Changes in foliar carbon isotope composition and seasonal stomatal conductance reveal adaptive traits in Mediterranean coppices affected by drought

Abstract

We estimated water-use efficiency and potential photosynthetic assimilation of Holm oak (Quercus ilex L.) on slopes of NW and SW aspects in a replicated field test examining the effects of intensifying drought in two Mediterranean coppice forests. We used standard techniques for quantifying gas exchange and carbon isotopes in leaves and analyzed total chlorophyll, carotenoids and nitrogen in leaves collected from Mediterranean forests managed under the coppice system. We postulated that responses to drought of coppiced trees would lead to differential responses in physiological traits and that these traits could be used by foresters to adapt to predicted warming and drying in the Mediterranean area. We observed physiological responses of the coppiced trees that suggested acclimation in photosynthetic potential and water-use efficiency: (1) a significant reduction in stomatal conductance (p<0.01) was recorded as the drought increased at the SW site; (2) foliar δ¹³C increased as drought increased at the SW site (p<0.01); (3) variations in levels of carotenoids and foliar nitrogen, and differences in foliar morphology were recorded, and were tentatively attributed to variation in photosynthetic assimilation between sites. These findings increase knowledge of the capacity for acclimation of managed forests in the Mediterranean region of Europe.

Keywords

Mediterranean forest ecosystems / forest acclimation / stable isotopes / leaf gas exchanges / water-use efficiency / foliar traits / adaptive silviculture

References

[1] Amorini E, Bruschini S, Cutini A, Fabbio G, Manetti MC. Silvicultural treatment of Holm oak (Quercus ilex L.) coppices in Southern Sardinia: thinning and related effects on stand structure and canopy cover. Annals of the Forestry Centre of the Agricultural Research Council (CRA-SEL), 1996, 27: 167-175.

[2] Beerling DJ, Heath J, Woodward FI, Mansfield TA. Interaction in trees: observations and mechanism. New Phytologist, 1996, 134: 235-242.

[3] Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon WT, Laprise R, et al. Solomon S, Quin D, Manning M, Chen Z, Marquis M, Averyt KB, Tingor M, Miller HL, et al. Regional climate projections. Climate Change 2007: The Physical Science Basis. Contributions of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. 2007, Cambride, United Kingdom/New York, NY: Cambridge University Press

[4] Ciancio O, Corona P, La Monaca A, Portoghesi L, Travaglini D. Conversion of clearcut beech coppices into high forests with continuous cover: A case study in central Italy. Forest Ecology and Management, 2006, 22: 235-240.

[5] Cordell S, Goldstein G, Mueller-Dombois D, Webb D, Vitousek PM. Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: role of phenotypic plasticity. Oecologia, 1998, 113: 188-196.

[6] Cordell S, Goldstein G, Meinzer FC, Handley L. Allocation of nitrogen and carbon in leaves of Metrosideros polymorpha regulates carboxylation capacity and δ¹³C along altitudinal gradient. Functional Ecology, 1999, 13: 811-818.

[7] Cubera E, Moreno G. Effect of single Quercus ilex trees upon spatial and seasonal changes in soil water content in dehesas of central western Spain. Annals of Forest Science, 2007, 64: 355-364.

[8] Damesin C, Rambal S, Joffre R. Seasonal and annual changes in leaf δ¹³C in two co-occurring Mediterranean oaks: relations to leaf growth and drought progression. Functional Ecology, 1998, 12: 778-785.

[9] David TS, Henriques MO, Kurz-Besson C, Nunes J, Valente F, Vaz M, Pereira JS, Siegwolf R, Chaves MM, Gazarini LC, et al. Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiology, 2007, 27: 793-803.

[10] De Lillis M, Matteucci G, Valentini R. Carbon assimilation, nitrogen, and photochemical efficiency of different Himalayan tree species along an altitudinal gradient. Photosynthetica, 2004, 42: 597-605.

[11] Di Matteo G, De Angelis P, Scarascia Mugnozza G. Application of isotope discrimination techniques to evaluate the functional response of Mediterranean coppices to high-forest conversion cut. Forest@, 2005, 2: 367-377.

[12] Ehleringer JR, Cerling TE. Atmospheric CO₂ and the ratio of intercellular to ambient CO₂ concentrations in plants. Tree Physiology, 1995, 15: 105-111.

[13] Evans JR. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia, 1989, 78: 9-19.

[14] Fabbio G, Cutini A, Mascia V. Silvicultural treatment of holm oak coppices (Quercus ilex L.) in Southern Sardinia: effects of canopy and crop thinning on microclimate. Annals of the Forestry Centre of the Agricultural Research Council (CRA-SEL), 1996, 27: 55-63.

[15] Faria T, Silverio D, Breia E, Cabral R, Abadia A, Abadia J, Pereira JS, Chaves MM. Differences in the response of carbon assimilation to summer stress (water deficits, high light and temperature) in four Mediterranean tree species. Physiologia Plantarum, 1998, 102: 419-429.

[16] Farquhar GD, O’Leary MH, Berry JA. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology, 1982, 9: 121-137.

[17] Field C, Mooney HA. Givinish TJ. The photosynthesis-nitrogen relationship in wild plants. On the Economy of Plants Form and Function. 1986, Cambridge: Cambridge University Press, 25 55

[18] Friend AD, Woodward FI, Switsur VR. Field measurements of photosynthesis, stomatal conductance, leaf nitrogen and δ¹³C along altitudinal gradients in Scotland. Functional Ecology, 1989, 3: 117-122.

[19] Gale J. The availability of carbon dioxide for photosynthesis at high altitudes: theoretical considerations. Ecology, 1972, 53: 494-497.

[20] Gale J. Plants and altitude — revisited. Annals of Botany, 2004, 94 199

[21] Garzia-Plazaola JI, Faria T, Abadia J, Abadia A, Chaves MM, Pereira JS. Seasonal changes in xanthophylls composition and photosynthesis in cork oak (Quercus suber L.) leaves under Mediterranean climate. Journal of Experimental Botany, 1997, 48: 1667-1674.

[22] Gratani L, Covone F, Larcher W. Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees, 2006, 20: 549-558.

[23] Hikosaka K, Nagamatsu D, Ishii HS, Hirose T. Photosynthesis-nitrogen relationships in species at different altitudes on Mount Kinablau, Malaysia. Ecological Research, 2002, 17: 305-313.

[24] Hultine KR, Marshall JD. Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia, 2000, 123: 32-40.

[25] Klein T, Di Matteo G, Rotemberg E, Cohen S, Yakir D. Differential ecophysiological response of a major Mediterranean pine species across a climatic gradient. Tree Physiology, 2013, 33: 26-36.

[26] Kogami H, Hanba YT, Kibe T, Terashima I, Masuzawa T. CO₂ transfer conductance, leaf structure and carbon isotope composition of Poly gonum cuspidatum leaves from low and high altitudes. Plant, Cell and Environment, 2001, 24: 529-538.

[27] Körner C, Farquhar GD, Roksandic Z. A global survey of carbon isotope discrimination in plants from high altitude. Oecologia, 1988, 74: 623-632.

[28] Körner C, Farquhar GD, Wong SC. Carbon isotope discrimination by follows latitudinal and altitudinal trends. Oecologia, 1991, 88: 30-40.

[29] Kyparissis A, Petropoulou Y, Manetas Y. Summer survival of leaves in a soft-leaved shrub (Phlomis fruticosa L., Labiatae) under Mediterranean field conditions: avoidance of photoinhibitory damage through decreased chlorophyll contents. Journal of Experimental Botany, 1995, 46: 1825-1831.

[30] Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic apparatus biomembranes. Methods in Enzymology, 1987, 148: 349-382.

[31] Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, Garcia-Gonzalo J, Seidl R, Delzon S, Corona P, Kolstro M, Lexer MJ, Marchetti M. Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Forest Ecology and Management, 2010, 259(4): 698-709.

[32] Marshall JD, Zhang J. Carbon isotope discrimination and water use efficiency of native plants of the north-central Rockies. Ecology, 1994, 75: 1887-1895.

[33] Maxime C, Hendrik D. Effects of climate on diameter growth of cooccurring Fagus sylvatica and Abies alba along an altitudinal gradient. Trees, 2011, 25: 265-276.

[34] Morandini R. (Coordinator). 1998. 1996: Special issue on Improvement of Mediterranean coppices. MEDCOP project. Annals of the Forestry Centre of the Agricultural Research Council (CRA-SEL), 27: 224 pp.

[35] Morecroft MD, Woodward FI, Marrs RH. Altitudinal trends in leaf nutrient contents, leaf size and δ¹³C of Alchemilla alpina. Functional Ecology, 1992, 6: 730-740.

[36] Morecroft MD, Woodward FI. Experiments on the causes of altitudinal differences in leaf nutrient contents, size, and δ¹³C of Alchemilla alpina. New Phytologist, 1996, 134: 471-479.

[37] Núñez-Olivera E, Martínez-Abaigar J, Escudero JC. Chlorophyll content of a Mediterranean shrub (Cistus ladanifer L.) over a latitude and altitude gradient in the Iberian Peninsula. Photosynthetica, 1994, 30: 133-142.

[38] Oliveira G, Penuelas J. Comparative photochemical and phenomorphological responses to winter stress of an evergreen (Quercus ilex L.) and a semi-deciduous (Cistus albidus L.) Mediterranean woody species. Acta Oecologica, 2000, 21: 97-107.

[39] Panek JA, Waring RH. Carbon isotope variation in Douglas-fir foliage: improving the δ¹³C-climate relationship. Tree Physiology, 1995, 15: 657-663.

[40] Paridari IC, Jalali SG, Sonboli A, Zarafshar M, Bruschi P. Leaf macroand micro-morphological altitudinal variability of Carpinus betulus in the Hyrcanian forest (Iran). Journal of Forestry Research, 2013, 24: 301-307.

[41] Piper FI, Fajardo A. No evidence of carbon limitation with tree age and height in Nothofagus pumilio under Mediterranean and temperate climate conditions. Annals of Botany, 2011, 108: 907-917.

[42] Sah SP, Brume R. Altitudinal gradients of natural abundance of stable isotopes of nitrogen and carbon in the needles and soil of a pine forest in Nepal. Journal of Forest Science, 2003, 49: 19-26.

[43] Sakata T, Yokoi Y. Analysis of the O₂ dependency in leaf-level photosynthesis of two Reynoutria japonica populations growing at different altitudes. Plant, Cell and Environment, 2002, 25: 65-74.

[44] Shi Z, Shirong L, Xingliang L, Centritto M. Altitudinal variation in photosynthetic capacity, diffusional conductance and δ¹³C of butterfly bush (Buddleja davidii) plants growing at high elevations. Physiologia Plantarum, 2006, 128: 722-731.

[45] Sun ZJ, Livingston NJ, Guy RD, Ethier GJ. Stable carbon isotopes as indicators of increased water use efficiency and productivity in white spruce (Picea glauca (Moench) Voss)) seedlings. Plant, Cell and Environment, 1996, 19: 887-894.

[46] Terashima I, Masuzawa T, Ohba H, Yokoi Y. Is photosynthesis suppressed at higher elevation because of low CO₂ pressure?. Ecology, 1995, 76: 2663-2668.

[47] Tognetti R, Cherubini P, Marchi S, Raschi A. Leaf traits and tree rings suggest different water-use and carbon assimilation strategies by twooccurring Quercus species in a Mediterranean mixed-forest stand in Tuscany, Italy. Tree Physiology, 2007, 27: 1741-1751.

[48] Valentini R, Scarascia Mugnozza G, Ehleringer JR. Hydrogen and carbon isotope ratios of selected species of a Mediterranean macchia ecosystem. Functional Ecology, 1992, 6: 627-631.

[49] Van De Water PK, Leavitt SW, Betancourt JL. Leaf δ¹³C variability with elevation, slope aspect, and precipitation in the southwest United States. Oecologia, 2002, 132: 332-343.

[50] Vitousek PM, Field CB, Matson PA. Variation in foliar δ¹³C in Hawaiian Metrosideros polymorpha: a case of internal resistance?. Oecologia, 1990, 84: 362-370.