) Role of xanthophyll cycle-mediated photoprotection in Arbutus unedo plants exposed to water stress during Mediterranean summer. Photosynthesis 46(3):378–386. doi:10.1007/s11099-008-0069-x

    Article  CAS  Google Scholar 

  • Borghetti M, Cinnirella S, Magnani F, Saracino A (1998) Impact of long-term drought on xylem embolism and growth in Pinus halepensis Mill. Trees (Berl) 12:187–195

    Google Scholar 

  • Boyer JS (1982) Plant productivity and environment potential for increasing crop plant productivity, genotypic selection. Science 218:443–448. doi:10.1126/science.218.4571.443

    Article  PubMed  Google Scholar 

  • Bunce JA (1996) Growth at elevated carbon dioxide concentration reduces hydraulic conductance in alfalfa and soybean. Glob Change Biol 2:155–158. doi:10.1111/j.1365-2486.1996.tb00061.x

    Article  Google Scholar 

  • Castell C, Terradas J, Tenhunen JD (1994) Water relations, gas exchange, and growth of resprouts and mature plant shoots of Arbutus unedo L. and Quercus ilex L. Oecologia 98:201–211. doi:10.1007/BF00341473

    Article  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264. doi:10.1071/FP02076

    Article  CAS  Google Scholar 

  • Churkina G, Running SW (1998) Contrasting climatic controls on the estimated productivity of global terrestrial biomes. Ecosystems (N Y, Print) 1:206–215. doi:10.1007/s100219900016

  • Cinnirella S, Magnani F, Saracino A, Borghetti M (2002) Response of a mature Pinus laricio plantation to a three-year restriction of water supply: structural and functional acclimation to drought. Tree Physiol 22:21–30

    PubMed  Google Scholar 

  • Cochard H (1992) Vulnerability of several conifers to air embolism. Tree Physiol 11:73–83

    PubMed  Google Scholar 

  • Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Symp Soc Exp Biol 31:471–505

    PubMed  CAS  Google Scholar 

  • De Dato G, Pellizzaro G, Cesaraccio C, Sirca C, De Angelis P, Duce P, Spano D, Scarascia Mugnozza G (2008) Effects of warmer and drier climate conditions on plant composition and biomass production in a Mediterranean shrubland community. iForest 1:39–48 [online: Feb 28, 2008] URL:http://www.sisef.it/iforest/

    Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xantophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26. doi:10.1016/S1360-1385(96)80019-7

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW III, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. J Plant Physiol 22:249–260

    CAS  Google Scholar 

  • Dewar RC (1997) A simple model of light and water use evaluated for Pinus radiata. Tree Physiol 17:259–265

    PubMed  Google Scholar 

  • Ewers BE, Oren R, Sperry JS (2000) Influence of nutrient versus water supply on hydraulic architecture and water balance in Pinus taeda. Plant Cell Environ 23:1055–1066. doi:10.1046/j.1365-3040.2000.00625.x

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosyntheis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. doi:10.1146/annurev.pp.40.060189.002443

    Article  CAS  Google Scholar 

  • Fernández M, Gil L, Pardos JA (2000) Effects of water supply on gas exchange in Pinus pinaster Ait. Provenances during their first growing season. Ann Sci 57:9–16. doi:10.1051/forest:2000107

    Article  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inibition of photosynthesis in C3 plants: stomatal and non-stomatal limitation revisited. Ann Bot (Lond) 89:183–189. doi:10.1093/aob/mcf027

    Article  CAS  Google Scholar 

  • Frazer GW, Fournier JA, Trofymow Hall RJ (2001) A comparison of digital and film fisheye photography for analysis of forest canopy structure and gap light transmission. Agric For Meteorol 109(4):249–263. doi:10.1016/S0168-1923(01)00274-X

    Article  Google Scholar 

  • Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93. doi:10.1111/j.1469-8137.2007.02087.x

    Article  PubMed  CAS  Google Scholar 

  • Gasco A, Nardini A, Gortan E, Salleo S (2006) Ion-mediated increase in the hydraulic conductivity of laurel stems: role of pits and consequences for the impact of cavitation on water transport. Plant Cell Environ 29:1946–1955. doi:10.1111/j.1365-3040.2006.01570.x

    Article  PubMed  CAS  Google Scholar 

  • Geiger DR, Servaites JC (1991) Carbon allocation and response to stress. In: Mooney HA, Winner WE, Pell EJ (eds) Response of plants to multiple stresses. Academic Press, San Diego, pp 103–127

    Google Scholar 

  • Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849. doi:10.1111/j.1365-3040.2005.01333.x

    Article  CAS  Google Scholar 

  • Grieu P, Guhel JM, Aussenac G (1988) The effects of soil and atmospheric drought on photosynthesis and stomatal control of gas exchange in three coniferous species. Physiol Plant 73:97–104. doi:10.1111/j.1399-3054.1988.tb09199.x

    Article  Google Scholar 

  • Gundersen P, Andersen BR, Beier C, Rasmussen L (1995) Experimental manipulations of water and nutrient input to a Norway spruce plantation at Klosterhede, Denmark. I. Unintended physical and chemical-changes by roof experiments. Plant Soil 168:601–611. doi:10.1007/BF00029374

    Article  Google Scholar 

  • Hanson PJ, Todd TE, Amtor JS (2001) A six-year study of sapling and large-tree on growth and mortality responses to natural and induced variability in precipitation and throughfall. Tree Physiol 21:345–358

    PubMed  CAS  Google Scholar 

  • Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121. doi:10.1046/j.1365-3040.2001.00660.x

    Article  Google Scholar 

  • IPCC (2001) Climate change 2001. In: Houghton JT (ed) The scientific basis. Cambridge University Press, Cambridge

    Google Scholar 

  • IPCC (2007) Climate change 2007: impacts, adaptation and vulnerability. Fourth Assessment Report. Summary for Policymakers. Working Group II

  • Irvine J, Perks MP, Magnani F, Grace J (1998) The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiol 18:393–402

    PubMed  Google Scholar 

  • Jarvis AJ, Davies WJ (1998) Modelling stomatal responses to soil and atmospheric drought. J Exp Bot 49:399–406. doi:10.1093/jexbot/49.suppl_1.399

    Article  Google Scholar 

  • Jefferies RA (1994) Drought and chlorophyll fluorescence in field-grown potato (Solanum tuberosum). Physiol Plant 90:93–97. doi:10.1111/j.1399-3054.1994.tb02197.x

    Article  CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. doi:10.1146/annurev.pp.42.060191.001525

    Article  CAS  Google Scholar 

  • Law BE, Goldstein AH, Anthoni PM, Unsworth MH, Panek JA, Bauer MR, Fracheboud JM, Hultman N (2001) Carbon dioxide and water vapor exchange by young and old ponderosa pine ecosystems during a dry summer. Tree Physiol 21(5):299–308

    PubMed  CAS  Google Scholar 

  • Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294. doi:10.1046/j.0016-8025.2001.00814.x

    Article  PubMed  CAS  Google Scholar 

  • Lebourgeois F, Levy G, Aussenac G, Clerc B, Willm F (1998) Influence of soil drying on leaf water potential, photosynthesis, stomatal conductance and growth in two black pine varieties. Ann Sci For 55(3):287–299. doi:10.1051/forest:19980302

    Article  Google Scholar 

  • Llorens L, Peñuelas J, Beier C, Emmett B, Estiarte M, Tietema A (2004a) Effects of an experimental increase of temperature and drought on the photosynthetic performance of two ericaceous shrub species along a north–south european gradient. Ecosystems (N Y, Print) 7:613–624. doi:10.1007/s10021-004-0180-1

    Article  CAS  Google Scholar 

  • Llorens L, Peñuelas J, Estiarte M, Bruna P (2004b) Contrasting growth changes in two dominant species of a Mediterranean shrubland submitted to experimental drought and warming. Ann Bot (Lond) 94:843–853. doi:10.1093/aob/mch211

    Article  Google Scholar 

  • Lloret F, Peñuelas J, Ogaya R (2004) Establishment of co-existing Mediterranean tree species under a varying soil moisture regime. J Veg Sci 15:237–244. doi:10.1658/1100-9233(2004)015[0237:EOCMTS]2.0.CO;2

    Article  Google Scholar 

  • Loreto F, Harley PC, Di Marco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by three different methods. Plant Physiol 98:1437–1443. doi:10.1104/pp.98.4.1437

    Article  PubMed  Google Scholar 

  • Martinez-Vilalta J, Mangiron M, Ogaya R, Sauret M, Serrano L, Peñuelas J, Piñol J (2003) Sap flow of three co-occurring Mediterranean trees under varying atmospheric and soil water conditions. Tree Physiol 23:747–758

    PubMed  Google Scholar 

  • Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182. doi:10.1046/j.1365-3040.2003.00991.x

    Article  Google Scholar 

  • Mencuccini M, Grace J (1995) Climate influences the leaf area/sapwood area ratio in Scots pine. Tree Physiol 15:1–10

    Article  PubMed  Google Scholar 

  • Müller M, Hernández I, Alegre L, Munné-Bosh S (2006) Enhanced α-tocopherol quinone levels and xanthophyll cycle de-epoxidation in rosemary plants exposed to water deficit during the Mediterranean winter. J Plant Physiol 163:601–606. doi:10.1016/j.jplph.2005.10.009

    Article  PubMed  CAS  Google Scholar 

  • Nemani RR, Keeling CD, Hashimoto H, Jolly WM, Piper SC, Tucker CJ, Myneni RB, Running SW (2003) Climate driven increases in global terrestrial net primary production from 1982 to 1999. Science 300:1560–1563. doi:10.1126/science.1082750

    Article  PubMed  CAS  Google Scholar 

  • Ogaya R, Peñuelas J (2003) Comparative field study of Quercus ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions. Environ Exp Bot 50(2):137–148. doi:10.1016/S0098-8472(03)00019-4

    Article  Google Scholar 

  • 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 189:291–299. doi:10.1007/s11258-006-9184-6

    Article  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from molecular mechanisms to the field. Bios Scientific, Oxford, pp 1–24

    Google Scholar 

  • Peñuelas J, Filella I, Lloret F, Siscart D, Piñol J (1998) Comparative field study of spring and summer leaf gas exchange and photobiology of the Mediterranean trees Quercus ilex and Phyllirea latifolia. J Exp Bot 49:229–238. doi:10.1093/jexbot/49.319.229

    Article  Google Scholar 

  • Rambal S, Ourcival JM, Joffre R, Mouillot F, Nouvellon Y, Reichstein M, Rocheteau A (2003) Drought controls over conductance and assimilation of a Mediterranean evergreen ecosystem: scaling from leaf to canopy. Glob Change Biol 9:1813–1824. doi:10.1111/j.1365-2486.2003.00687.x

    Article  Google Scholar 

  • Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386. doi:10.1046/j.0028-646X.2001.00334.x

    Article  CAS  Google Scholar 

  • Reichstein M, Tenhunen JD, Roupsard O, Ourcival JM, Rambal S, Miglietta F, Peressotti A, Pecchiari M, Tirone G, Valentini R (2002) Severe drought effects on ecosystem CO2 and H2O fluxes at three Mediterranean evergreen sites, revision of current hypothesis? Glob Change Biol 8:999–1017. doi:10.1046/j.1365-2486.2002.00530.x

    Article  Google Scholar 

  • Ripullone F, Lauteri M, Grassi G, Amato M, Borghetti M (2004) Variation in nitrogen supply changes water-use efficiency of Pseudotsuga menziesii and Populus × euroamericana; a comparison of three approaches to determine water-use efficiency. Tree Physiol 24:671–679

    PubMed  Google Scholar 

  • Ripullone F, Guerrieri MR, Magnani F, Nolè A, Borghetti M (2007) Stomatal conductance and leaf water potential responses to hydraulic conductance variation in Pinus pinaster seedlings. Trees (Berl) 21:371–378. doi:10.1007/s00468-007-0130-6

    Article  Google Scholar 

  • Saliendra NZ, Sperry JS, Comstock JP (1995) Influence of leaf water status on stomatal response to humidity, hydraulic conductance and soil drought in Betula occidentalis. Planta 196:357–366. doi:10.1007/BF00201396

    Article  CAS  Google Scholar 

  • Sarris D, Christodoulakis D, Körner C (2007) Recent decline in precipitation and tree growth in the eastern Mediterranean. Glob Change Biol 13:1187–1200. doi:10.1111/j.1365-2486.2007.01348.x

    Article  Google Scholar 

  • Saurer M, Siegwolf R (2007) Human impacts on tree-ring growth reconstructed from stable isotopes. In: Dawson TE, Siegwolf R (eds) Stable isotopes as indicators of ecological change terrestrial ecology series. Elsevier, Amsterdam, pp 49–62

    Chapter  Google Scholar 

  • Serrano L, Peñuelas J (2005) Contribution of physiological and morphological adjustments to drought resistance in two Mediterranean tree species. Biol Plant 49(4):551–559. doi:10.1007/s10535-005-0049-y

    Article  Google Scholar 

  • Sperry JS, Pockmann WT (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant Cell Environ 16:279–287. doi:10.1111/j.1365-3040.1993.tb00870.x

    Article  Google Scholar 

  • Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25(2):251–263. doi:10.1046/j.0016-8025.2001.00799.x

    Article  PubMed  Google Scholar 

  • 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 Bot 49:419–432. doi:10.1093/jexbot/49.suppl_1.419

    Article  Google Scholar 

  • Topp GC, Davis JL (1985) Time domain reflectometry (TDR) and its application to irrigation scheduling. In: Hillel D (ed) Advances in irrigation, vol 3. Academic Press, New York, pp 107–127

    Google Scholar 

  • Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Ann Rev Plant Physiol Mol Biol 40:19–38. doi:10.1146/annurev.pp.40.060189.000315

    Article  Google Scholar 

  • Uemura A, Ishida A, Tobias DJ, Koike N, Matsumoto Y (2004) Linkage between seasonal gas exchange and hydraulic acclimation in the top canopy leaves of Fagus trees in a mesic forest in Japan. Trees (Berl) 18:452–459. doi:10.1007/s00468-004-0328-9

    Article  Google Scholar 

  • Warren CR, Livingston NJ, Turpin DH (2004) Water stress decreases the transfer conductance of Douglas-fir (Pseudotsuga menziesii) seedlings. Tree Physiol 24:971–979

    PubMed  CAS  Google Scholar 

  • Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426. doi:10.1038/282424a0

    Article  Google Scholar 

  • Zunzunegui M, Fernandez Baco L, Diaz Barradas MC, Garcia Novo F (1999) Seasonal changes in photochemical efficiency in leaves of Halimium halimifolium, a Mediterranean semideciduous shrub. Photosynthetica 37(1):17–31. doi:10.1023/A:1007058611140

    Article  Google Scholar 

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Acknowledgments

This research was supported by the EU Project n. EKV2-CT-2002-00158 MIND (Mediterranean terrestrial ecosystem and Increasing Drought)—V° EU-Framework Programme—Environmental and Sustainable Development—Key action 2, Global change, climate and biodiversity and the MIUR-PRIN Project—prot. N. 2003073315_003 “Drought and Mediterranean forests: stomatal mechanisms in the regulation of plant gas exchanges”. The authors would like to thank the coordinator of the MIND project Dr. Franco Miglietta and Dr. Marco Pecchiari for the concession of SWC and precipitation data. The authors also express their gratitude to S. Cortes Ebner, P. Boldreghini, A. Lapolla, M. Anichini, L. Cantoni and G. Lupaldi for field work assistance.

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Authors and Affiliations

  1. Department of Crop System, Forestry and Environmental Sciences, University of Basilicata, Via dell’Ateneo Lucano, 10, 85100, Potenza, Italy

    Francesco Ripullone, Marco Borghetti, Maria Rosa Guerrieri & Angelo Nolè

  2. Department of Environmental Technologies and Forestry Sciences, University of Florence, Florence, Italy

    Sabrina Raddi

  3. Institute of Biometeorology, CNR, Florence, Italy

    Rita Baraldi

  4. Department of Plant Cultivation, University of Bologna, Bologna, Italy

    Elisa Vicinelli & Federico Magnani

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  1. Francesco Ripullone
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  2. Marco Borghetti
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Correspondence to Francesco Ripullone.

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Ripullone, F., Borghetti, M., Raddi, S. et al. Physiological and structural changes in response to altered precipitation regimes in a Mediterranean macchia ecosystem. Trees 23, 823–834 (2009). https://doi.org/10.1007/s00468-009-0323-2

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