Ecophysiological Traits Associated with Drought in Mediterranean Tree Seedlings: Individual Responses versus Interspecific Trends in Eleven Species

Abstract

Species differ regarding their drought tolerance and individuals of a given species can modify their morphology and physiology in response to drought. However, since evolutionary and ecological selective pressures differ, individual and interspecific responses to drought might not match. We determined summer survival and a number of ecophysiological variables in two factorial experiments with seedlings of eleven tree species present in Mediterranean ecosystems, grown under slowly imposed water stress and control conditions. Plants experiencing drought exhibited reduced growth, low specific leaf area, chlorophyll content, and photosynthetic rate when compared to the controls, and species-specific drought tolerance was associated with an analogous set of trait values. However, while species with high leaf area ratio and shoot-root ratio exhibited greater drought tolerance, drought induced the reversed response within species. Contrary to expectations, water use efficiency was lower in drought-tolerant species and decreased in water-stressed individuals compared to the control plants. There was a distinctive phylogenetic signal in the functional grouping of species, with oaks, pines, and other genera being clearly different from each other in their drought tolerance and in their functional responses to drought. However, all relationships between ecophysiological variables and drought tolerance were significant after accounting for phylogenetic effects, with the exception of the relationship between drought tolerance and photochemical efficiency. Our results show that drought tolerance is not achieved by a single combination of trait values, and that even though evolutionary processes and individual responses tend to render similar results in terms of functional traits associated with drought, they do not necessarily match.

Key words

Drought tolerance - functional traits - Mediterranean plants - phylogeny - water use efficiency - woody seedlings.

References

• 1 Ackerly D. D., Dudley S. A., Sultan S. E., Schmitt J., Coleman J. S., Randal Linder C., Sandquist D. R., Geber M. A., Evans A. S., Dawson T. E., Lechowicz M. J.. The evolution of plant ecophysiological traits: recent advances and future directions.  Bioscience. (2000);  50 979-995
• 2 Adams H. D., Kolb T. E.. Drought responses of conifers in ecotone forests of northern Arizona: tree ring growth and leaf delta 13C.  Oecologia. (2004);  140 217-225
• 3 Balaguer L., Pugnaire F. I., Martinez-Ferri E., Armas C., Valladares F., Manrique E.. Ecophysiological significance of chlorophyll loss and reduced photochemical efficiency under extreme aridity in Stipa tenacissima L.  Plant and Soil. (2002);  240 343-352
• 4 Barnes J. D., Balaguer L., Manrique E., Elvira S., Davison A. W.. A reappraisal of the use of DMSO for the extraction and determination of chlorophyll a and b in lichens and higher plants.  Environmental and Experimental Botany. (1992);  32 85-100
• 5 Cabrera H. M.. Ecophysiological responses of plants in ecosystems with Mediterranean-like climate and high mountain environments.  Revista Chilena De Historia Natural. (2002);  75 625-637
• 6 Cornic G.. Drought stress and high light effects on leaf photosynthesis. Baker, N. R. and Bowyer, J. R., eds. Photoinhibition of Photosynthesis. From Molecular Mechanisms to the Field. Oxford; Bios Scientific Publishers (1994): 297-314
• 7 Deka R. N., Wairiu M., Mtakwa P. W., Mullins C. E., Veenendaal E. M., Townend J.. Use and accuracy of the filter-paper technique for measurement of soil matric potential.  European Journal of Soil Science. (1995);  46 233-238
• 8 di Pasquale G., di Martino P., Mazzoleni S.. Forest history in the Mediterranean region. Mazzoleni, S., di Pasquale, G., Mulligan, M., di Martino, P., and Rego, F., eds. Recent Dynamics of the Mediterranean Vegetation and Landscape. Chichester; John Wiley and Sons (2004): 259-279
• 9 Felsenstein J.. Phylogenies and the comparative method.  American Naturalist. (1985);  125 1-15
• 10 Ferrio J. P., Florit A., Vega A., Serrano L., Voltas J.. D13C and tree-ring width reflect different drought responses in Quercus ilex and Pinus halepensis.  Oecologia. (2003);  442 512-518
• 11 Flexas J., Galmes J., Ribas-Carbo M., Medrano H.. The effects of water stress on plant respiration. Lambers, H. and Ribas-Carbo, M., eds. Plant Respiration. From Cell to Ecosystem. Dordrecht, The Netherlands; Springer (2005): 85-94
• 12 Garland T. J., Dickerman A. W., Janis C. M., Jones J. A.. Phylogenetic analysis of covariance by computer simulation.  Systematic Biology. (1993);  42 265-292
• 13 Garland T. J., Midford P. E., Ives A. R.. An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral states.  American Zoologist. (1999);  39 374-388
• 14 Ghashghaie J., Duranceau M., Badeck F. W., Cornic G., Adeline M. T., Deleens E.. Delta C‐13 of CO₂ respired in the dark in relation to delta C‐13 of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought.  Plant, Cell and Environment. (2001);  24 505-515
• 15 Gulías J., Flexas J., Abadía A., Medrano H.. Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species.  Tree Physiology. (2002);  22 687-697
• 16 Hunt R., Nicholls A. O.. Stress and the course control of root-shoot partitioning in herbaceous plants.  Oikos. (1986);  47 149-158
• 17 Instituto Nacional de Meteorología .Calendario Meteorológico 2003. Madrid; Ministerio de Medio Ambiente (2003)
• 18 Liston A., Robinson W. A., Piñero D., Alvarez-Buylla E. R.. Phylogenetics of Pinus (Pinaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences.  Molecular Phylogenetics and Evolution. (1999);  11 95-109
• 19 Liu F. L., Jensen C. R., Shahanzari A., Andersen M. N., Jacobsen S. E.. ABA regulated stomatal control and photosynthetic water use efficiency of potato (Solanum tuberosum L.) during progressive soil drying.  Plant Science. (2005);  168 831-836
• 20 Lloret F., Casanovas C., Peñuelas J.. Seedling survival of Mediterranean shrubland species in relation to root : shoot ratio, seed size and water and nitrogen use.  Functional Ecology. (1999);  13 210-216
• 21 López-González G.. Los Árboles y Arbustos de la Península Ibérica e Islas Baleares. Madrid; Ediciones Mundi-Prensa (2001)
• 22 Ludlow M. M.. Strategies of response to water stress. Kreeb, K. H., Richter, H., and Hinckley, T. M., eds. Structural and Functional Responses to Environmental Stresses: Water Shortage. The Hague; SPB Academic Pub (1987): 86-99
• 23 Manos P. S., Doyle J. J., Nixon K. C.. Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae).  Molecular Phylogenetics and Evolution. (1999);  12 333-349
• 24 Martinez-Ferri E., Balaguer L., Valladares F., Chico J. M., Manrique E.. Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer.  Tree Physiology. (2000);  20 131-138
• 25 Martinez-Vilalta J., Prat E., Oliveras I., Piñol J.. Xylem hydraulic properties of roots and stems of nine Mediterranean woody species.  Oecologia. (2002);  133 19-29
• 26 Maxwell K., Johnson G. N.. Chlorophyll fluorescence - a practical guide.  Journal of Experimental Botany. (2000);  51 659-668
• 27 Médail F., Quézel P.. Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin.  Annals of the Missouri Botanical Garden. (1997);  84 112-127
• 28 Mediavilla S., Escudero A.. Stomatal responses to drought of mature trees and seedlings of two co-occurring Mediterranean oaks.  Forest Ecology and Management. (2004);  187 281-294
• 29 Nogues S., Alegre L.. An increase in water deficit has no impact on the photosynthetic capacity of field-grown Mediterranean plants.  Functional Plant Biology. (2002);  29 621-630
• 30 Ogaya R., Peñuelas J.. Comparative field study of Quercus ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions.  Environmental and Experimental Botany. (2003);  50 137-148
• 31 Pagter M., Bragato C., Brix H.. Tolerance and physiological responses of Phragmites australis to water deficit.  Aquatic Botany. (2005);  81 285-299
• 32 Palamarev E.. Paleobotanical evidences of the Tertiary history and origin of the Mediterranean sclerophyll dendroflora.  Plant Systematics and Evolution. (1989);  162 93-107
• 33 Pearcy R. W., Yang W.. A three-dimensional shoot architecture model for assessment of light capture and carbon gain by understory plants.  Oecologia. (1996);  108 1-12
• 34 Reichstein M., Tenhunen J. D., Roupsard O., Ourcival J. M., Rambal S., Miglietta F., Peressotti A., Pecchiari M., Tirone G., Valentini R.. Severe drought effects on ecosystem CO₂ and H₂O fluxes at three Mediterranean evergreen sites: revision of current hypotheses?.  Global Change Biology. (2002);  8 999-1017
• 35 Retana J., Espelta J. M., Gracia M., Riba M.. Seedling recruitment. Roda, F., Retana, J., Gracia, C., and Bellot, J., eds. Ecology of Mediterranean Evergreen Oak Forests. Berlin; Springer Verlag (1999): 89-103
• 36 Romero P., Navarro J. M., Garcia F., Ordaz P. B.. Effects of regulated deficit irrigation during the pre-harvest period on gas exchange, leaf development and crop yield of mature almond trees.  Tree Physiology. (2004);  24 303-312
• 37 Sánchez-Gómez D., Valladares F., Zavala M. A.. Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation.  New Phytologist. (2006); 
• 38 Soltis D. E., Soltis P. S., Chase M. W., Mort M. E., Albach D. C., Zanis M., Savolainen V., Hahn W. H., Hoot S. B., Fay M. F., Axtell M., Swensen S. M., Prince L. M., Kress W. J. O. H. N., Nixon K. C., Farris J. S.. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences.  Botanical Journal of the Linnean Society. (2000);  133 381-461
• 39 Suc J. P.. Origin and evolution of the Mediterranean vegetation and climate in Europe.  Nature. (1984);  307 429-432
• 40 Thompson J. D.. Plant Evolution in the Mediterranean. New York; Oxford University Press (2005)
• 41 Turner N. C.. Sustainable production of crops and pastures under drought in a Mediterranean environment.  Annals of Applied Biology. (2004);  144 139-147
• 42 Valladares F., Pearcy R. W.. Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia.  Plant, Cell and Environment. (1997);  20 25-36
• 43 Valladares F., Pearcy R. W.. The functional ecology of shoot architecture in sun and shade plants of Heteromeles arbutifolia M. Roem., a Californian chaparral shrub.  Oecologia. (1998);  114 1-10
• 44 Valladares F., Martinez-Ferri E., Balaguer L., Perez-Corona E., Manrique E.. Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy?.  New Phytologist. (2000);  148 79-91
• 45 Valladares F.. Ecology: functions, patterns, and evolution. In Encyclopaedia of Plant and Crop Science. New York; Marcel Dekker (2004): 404-406
• 46 Valladares F., Dobarro I., Sánchez-Gómez D., Pearcy R. W.. Photoinhibition and drought in Mediterranean woody saplings: scaling effects and interactions in sun and shade phenotypes.  Journal of Experimental Botany. (2005);  56 483-494
• 47 Webb C. O., Ackerly D. D., McPeek M. A., Donoghue M. J.. Phylogenies and community ecology.  Annual Review of Ecology and Systematics. (2002);  33 475-505
• 48 Webb C. O., Donoghue M. J.. Phylomatic: a database for applied phylogenetics. Online, URL: http://www.phylodiversity.net/phylomatic.html. (2002)

Editor: H. de Kroon