Differences in morpho-physiological leaf traits reflect the response of growth to drought in a seeder but not in a resprouter Mediterranean species
David A. Ramírez A B D , Antonio Parra A , Víctor Resco de Dios A C and José M. Moreno A D
+ Author Affiliations
- Author Affiliations
A Departamento de Ciencias Ambientales, Universidad de Castilla-La Mancha, 45071 Toledo, Spain.
B Present address: Programa de Doctorado en Recursos Hídricos, Universidad Nacional Agraria La Molina, Lima 12, Perú.
C Present address: Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, NSW 2753, Australia.
D Corresponding author. Emails: dramirez@lamolina.edu.pe; josem.moreno@uclm.es
Functional Plant Biology 39(4) 332-341 https://doi.org/10.1071/FP11232
Submitted: 15 October 2011 Accepted: 28 January 2012 Published: 8 March 2012
Abstract
Understanding the mechanisms underlying the response of different plant functional types to current and projected changes in rainfall is particularly important in drought-prone areas like the Mediterranean. Here, we report the responses of two species with contrasting leaf characteristics and post-fire regeneration strategies (Cistus ladanifer L., malacophyllous, seeder; Erica arborea L., sclerophyllous, resprouter) to a manipulative field experiment that simulated a severe drought (45% reduction of historical average rainfall). We measured monthly changes in relative growth rate (RGR), specific leaf area (SLA), bulk leaf carbon isotope composition (δ13C), predawn water potential (Ψpd), photosynthetic gas exchange, bulk modulus of elasticity and osmotic potential at maximum turgor (π). Temporal (monthly) changes in RGR of C. ladanifer were correlated with all measured leaf traits (except π) and followed Ψpd variation. However, the temporal pattern of RGR in E. arborea was largely unrelated to water availability. SLA monthly variation reflected RGR variation reasonably well in C. ladanifer, but not in E. arborea, in which shoot growth and δ13C increased at the time of maximum water stress in late summer. The relationship between water availability, and RGR and carbon assimilation in C. ladanifer, and the lack of any relationship in E. arborea suggest that the former has an enhanced capacity to harness unpredictable rainfall pulses compared with the latter. These contrasting responses to water availability indicate that the projected changes in rainfall with global warming could alter the competitive ability of these two species, and contribute to changes in plant dominance in Mediterranean shrublands.
Additional keywords: Cistus ladanifer, climate change, Erica arborea, relative growth rate, shoot water potential, specific leaf area, water stress.
References
Acácio V, Holmgren M, Rego F, Moreira F, Mohren GMJ (2009) Are drought and wildfires turning Mediterranean cork oak forests into persistent shrublands? Agroforestry Systems 76, 389–400.| Are drought and wildfires turning Mediterranean cork oak forests into persistent shrublands?Crossref | GoogleScholarGoogle Scholar |
Alpert P, Ben-gai T, Baharad A, Benjamini Y, Yekutieli D, Colacino M, Diodato L, Ramis C, Homar V, Romero R, Michaelides S, Manes A (2002) The paradoxical increase of Mediterranean extreme daily rainfall in spite of decrease in total values. Geophysical Research Letters 29, 1536
| The paradoxical increase of Mediterranean extreme daily rainfall in spite of decrease in total values.Crossref | GoogleScholarGoogle Scholar |
Antúnez I, Retamosa EC, Villar R (2001) Relative growth rate in phylogenetically related deciduous and evergreen woody species. Oecologia 128, 172–180.
| Relative growth rate in phylogenetically related deciduous and evergreen woody species.Crossref | GoogleScholarGoogle Scholar |
Bacelar EA, Correia CM, Moutinho-Pereira JM, Goncalves BC, Lopes JI, Torres-Pereira JMG (2004) Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions. Tree Physiology 24, 233–239.
| Sclerophylly and leaf anatomical traits of five field-grown olive cultivars growing under drought conditions.Crossref | GoogleScholarGoogle Scholar |
Canadell J, López-Soria L (1998) Lignotuber reserves support regrowth following clipping of two Mediterranean shrubs. Functional Ecology 12, 31–38.
| Lignotuber reserves support regrowth following clipping of two Mediterranean shrubs.Crossref | GoogleScholarGoogle Scholar |
Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proceedings of the National Academy of Sciences of the United States of America 108, 1474–1478.
| Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Smt7w%3D&md5=959c218f2ff1bf80360387aa78c6a265CAS |
Castro-Díez P, Villar-Salvador P, Perez-Rontome C, Maestro-Martinez M, Montserrat-Marti G (1998) Leaf morphology, leaf chemical composition and stem xylem characteristics in two Pistacia (Anacardiaceae) species along a climatic gradient. Flora 193, 195–202.
Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Magaña Rueda V, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor, HL Miller) pp. 847–940. (Cambridge University Press: Cambridge, USA).
Clemente AS, Rego FC, Correia OA (2005) Growth, water relations and photosynthesis of seedlings and resprouts after fire. Acta Oecologica 27, 233–243.
| Growth, water relations and photosynthesis of seedlings and resprouts after fire.Crossref | GoogleScholarGoogle Scholar |
Crescente MF, Gratani L, Larcher W (2002) Shoot growth efficiency and production of Quercus ilex L. in different climates. Flora 197, 2–9.
| Shoot growth efficiency and production of Quercus ilex L. in different climates.Crossref | GoogleScholarGoogle Scholar |
Cruz A, Moreno JM (2001) Seasonal course of total non-structural carbohydrates in the lignotuberous Mediterranean-type shrub Erica australis. Oecologia 128, 343–350.
| Seasonal course of total non-structural carbohydrates in the lignotuberous Mediterranean-type shrub Erica australis.Crossref | GoogleScholarGoogle Scholar |
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33, 507–559.
| Stable isotopes in plant ecology.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11, 539–552.
| Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSju7w%3D&md5=1fd9a4ad673a0636925c23a9450b3f1dCAS |
Filella I, Peñuelas J (2003) Partitioning of water and nitrogen in co-occurring Mediterranean woody shrub species of different evolutionary history. Oecologia 137, 51–61.
| Partitioning of water and nitrogen in co-occurring Mediterranean woody shrub species of different evolutionary history.Crossref | GoogleScholarGoogle Scholar |
Galmés J, Flexas J, Savé R, Medrano H (2007) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant and Soil 290, 139–155.
| Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery.Crossref | GoogleScholarGoogle Scholar |
García-Ruiz JM, López-Moreno JI, Vicente-Serrano SM, Lasanta–Martínez T, Beguería S (2011) Mediterranean water resources in a global change scenario. Earth-Science Reviews 105, 121–139.
| Mediterranean water resources in a global change scenario.Crossref | GoogleScholarGoogle Scholar |
Geiger DR, Servaites JC (1991) Carbon allocation and response to stress. In ‘Response of plants to multiple stresses’. (Eds HA Mooney, WE Winner, EJ Pell) pp. 103–127. (Academic Press: London).
Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global and Planetary Change 63, 90–104.
| Climate change projections for the Mediterranean region.Crossref | GoogleScholarGoogle Scholar |
Gratani L, Varone L (2004) Leaf key traits of Erica arborea L., Erica multiflora L. and Rosmarinus officinalis L. co-occurring in the Mediterranean maquis. Flora 199, 58–69.
| Leaf key traits of Erica arborea L., Erica multiflora L. and Rosmarinus officinalis L. co-occurring in the Mediterranean maquis.Crossref | GoogleScholarGoogle Scholar |
Gratani L, Varone L (2006) Long-time variations in leaf mass and area of Mediterranean evergreen broad-leaf and narrow-leaf maquis species. Photosynthetica 44, 161–168.
| Long-time variations in leaf mass and area of Mediterranean evergreen broad-leaf and narrow-leaf maquis species.Crossref | GoogleScholarGoogle Scholar |
Groom PK, Lamont BB (1999) Which common indices of sclerophylly best reflect differences in leaf structure? Ecoscience 6, 471–474.
Haase P, Pugnaire FI, Clark SC, Incoll LD (1999) Environmental control of canopy dynamics and photosynthetic rate in the evergreen tussock grass Stipa tenacissima. Plant Ecology 145, 327–339.
| Environmental control of canopy dynamics and photosynthetic rate in the evergreen tussock grass Stipa tenacissima.Crossref | GoogleScholarGoogle Scholar |
Harper JL (1977) ‘Population biology of plants.’ (Academic Press Inc.: San Diego)
Hunt R, Lloyd PS (1987) Growth and partitioning. New Phytologist 103, 235–250.
Joffre R, Rambal S, Damesin C (2007) Functional attributes in Mediterranean-type ecosystems. In ‘Handbook of functional plant ecology’. (Eds FI Pugnaire, F Valladares) pp. 285–312. (CRC Press, Taylor & Francis Group: New York)
Jones HG (1992) ‘Plants and microclimate, a quantitative approach to environmental plant physiology.’ (Cambridge University Press: Cambridge, USA)
Jongen M, Pereira JS, Aires LMI, Pio CA (2011) The effects of drought and timing of precipitation on the inter-annual variation in ecosystem–atmosphere exchange in a Mediterranean grassland. Agricultural and Forest Meteorology 151, 595–606.
| The effects of drought and timing of precipitation on the inter-annual variation in ecosystem–atmosphere exchange in a Mediterranean grassland.Crossref | GoogleScholarGoogle Scholar |
Kozlowski TT, Pallardy SG (1997) ‘Growth control in woody plants.’ (Academic Press: San Diego, CA)
Lambers H, Chapin FS, III, Pons TL (2008) ‘Plant physiological ecology.’ (Springer: New York)
Lana X, Martínez MD, Burgueño A, Serra C, Martín-Vide J, Gómez L (2006) Distributions of long dry spells in the Iberian Peninsula. International Journal of Climatology 26, 1999–2021.
| Distributions of long dry spells in the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |
Larcher W (2003) ‘Physiological plant ecology, ecophysiology and stress physiology of functional groups.’ 4th edn. (Springer-Verlag: Berlin)
Luna MB (1998) Fenología y esfuerzo reproductivo de las especies arbustivas de un jaral-brezal del centro de la Península Ibérica. MSc thesis. Madrid University, Spain.
Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao Z-C (2007) Global climate projections. In ‘Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor, HL Miller) pp. 747–846. (Cambridge University Press: Cambridge, USA)
Miranda JD, Armas C, Padilla FM, Pugnaire FI (2011) Climatic change and rainfall patterns: effects on semi-arid plant communities of the Iberian Southeast. Journal of Arid Environments 75, 1302–1309.
| Climatic change and rainfall patterns: effects on semi-arid plant communities of the Iberian Southeast.Crossref | GoogleScholarGoogle Scholar |
Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SSO (2008) Leaf water relations during summer water deficit: differential responses in turgor maintenance and variation in leaf structure among different plant communities in south-western Australia. Plant, Cell & Environment 31, 1791–1802.
| Leaf water relations during summer water deficit: differential responses in turgor maintenance and variation in leaf structure among different plant communities in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Mouillot F, Rambal S, Joffre R (2002) Simulating climate change impacts on fire frequency and vegetation dynamics in a Mediterranean-type ecosystem. Global Change Biology 8, 423–437.
| Simulating climate change impacts on fire frequency and vegetation dynamics in a Mediterranean-type ecosystem.Crossref | GoogleScholarGoogle Scholar |
Naveh Z (1975) The evolutionary significance of fire in the Mediterranean region. Vegetatio 29, 199–208.
| The evolutionary significance of fire in the Mediterranean region.Crossref | GoogleScholarGoogle Scholar |
Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82, 453–469.
| Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs.Crossref | GoogleScholarGoogle Scholar |
Niinemets U, Lukjanova A (2003) Needle longevity, shoot growth and branching frequency in relation to site fertility and within-canopy light conditions in Pinus sylvestris. Annals of Forest Science 60, 195–208.
| Needle longevity, shoot growth and branching frequency in relation to site fertility and within-canopy light conditions in Pinus sylvestris.Crossref | GoogleScholarGoogle Scholar |
Nilsen ET, Orcutt DM (1996) ‘Physiology of plants under stress – abiotic factors.’ (John Wiley and Sons: New York)
Parra A, Ramírez DA, Resco V, Velasco A, Moreno JM (2012) Modifying rainfall patterns in a Mediterranean shrubland: system design, plant responses, and experimental burning. International Journal of Biometeorology
| Modifying rainfall patterns in a Mediterranean shrubland: system design, plant responses, and experimental burning.Crossref | GoogleScholarGoogle Scholar | in press.
Pasho E, Camarero JJ, de Luis M, Vicente-Serrano SM (2011) Impacts of drought at different time scales on forest growth across a wide climatic gradient in north-eastern Spain. Agricultural and Forest Meteorology 151, 1800–1811.
| Impacts of drought at different time scales on forest growth across a wide climatic gradient in north-eastern Spain.Crossref | GoogleScholarGoogle Scholar |
Paula S, Pausas JG (2006) Leaf traits and resprouting ability in the Mediterranean basin. Functional Ecology 20, 941–947.
| Leaf traits and resprouting ability in the Mediterranean basin.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Lloret F, Montoya R (2001) Severe drought effects on Mediterranean flora in Spain. Forest Science 47, 214–218.
Pereira JS, Chaves MM (1995) Plant responses to drougth under climate change in Mediterranean-type ecosystems. In ‘Global change and Mediterranean-type ecosystems’. (Eds JM Moreno, WC Oechel) pp. 140–160. (Springer-Verlag: New York)
Pérez Latorre AVP, Cabezudo B (2002) Use of monocharacteristic growth forms and phenological phases to describe and differentiate plant communities in Mediterranean-type ecosystems. Plant Ecology 161, 231–249.
| Use of monocharacteristic growth forms and phenological phases to describe and differentiate plant communities in Mediterranean-type ecosystems.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Garnier E (2007) Ecological significance of inherent variation in relative growth rate and its components. In ‘Handbook of functional plant ecology’. (Eds FI Pugnaire, F Valladares) pp. 67–100. (CRC Press, Taylor & Francis Group: New York)
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Puigdefábregas J (1998) Ecological impacts of global change on drylands and their implications for desertification. Land Degradation and Development 9, 393–406.
| Ecological impacts of global change on drylands and their implications for desertification.Crossref | GoogleScholarGoogle Scholar |
Resco V, Ferrio JP, Carreira JA, Calvo L, Casals P, Ferrero-Serrano A, Marcos E, Moreno JM, Ramírez DA, Sebastià MT, Valladares F, Williams DG (2011) The stable isotope ecology of terrestrial plant succession. Plant Ecology & Diversity 4, 117–130.
| The stable isotope ecology of terrestrial plant succession.Crossref | GoogleScholarGoogle Scholar |
Rivas-Martínez S (1979) Brezales y jarales de Europa occidental (revisión fitosociológica de las clases Calluno-Ulicetea y Cisto-Lavanduletea). Lazaroa 1, 5–127.
Ruiz-Robleto J, Villar R (2005) Relative growth rate and biomass allocation in ten woody species with different leaf longevity using phylogenetic independent contrasts (PICs). Plant Biology 7, 484–494.
| Relative growth rate and biomass allocation in ten woody species with different leaf longevity using phylogenetic independent contrasts (PICs).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mvpt1GrsQ%3D%3D&md5=341de47e916cbe668ec9a504d80ccfadCAS |
Santana J, Porto M, Reino L, Beja P (2011) Long-term understory recovery after mechanical fuel reduction in Mediterranean cork oak forests. Forest Ecology and Management 261, 447–459.
| Long-term understory recovery after mechanical fuel reduction in Mediterranean cork oak forests.Crossref | GoogleScholarGoogle Scholar |
Saura-Mas S, Lloret F (2010) Foliar stable carbon and nitrogen isotopes in woody Mediterranean species with different life form and post-fire regeneration. Plant Biology 12, 125–133.
| Foliar stable carbon and nitrogen isotopes in woody Mediterranean species with different life form and post-fire regeneration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslWqt7s%3D&md5=01c5d43b0f2510c394aba5187b4f8ceaCAS |
Schulte PJ, Hinckley AR (1985) A comparison of pressure volume curve data analysis techniques. Journal of Experimental Botany 36, 1590–1602.
| A comparison of pressure volume curve data analysis techniques.Crossref | GoogleScholarGoogle Scholar |
Schulze E-D, Beck E, Müller-Hohenstein K (2005) ‘Plant ecology.’ (Springer-Verlag: Heidelberg)
Serrano L, Peñuelas J, Ogaya R, Save R (2005) Tissue-water relations of two co-occurring evergreen Mediterranean species in response to seasonal and experimental drought conditions. Journal of Plant Research 118, 263–269.
| Tissue-water relations of two co-occurring evergreen Mediterranean species in response to seasonal and experimental drought conditions.Crossref | GoogleScholarGoogle Scholar |
Silva JS, Rego FC (2004) Root to shoot relationship in Mediterranean woody plants from Central Portugal. Biologia 59, 1–7.
Tognetti R, Raschi A, Jones MB (2002) Seasonal changes in tissue elasticity and water transport efficiency in three co-occurring Mediterranean shrubs under natural long-term CO2 enrichment. Functional Plant Biology 29, 1097–1106.
| Seasonal changes in tissue elasticity and water transport efficiency in three co-occurring Mediterranean shrubs under natural long-term CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |
Turner NC (1988) Measurement of plant water status by the pressure chamber technique. Irrigation Science 9, 289–308.
| Measurement of plant water status by the pressure chamber technique.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Jarvis PG (1982) ‘Water in tissues and cells. Vol. 12.’ (Springer-Verlag: Berlin)
Unger S, Máguas C, Pereira JS, David TS, Werner C (2012) Interpreting post-drought rewetting effects on soil and ecosystem carbon dynamics in a Mediterranean oak savannah. Agricultural and Forest Meteorology 154–155, 9–18.
| Interpreting post-drought rewetting effects on soil and ecosystem carbon dynamics in a Mediterranean oak savannah.Crossref | GoogleScholarGoogle Scholar |
Vázquez A, Moreno JM (2001) Spatial distribution of forest fires in Sierrra de Gredos (Central Spain). Forest Ecology and Management 147, 55–65.
| Spatial distribution of forest fires in Sierrra de Gredos (Central Spain).Crossref | GoogleScholarGoogle Scholar |
Waring RH, Cleary BD (1967) Plant moisture stress: evaluation by pressure bomb. Science 155, 1248–1254.
| Plant moisture stress: evaluation by pressure bomb.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvmtlWgtA%3D%3D&md5=fb61889ba8106c83579528a1d5c1d5baCAS |
Werner C, Máguas C (2010) Carbon isotope discrimination as a tracer of functional traits in a Mediterranean macchia plant community. Functional Plant Biology 37, 467–477.
| Carbon isotope discrimination as a tracer of functional traits in a Mediterranean macchia plant community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFKnu7Y%3D&md5=b1f3b99caa3559a655d547d0ee69d663CAS |
Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88, 486–493.
