Skip to main content
Log in

Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Assessing natural variability of leaf water use efficiency in plants adapted to extreme conditions of the Mediterranean climate represents an important step in the evaluation of the usefulness of some plant ecophysiological traits under water stress. Eleven Mediterranean species naturally inhabiting the Balearic Islands and corresponding to different growth forms (herbs, semi-deciduous shrubs, woody evergreen shrubs and woody evergreen semi-shrubs) were subject to progressive soil water depletion. Leaf intrinsic water use efficiency was measured by gas exchange at four different degrees of water stress. Under well watered conditions, differences in leaf intrinsic water use efficiency (A N/g s) among growth forms were limited to woody evergreen semi-shrubs, which presented the highest values. Under water stress conditions, differences became more evident, with a trend for an increase in A N/g s from woody evergreen shrubs, through semi-deciduous shrubs and herbaceous to woody evergreen semi-shrubs. The observed variation in A N/g s correlated with several physiological (leaf water potential, soil to leaf hydraulic conductance and stomatal conductance) and morphological (stomatal density) parameters, displaying a general relationship for all growth forms. This suggests that the capacity for withstanding water limitation is adaptive for all Mediterranean species. However, when A N/g s was related to leaf mass area, this relationship was not generally applicable, and depended on growth forms, suggesting that different growth forms display specific morphological adjustments in response to water shortage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abril M, Hanano R (1998) Ecophysiological responses of three evergreen woody Mediterranean species to water stress. Acta Oecol 19:377–387, doi:10.1016/S1146-609X(98)80042-8

    Google Scholar 

  • Aguiló F, Medrano H (1994) Comparative effect of drought on North European and Balearic populations of Lolium perenne. Ann Appl Biol 38:131–137

    Google Scholar 

  • Angelopoulos K, Dichio B, Xiloyannis C (1996) Inhibition of photosynthesis in olive tress (Olea europaea L.) during water stress and rewatering. J Exp Bot 47:1093–1100, doi:10.1093/jxb/47.8.1093

    CAS  Google Scholar 

  • Aranda I, Castro L, Pardos M, Gil L, Pardos PA (2005) Effects of the interaction between drought and shade on water relations, gas exchange and morphological traits in cork oak (Quercus suber L.) seedlings. For Ecol Manage 210:117–129, doi:10.1016/j.foreco.2005.02.012

    Google Scholar 

  • Aranda I, Pardos M, Puertolas J, Jimenez MD, Pardos JA (2007) Water-use efficiency in cork oak (Quercus suber) is modified by the interaction of water and light availabilities. Tree Physiol 27:671–677

    PubMed  Google Scholar 

  • Arndt SK (2006) Integrated research of plant functional traits is important for the understanding of ecosystem processes. Plant Soil 285:1–3, doi:10.1007/s11104-006-9097-0

    CAS  Google Scholar 

  • Asbjornsen H, Shepherd G, Helmers M (2008) Seasonal patterns in depth of water uptake under contrasting annual and perennial systems in the Corn Belt Region of the Midwestern U.S. Plant Soil 208:69–92, doi:10.1007/s11104-008-9607-3

    Google Scholar 

  • Asensio D, Peñuelas J, Ogaya R, Llusià J (2007) Seasonal soil and CO2 exchange rates in a Mediterranean holm oak forest and their responses to drought conditions. Atmos Environ 41:2447–2455, doi:10.1016/j.atmosenv.2006.05.008

    CAS  Google Scholar 

  • Asseng S, Turner NC, Keating (2001) Analysis of water- and nitrogen-use efficiency of wheat in a Mediterranean climate. Plant Soil 233:127–143, doi:10.1023/A:1010381602223

    CAS  Google Scholar 

  • Bell LW, Williams AH, Ryan MH, Ewing M (2007) Water relations and adaptations to increasing water deficit in three perennial legumes, Medicago sativa, Dorycnium hirsutum and Dorycnium rectum. Plant Soil 290:231–243, doi:10.1007/s11104-006-9155-7

    CAS  Google Scholar 

  • Bota J, Flexas J, Medrano H (2001) Genetic variability of photosynthesis and water use in Balearic grapevine cultivars. Ann Appl Biol 138:353–361, doi:10.1111/j.1744-7348.2001.tb00120.x

    Google Scholar 

  • Bota J, Medrano H, Flexas J (2004a) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol 162:671–681, doi:10.1111/j.1469-8137.2004.01056.x

    CAS  Google Scholar 

  • Bota J, Stasyk O, Flexas J, Medrano H (2004b) Effect of water stress on partitioning of C14-labelled photosynthates in Vitis vinifera. Funct Plant Biol 7:697–708, doi:10.1071/FP03262

    Google Scholar 

  • Castell C, Terradas J (1995) Water relations, gas exchange and growth of dominant and suppressed shots of Arbutus unedo L. Tree Physiol 15:405–409

    PubMed  Google Scholar 

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

    Google Scholar 

  • Castrillo M, Kruger NJ, Whatley FR (1992) Sucrose metabolism in mango fruit during ripening. Plant Sci 84:45–51, doi:10.1016/0168-9452(92)90206-2

    CAS  Google Scholar 

  • Caravaca F, Figueroa D, Barea JM, Azcón-Aguilar C, Roldán A (2004) Effect of mycorrhizal inoculation on nutrient acquisition, gas exchange, and nitrate reductase activity of two Mediterranean-autochthonous species under drought stress. J Plant Nutr 27:57–74, doi:10.1081/PLN-120027547

    CAS  Google Scholar 

  • Centritto M, Loreto F, Chartzoulakis K (2003) The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive samplings. Plant Cell Environ 26:585–594, doi:10.1046/j.1365-3040.2003.00993.x

    Google Scholar 

  • Chartzoulakis K, Patakas A, Bosabalidis AM (1999) Changes in water relations, photosynthesis and leaf anatomy induced by intermittent drought in two olive cultivars. Environ Exp Bot 30:239–264

    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

    CAS  Google Scholar 

  • Clary J, Savé R, Biel C, Herralde F (2004) Water relations in competitive interactions of Mediterranean grasses and shrubs. Ann Appl Biol 144:149–155, doi:10.1111/j.1744-7348.2004.tb00328.x

    Google Scholar 

  • Clemente AS, Rego FC, Correia OA (2005) Growth, water relations and photosynthesis of seedlings and resprouts after fire. Acta Oecol 27:233–243, doi:10.1016/j.actao.2005.01.005

    Google Scholar 

  • Corcuera L, Morales F, Abadía A, Gil-Pelegrín E (2005) Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula. Tree Physiol 25:599–608

    PubMed  CAS  Google Scholar 

  • Damesin C, Rambal S (1995) Field-study of leaf photosynthetic performance by a Mediterranean deciduous oak tree (Quercus pubescens) during a severe summer drought. New Phytol 131:159–167, doi:10.1111/j.1469-8137.1995.tb05717.x

    Google Scholar 

  • Damesin C, Rambal S, Joffre R (1998) Co-occurrence of trees with differing leaf habit: a functional approach on Mediterranean oaks. Acta Oecol 19:195–204, doi:10.1016/S1146-609X(98)80024-6

    Google Scholar 

  • De Souza CR, Maroco JP, dos Santos TP, Rodrigues ML, Lopes C, Pereira JS, Chaves MM (2003) Partial rootzone drying: regulation of stomatal aperture and carbon assimilation in field-grown grapevines (Vitis vinifera cv. Moscatel). Funct Plant Biol 30:653–662, doi:10.1071/FP02115

    Google Scholar 

  • De Souza CR, Maroco JP, dos Santos TP, Rodrigues ML, Lopes C, Pereira JS, Chaves MM (2005) Control of stomatal aperture and carbon uptake by deficit irrigation in two grapevine cultivars. Agric Ecosyst Environ 106:261–274, doi:10.1016/j.agee.2004.10.014

    Google Scholar 

  • Ehleringer JR (1993) Carbon and water relations in desert plants: an isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic, San Diego, pp 155–172

    Google Scholar 

  • Ehleringer JR, Mooney HA (1982) Productivity of desert and Mediterranean-climate plants. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology. physiological plant ecology II, Vol. 12. Springer, Berlin, pp 205–231

    Google Scholar 

  • Faria T, Silvério D, Breia E, Cabral R, Abadía A, Abadía J, Pereira JS, Chaves MM (1998) Differences in the response of carbon assimilation to summer stress (water deficits, high light and temperature) in four Mediterranean tree species. Physiol Plant 102:419–428, doi:10.1034/j.1399-3054.1998.1020310.x

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Flexas J, Escalona JM, Medrano H (1999) Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines. Plant Cell Environ 22:39–48, doi:10.1046/j.1365-3040.1999.00371.x

    Google Scholar 

  • Flexas J, Briantas JM, Cerovic Z, Medrano H, Moya I (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sens Environ 73:283–297, doi:10.1016/S0034-4257(00)00104-8

    Google Scholar 

  • Flexas J, Gulías J, Jonasson S, Medrano H, Mus M (2001) Seasonal patterns and control of gas-exchange in local populations of the Mediterranean evergreen shrub Pistacia lentiscus L. Acta Oecol 22:33–43, doi:10.1016/S1146-609X(00)01099-7

    Google Scholar 

  • Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Funct Plant Biol 29:461–471, doi:10.1071/PP01119

    Google Scholar 

  • Flexas J, Gulías J, Medrano H (2003) Leaf photosynthesis in Mediterranean vegetation. In: Hemantaranjan A (ed) Advances in plant physiology, vol. V. Scientific Publishers, Jodhpur, pp 181–226

    Google Scholar 

  • Flexas J, Bota J, Cifre J, Escalona JM, Galmés J, Gulías J, Lefi E-K, Martínez-Cañellas SF, Moreno MT, Ribas-Carbó M, Riera D, Sampol B, Medrano H (2004) Understanding down-regulation of photosynthesis under water stress: future prospects and searching for physiological tools for irrigation management. Ann Appl Biol 144:273–283, doi:10.1111/j.1744-7348.2004.tb00343.x

    Google Scholar 

  • Flexas J, Ribas-Carbó M, Díaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621, doi:10.1111/j.1365-3040.2007.01757.x

    PubMed  CAS  Google Scholar 

  • Gallé A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytol 174:799–810, doi:10.1111/j.1469-8137.2007.02047.x

    PubMed  Google Scholar 

  • Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005a) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant Cell Environ 28:571–579, doi:10.1111/j.1365-3040.2005.01300.x

    Google Scholar 

  • Galmés J, Cifre J, Medrano H, Flexas J (2005b) Modulation of relative growth rate and its components by water stress in Mediterranean species with different growth forms. Oecologia 145:21–31, doi:10.1007/s00442-005-0106-4

    PubMed  Google Scholar 

  • Galmés J, Flexas J, Savé R, Medrano H (2007a) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil 290:139–155, doi:10.1007/s11104-006-9148-6

    Google Scholar 

  • Galmés J, Medrano H, Flexas J (2007b) 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

    PubMed  Google Scholar 

  • Galmés J, Abadía A, Medrano H, Flexas J (2007c) Photosynthesis and photoprotection processes in the wild-extinct plant Lysimachia minoricensis. Environ Exp Bot 60:308–317, doi:10.1016/j.envexpbot.2006.12.016

    Google Scholar 

  • Galmés J, Medrano H, Flexas J (2007d) Photosynthesis and photoinhibition in response to drought in a pubescent (var. minor) and a glabrous (var. palaui) variety of Digitalis minor. Environ Exp Bot 60:105–111, doi:10.1016/j.envexpbot.2006.08.001

    Google Scholar 

  • García-Plazaola JI, Faria T, Abadía J, Abadía A, Chaves MM, Pereira JS (1997) Seasonal changes in xanthophyll composition and photosynthesis in cork oak (Quercus suber L.) leaves under Mediterranean climate. J Exp Bot 48:1667–1674

    Google Scholar 

  • Garten CT, Taylor GE (1992) Foliar delta C-13 within a temperature deciduous forest—spatial, temporal, and species sources of variation. Oecologia 90:1–7, doi:10.1007/BF00317801

    Google Scholar 

  • Goulden ML (1996) Carbon assimilation and water-use efficiency by neighbouring Mediterranean-climate oaks that differ in water access. Tree Physiol 16:417–424

    PubMed  CAS  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

    CAS  Google Scholar 

  • Gratani L (1993) Response to microclimate of morphological leaf attributes, photosynthetic and water relations of evergreen sclerophyllous shrub species. Photosynthetica 29:573–582

    Google Scholar 

  • Gratani L (1995) Structural and ecophysiological plasticity of some evergreen species of the Mediterranean maquis in response to climate. Photosynthetica 31:335–343

    CAS  Google Scholar 

  • Gratani L (1996) Leaf and shoot growth dynamics of Quercus ilex L. Acta Oecol 17:17–27

    Google Scholar 

  • Gratani L, Varone L (2004) Adaptive photosynthetic strategies of the Mediterranean maquis species according to their origin. Photosynthetica 42:551–558, doi:10.1007/S11099-005-0012-3

    Google Scholar 

  • Gulías J, Flexas J, Abadía A, Medrano H (2002) Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining of Rhamnus ludovici-salvatoris, an endemic Balearic species. Tree Physiol 22:687–697

    PubMed  Google Scholar 

  • Gulías J, Flexas J, Mus M, Cifre J, Lefi E, Medrano H (2003) Relationship between maximum leaf photosynthesis, nitrogen content and specific leaf area in balearic endemic and non-endemic Mediterranean species. Ann Bot (Lond) 92:215–222, doi:10.1093/aob/mcg123

    Google Scholar 

  • Harley PC, Tenhunen JD, Beyschlag W, Lange OL (1987) Seasonal photosynthetic rates and photosynthetic capacity in leaves of Cistus salvifolius, a European Mediterranean semi-deciduous shrub. Oecologia 74:380–388, doi:10.1007/BF00378934

    Google Scholar 

  • Kurz-Besson C, Otieno D, Lobo do Vale R, Siedwolf R, Schmidt M, Herd A, Nogueira C, David TS, David JS, Tenhunen J, Pereira JS, Chaves M (2006) Hydraulic lift in cork oak trees in a savannah-type Mediterranean ecosystem and its contribution to the local water balance. Plant Soil 282:361–378, doi:10.1007/s11104-006-0005-4

    CAS  Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for ecological causes and consequences. Adv Ecol Res 23:187–261, doi:10.1016/S0065-2504(08)60148-8

    CAS  Google Scholar 

  • Lefi E, Gulías J, Cifre J, Ben Younes M, Medrano H (2004) Drought effects on the dynamics of leaf production and senescence in field-grown Medicago arborea and Medicago citrina. Ann Appl Biol 144:169–176, doi:10.1111/j.1744-7348.2004.tb00330.x

    Google Scholar 

  • Levizou L, Petropoulou Y, Manetas Y (2004) Carotenoid composition of peridermal twigs does not fully conform to a shade acclimation hypothesis. Photosynthetica 42:591–596, doi:10.1007/S11099-005-0018-x

    CAS  Google Scholar 

  • Llorens L, Peñuelas J, Filella I (2003) Diurnal and seasonal variations in the photosynthetic performance and water relations of two co-occurring Mediterranean shrubs, Erica multiflora and Globularia alypum. Physiol Plant 118:84–95, doi:10.1034/j.1399-3054.2003.00101.x

    PubMed  CAS  Google Scholar 

  • Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ 26:595–601, doi:10.1046/j.1365-3040.2003.00994.x

    CAS  Google Scholar 

  • Manes F, Seufert G, Vitale M (1997) Ecophysiological studies of Mediterranean plant species at the Castelporziano Estate. Atmos Environ 31:51–60, doi:10.1016/S1352-2310(97)00073-3

    CAS  Google Scholar 

  • Manes F, Vitale M, Donato E, Giannini M, Puppi G (2006) Different ability of three Mediterranean oak species to tolerate progressive water stress. Photosynthetica 44:387–393, doi:10.1007/s11099-006-0040-7

    Google Scholar 

  • Mappin KA, Pate JS, Bell TL (2003) Productivity and water relations of burnt and long-unburnt semi-arid shrubland in Western Australia. Plant Soil 257:321–340, doi:10.1023/A:1027349501441

    CAS  Google Scholar 

  • Margaris NS (1981) Adaptive strategies in plants dominating Mediterranean-type ecosystems. In: di Castri F, Goodall DW, Spetch RL (eds) Ecosystems of the World V11: Mediterranean-type Shrublands. Elsevier Scientific, Amsterdam, pp 309–315

    Google Scholar 

  • Maroco JP, Rodrigues ML, Lopes C, Chaves MM (2002) Limitations to leaf photosynthesis in field-grown grapevine under drought—metabolic and modelling approaches. Funct Plant Biol 29:451–459, doi:10.1071/PP01040

    Google Scholar 

  • Marshall JD, Zhang J (1994) Carbon isotope discrimination and water use efficiency in native plants of the north-central Rockies. Ecology 75:1887–1895, doi:10.2307/1941593

    Google Scholar 

  • Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20:131–138

    PubMed  Google Scholar 

  • Mediavilla S, Escudero A (2003a) Stomatal responses to drought at a Mediterranean site: a comparative study of co-occurring woody species differing in leaf longevity. Tree Physiol 23:987–996

    PubMed  Google Scholar 

  • Mediavilla S, Escudero A (2003b) Mature trees versus seedlings: differences in leaf traits and gas exchange patterns in three co-occurring Mediterranean oaks. Ann Sci 60:455–460, doi:10.1051/forest:2003038

    Google Scholar 

  • Mediavilla S, Santiago H, Escudero A (2002) Stomatal and mesophyll limitations to photosynthesis in one evergreen and one deciduous Mediterranean oak species. Photosynthetica 40:553–559, doi:10.1023/A:1024399919107

    CAS  Google Scholar 

  • Medrano H, Escalona JM, Bota J, Gulías J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: the interest of stomatal conductance as a reference parameter. Ann Bot (Lond) 89:895–905, doi:10.1093/aob/mcf079

    CAS  Google Scholar 

  • Medrano H, Escalona JM, Cifre J, Bota J, Flexas J (2003) A ten-year study on the physiology of two Spanish grapevine cultivars under field conditions: effects of water availability from leaf photosynthesis to grape yield and quality. Funct Plant Biol 30:607–619, doi:10.1071/FP02110

    CAS  Google Scholar 

  • Mooney HA (1982) Habitat, plant form and plant water relations in Mediterranean climate regions. Ecologia Mediterranea 8:287–296

    Google Scholar 

  • Munné-Bosch S, Alegre L (2000) The significance of beta-carotene, alpha-tocopherol and the xanthophyll cycle in droughted Melissa officinalis plants. Aust J Plant Physiol 27:139–146

    Google Scholar 

  • Munné-Bosch S, Schwarz K, Alegre L (1999) Enhanced formation of alpha-tocopherol and highly oxidized abietane diterpenes in water-stressed rosemary plants. Plant Physiol 121:1047–1052, doi:10.1104/pp.121.3.1047

    PubMed  Google Scholar 

  • Munné-Bosch S, Jubany-Mari T, Alegre L (2003) Enhanced photo- and antioxidative protection, and hydrogen peroxide accumulation in drought-stressed Cistus clusii and Cistus albidus plants. Tree Physiol 23:1–12

    PubMed  Google Scholar 

  • Nieva FJJ, Castellanos EM, Figueroa ME, Gil F (1999) Gas exchange and chlorophyll fluorescence of C3 and C4 salt marsh species. Photosynthetica 36:397–406, doi:10.1023/A:1007024019133

    CAS  Google Scholar 

  • Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in tress and shrubs. Ecology 82:453–469

    Google Scholar 

  • Peña-Rojas K, Aranda X, Joffre R, Fleck I (2005) Leaf morphology, photochemistry and water status changes in resprouting Quercus ilex during drought. Funct Plant Biol 32:117–130, doi:10.1071/FP04137

    Google Scholar 

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

    Google Scholar 

  • Peñuelas J, Munné-Bosch S, Llusià J, Filella I (2004) Leaf reflectance and photo- and antioxidant protection in field-grown summer-stressed Phillyrea angustifolia. Optical signals of oxidative stress. New Phytol 162:115–162, doi:10.1046/j.1469-8137.2004.01007.x

    Google Scholar 

  • Picon C, Ferhi A, Guehl JM (1997) Concentration and δ13C of leaf carbohydrates in relation to gas exchange in Quercus robur under elevated CO2 and drought. J Exp Bot 48:1547–1556

    CAS  Google Scholar 

  • Ponton S, Dupouey JL, Breda N, Dreyer E (2002) Comparison of water-use efficiency of seedlings from two sympatric oak genotypes: genotype x environment interactions. Tree Physiol 22:413–422

    PubMed  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Browman WD (1999) Generality of leaf relationships: a test across six biomes. Ecology 80:1955–1969

    Article  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 hypotheses? Glob Change Biol 8:999–1017, doi:10.1046/j.1365-2486.2002.00530.x

    Google Scholar 

  • Reichstein M, Tenhunen J, Roupsard O, Ourcival JM, Rambal S, Miglietta F, Peressotti Pecchiari M, Tirone G, Valentini R (2003) Inverse modeling of seasonal effects on canopy CO2/H2O exchange in three Mediterranean ecosystems. J Geophys Res 108:4726, doi:10.1029/2003JD003430

    Google Scholar 

  • Sala A, Tenhunen JD (1996) Simulations of canopy net photosynthesis and transpiration in Quercus ilex L under the influence of seasonal drought. Agr For Metereol 78:203–222, doi:10.1016/0168-1923(95)02250-3

    Google Scholar 

  • Salleo S, Nardini A, Pitt F, Lo Gullo MA (2000) Xylem cavitation and hydraulic control of stomatal conductance in laurel (Laurus nobilis L.). Plant Cell Environ 23:71–79, doi:10.1046/j.1365-3040.2000.00516.x

    Google Scholar 

  • Sampol B, Bota J, Riera D, Medrano H, Flexas J (2003) Analysis of the virus-induced inhibition of photosynthesis in malmsey grapevines. New Phytol 160:403–412, doi:10.1046/j.1469-8137.2003.00882.x

    CAS  Google Scholar 

  • Schultz HR (2003) Differences in hydraulic architecture account for near isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars under drought. Plant Cell Environ 26:1393–1405, doi:10.1046/j.1365-3040.2003.01064.x

    Google Scholar 

  • Schulze E-D, Hall AE (1982) Stomatal responses to water loss and CO2 assimilation rates in plants of contrasting environments. In: Lange OL, Nobel P, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology. Physiological plant ecology, vol. 12B. Springer, Berlin, pp 181–230

    Google Scholar 

  • Sharkey TD (1985) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot Rev 51:53–105, doi:10.1007/BF02861058

    Google Scholar 

  • Sperry JS, Pockman 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

    Google Scholar 

  • Tenhunen JD, Lange OL, Harley PC, Beyschalg W, Meyer S (1985) Limitations due to water-stress on leaf net photosynthesis of Quercus coccifera in the Portuguese evergreen scrub. Oecologia 67:23–30, doi:10.1007/BF00378446

    Google Scholar 

  • Tenhunen JD, Harley PC, Beyschlag W, Lange OL (1987a) A model of net photosynthesis for leaves of the sclerophyll Quercus coccifera. In: Tenhunen JA, Caterino FM, Lange OL, Oechel WC (eds) Plant response to stress. Springer, Berlin, pp 339–354

    Google Scholar 

  • Tenhunen JD, Beyschlag W, Lange OL, Harley PC (1987b) Changes during summer drought in leaf CO2 uptake rates of macchia shrubs growing in Portugal: limitations due to photosynthetic capacity, carboxylation efficiency, and stomatal conductance. In: Tenhunen JA, Caterino FM, Lange OL, Oechel WC (eds) Plant response to stress. Springer, Berlin, pp 305–327

    Google Scholar 

  • Tuberosa R, Giuliani S, Parry MAJ, Araus JL (2007) Improving water use efficiency in Mediterranean agriculture: what limits the adoption of new technologies? Ann Appl Biol 150:157–162, doi:10.1111/j.1744-7348.2007.00127.x

    Google Scholar 

  • Valentini R, Epron D, De Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Quercus cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ 18:631–640, doi:10.1111/j.1365-3040.1995.tb00564.x

    CAS  Google Scholar 

  • Valladares F, Pearcy (1997) Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia. Plant Cell Environ 20:25–36, doi:10.1046/j.1365-3040.1997.d01-8.x

    Google Scholar 

  • Valladares F, Sánchez-Gómez D (2005) Ecophysiological traits associated with drought in Mediterranean tree seedlings: individual responses versus interspecific trends in eleven species. Plant Biol 8:688–697, doi:10.1055/s-2006-924107

    Google Scholar 

  • Virgona JM, Barlow EWR (1991) Drought stress induces changes in the non-structural carbohydrate composition of wheat stems. Aust J Plant Physiol 18:239–247

    CAS  Google Scholar 

  • Von Caemmerer S, Evans JR (1991) Determination of the average partial pressure of CO2 in chloroplasts from leaves of several C3 plants. Aust J Plant Physiol 18:287–305

    Article  Google Scholar 

  • Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 concentration from pre-industrial levels. Nature 327:617–618, doi:10.1038/327617a0

    Google Scholar 

  • Woodward FI, Bazzaz FA (1988) The responses of stomatal density to CO2 partial pressure. J Exp Bot 209:1771–1781, doi:10.1093/jxb/39.12.1771

    Google Scholar 

  • Weyers JDB, Johansen LG (1985) Accurate estimation of stomatal aperture from silicone rubber impressions. New Phytol 101:109–115, doi:10.1111/j.1469-8137.1985.tb02820.x

    Google Scholar 

  • Wildy DT, Pate JS, Sefcik T (2004) Water-use efficiency of a mallee eucalypt growing naturally and in short-rotation coppice cultivation. Plant Soil 262:111–128, doi:10.1023/B:PLSO.0000037030.61945.0d

    CAS  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulías J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas E, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–827, doi:10.1038/nature02403

    PubMed  CAS  Google Scholar 

  • Xu L, Baldocchi DD (2003) Seasonal trends in photosynthetic parameters and stomatal conductance of blue oak (Quercus douglasii) under prolonged summer drought and high temperature. Tree Physiol 23:865–877

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was financed by the project PRIB-2004-10144 “Variability in the water-use efficiency by plants: Optimization of water-use” (Conselleria d’Economia, Hisenda i Innovació, Govern de les Illes Balears). JG was granted a post-doctoral fellowship (MEC). Drs Ribas-Carbó and Kane are acknowledged for their helpful comments in previous versions of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeroni Galmés.

Additional information

Responsible Editor: Hans Lambers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental data

Soil water content (SWC, as % with respect to control values), pre-dawn leaf water potential (ΨPD), stomatal conductance (gs) and intrinsic water use efficiency (AN/gs) for the 11 selected species under different irrigation treatments: control (CO), mild water stress (MiWS), moderate water stress (MoWS), severe water stress (SeWS) and re-watering (RW). Values are mean ± SE of four replicates (DOC 26.5 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Medrano, H., Flexas, J. & Galmés, J. Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms. Plant Soil 317, 17–29 (2009). https://doi.org/10.1007/s11104-008-9785-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-008-9785-z

Keywords

Navigation