Seasonal changes in the physiological activity of regeneration under a natural light gradient in a Pinus pinea regular stand

Marta Pardos, Jaim Puértolas, Guillermo Madrigal, Enrique Garriga, Santiago de Blas, Rafael Calama

Abstract


Seasonal courses of chlorophyll a fluorescence, gas exchange parameters and water status, joined to environmental variables, were measured in four age classes of stone pine (Pinus pinea L.) natural regeneration under a natural light gradient in a stone pine regular stand throughout 2007 and 2008. One-year old seedlings were worse adapted to the extreme drought conditions recorded in summer (especially in 2008), showing lower predawn and midday Fv/Fm values, slightly lower photosynthetic rates at midday, lower PSII values, lower water potentials (pd andmin), and high mortality (90%). The oldest seedlings (class 4, 51-200 cm high), although they do not experience the lowest min in July 2008, were not able to maintain a positive carbon gain at midday, even showing the lowest photosynthetic rates. However, they rapidly recovered once the climatic conditions were softened in early autumn. During late autumn low Fv/Fm values were found especially in one-year old seedlings, indicating that maximal photochemical efficiency of PSII is sensitive to the autumn temperatures below cero recorded during both years. Thus, stone pine regeneration adapts its physiology to the seasonal course of temperature and water availability, showing a different photosynthetic performance according to age class. However, seedling physiology is not affected by the natural light gradient found in the studied stand, probably related to the low variability recorded in GSF values and the low density of the stand. We suggest that such low stand densities cannot assure one-year old seedlings’ survival, but are sufficient for older seedlings.

Keywords


Stone pine; natural regeneration; drought; cold; gas exchange; photochemical efficiency; water status

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References


Annaz D., Karmiloff-Smith A., Johnson M.H., Thomas M.S.C., 2009. A cross-syndrome study of the development of holistic face recognition in children with autism, Down syndrome, and Williams syndrome. J Exp Child Psychol 102, 456-486. http://dx.doi.org/10.1016/j.jecp.2008.11.005 PMid:19193384

Aussenac G., 2000. Interactions between forest stands and microclimate: ecophysiological aspects and consequences for silviculture. Ann For Sci 57, 287-301. http://dx.doi.org/10.1051/forest:2000119

Barbeito I., Pardos M., Calama R., Cañellas I., 2008. Effect of stand structure on Stone pine (Pinus pinea L.) regeneration dynamics. Forestry. doi: 10.1093/forestry/cpn037. http://dx.doi.org/10.1093/forestry/cpn037

Bond B.J., 2000. Age-related changes in photosynthesis of oody plants. Trends Pl Sci Rev 5, 349-353. http://dx.doi.org/10.1016/S1360-1385(00)01691-5

Calama R., Montero G., 2007. Cone and seed production from stone pine (Pinus pinea L.) stands in Central Range (Spain). Eur J For Res 126, 23-35 . http://dx.doi.org/10.1007/s10342-005-0100-8

Castro J., Zamora R., Hódar J.A., Gómez J.M., 2005. Alleviation of summer drought boosts establishment success of Pinus sylvestris in a Mediterranean mountain: an experimental approach. Plant Ecol 181, 191-202. http://dx.doi.org/10.1007/s11258-005-6626-5

Chaves M.M., Pereira J.S., Maroco J., Rodrigues M.L., Ricardo C.P.P., Osorio M.L., Carvalho I., Faria T., Pnheiro C., 2002. How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot-London 89, 907-916. http://dx.doi.org/10.1093/aob/mcf105

Chaves A.R.M., Ten-Caten A., H.A., Ribeiro A., Damatta F.M., 2008, Seasonal changes in photoprotective mechanisms of leaves from shaded and unshaded field-grown coffe (Coffea Arabica L.) trees. Trees 22, 351-361. http://dx.doi.org/10.1007/s00468-007-0190-7

Climent J., Costa E Silva F., Chambel M.R., Pardos M., Almeida M.H., 2009. Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting ecological niches. Ann For Sci 66(4), 407. http://dx.doi.org/10.1051/forest/2009016

Cordeiro Y.E.M., Pinheiro H.A., Dos Santos Filho B.G., Corrêa S.S., E Silva J.R.R., Dias-Filho M.B., 2009. Physiological and morphological responses of young mahogany (Swietenia macrophyllaa King) plants to drought. For Ecol Managem 258, 1449-1455.

Dawson T.E., Ehleringer J.R., 1993. Gender-specific physiology, carbon isotope discrimination and habitat distribution in boxelder. Acer negundo. Ecology 74, 798-815. http://dx.doi.org/10.2307/1940807

Dawson T.E., 1996. Determining water use by trees and forests from isotopic, energy balance and transpiration analysis: the roles of tree size and hydraulic lift. Tree Physiol 16, 263-272. http://dx.doi.org/10.1093/treephys/16.1-2.263 PMid:14871771

Delaney H.D., Maxwell S.E., 1981. On using analysis of covariance in repeated measures designs. Multivariate Behavioral Res 16, 105-123. http://dx.doi.org/10.1207/s15327906mbr1601_6

Demmig-Adams B., Adams W.W., Witer K., Meyer A., Schreiber U., Pereira J.S., Krüger A, Czygan F.C., Lagne O.L., 1989. Photochemical efficiency of photosystem II, photon yield of O2 evolution, photosynthesis capacity and carotenoid composition during the midday depression of net CO2 uptake in Arbutus under grown in Portugal. Planta 177, 377-387. http://dx.doi.org/10.1007/BF00403596

Donovan L.A., Ehleringer J.R., 1991. Ecophysiological differences among juvenile and reproductive plants of several woody species. Oecologia 86, 594-597. http://dx.doi.org/10.1007/BF00318327

Epron D., Dreyer E., Bréda N., 1992. Photosynthesis of oak trees [Quercus petraea (Matt) Liebl] during drought under field conditions: diurnal courses of net CO2 assimilation and photochemical efficiency of photosystem II. Plant Cell Environ 15, 809-820. http://dx.doi.org/10.1111/j.1365-3040.1992.tb02148.x

Filella I., Llusià J., Piñol J., Peñuelas J., 1998 Leaf gas exchange and fluorescence of Phyllirea latifolia, Pistacia lentiscus and Quercus ilex saplings in severe drought and high temperature conditions. Environ Exp Bot 39, 213-220. http://dx.doi.org/10.1016/S0098-8472(97)00045-2

Flexas J., Medrano H., 2002. Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitation revisited. Ann Bot 89, 183-189. http://dx.doi.org/10.1093/aob/mcf027

Fotelli M.N., Radoglou K.M., Constantinidou H.I.A., 2000. Water stress responses of seedlings of four Mediterranean oak species. Tree Physiol 20, 1065-1075. http://dx.doi.org/10.1093/treephys/20.16.1065 PMid:11269958

García-Plazaola J.I., Faria T., Abadía J., Abadía A., Chaves M.M., Pereira J.S., 1997. Seasonal changes in xantophyll composition and photosynthesis of Cork oak (Quercus suber L.) leaves under mediterraean climate. J Exp Bot 48, 1667-1674.

Hernández-Santana V., Martínez-Vilalta J., Martínez-Fernández J., Williams M., 2009. Evaluating the effect of drier and warmer conditions on water use by Quercus pyrenaica. For Ecol Managem 258, 1719-1730.

Irvine J., Perks P., Magnani F., Grace J. 1998. The response of Pinus sylvestris to drought: stomatal control of transpiration and hydraulic conductance. Tree Physiol 18, 393-402. http://dx.doi.org/10.1093/treephys/18.6.393 PMid:12651364

Keenan T., García R., Friend A.A., Zaehle S., Gracia C., Sabaté S., 2009. Improved understanding of drought control seasonal variation in Mediterranean forest canopy CO2 and water fluxes through combined in situ measurements and ecosystem modelling. Biogeosciences 6, 1423-1444. http://dx.doi.org/10.5194/bg-6-1423-2009

Kolb T.E., Stone J.E., 2000. Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine-oak forest. Tree Physiol 20, 1-12. http://dx.doi.org/10.1093/treephys/20.1.1 PMid:12651521

Kozlowski T.T., Pallardy S.G., 2007. Physiology of woody plants. Academic Press, San Diego, California. 411 pp.

Latham R.E., 1992. Co-occurring tree species change rank in seedling performance with resources varied experimentally. Ecology 73(6), 2129-2144. http://dx.doi.org/10.2307/1941461

Llusiá J., Peñuelas J., 2000. Seasonal patterns of terpene content and emission from seven Mediterranean woody species in field conditions.

Manetas Y., Petropoulou Y., Stamatakis K., Nikolopoulos D., Levizou E., Psaras G., Karabourniotis G., 1997. Beneficial effects of enhaced UV-B radiation under field conditions: improvement of needle water relations and survival capacity of Pinus pinea L. seedlings during the dry Mediterranean summer. Plant Ecol 128, 100-108. http://dx.doi.org/10.1023/A:1009706806427

Martínez-Ferri E., Balaguer L., Valladares F., Chico J.M., Manrique E., 2000. Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20, 131-138 http://dx.doi.org/10.1093/treephys/20.2.131 PMid:12651481

Masetti C., Mencuccini M., 1991. Régéneration naturelle du pin pignon (Pinus pinea L.) dans la Pineta Granducale di Alberese (Parco Naturale della Maremma, Toscana, Italie). Ecol Mediterr 17, 103-118 .

Matzner S.L., Rice K.J., Richards J.H., 2003. Patterns of stomatal conductance among blue oak (Quercus douglassi) size classes and populations: implications for seedling establishment. Tree Physiol 23, 777-784. http://dx.doi.org/10.1093/treephys/23.11.777 PMid:12839731

Mayseyk K., Grünzweig J.M., Rotenberg E., Yakir D., 2008. Respiration acclimation contributes to high carbon-use efficiency in a seasonally dry pine forest. Glob. Change Biol 14, 1553-1567. http://dx.doi.org/10.1111/j.1365-2486.2008.01604.x

Mayseyk K., Lin T., Rotenberg E., Grünzweig J.M., Schwartz A., Yakir D., 2008. Physiology-phenology interactions in a productive semi-arid pine forest. New Phytol 178, 603-616. http://dx.doi.org/10.1111/j.1469-8137.2008.02391.x PMid:18331428

Mendoza I., Zamora R., Castro J., 2009. A seeding experiment for testing tree-community recruitment under variable environments: implications for forest regeneration and conservation in mediterranean habitats. Biolog Conservat 142, 1491-1499. http://dx.doi.org/10.1016/j.biocon.2009.02.018

Montero G., Calama R., Ruiz-Peinado R., 2008. Selvicultura de Pinus pinea L. In: Compendio de selvicultura aplicada en España (Serrada R., Montero G., Reque J.A., eds). INIA, MEC, Madrid. pp. 432-470.

Moser E.B., Saxton A.M., Pezeshki S.R., 1990. Repeated measures analysis of variance: application to tree research, Can J For Res 20, 524-535. http://dx.doi.org/10.1139/x90-069

Ogaya R., Peñuelas J., 2003a. Comparative seasonal gas exchange and chlorophyll fluorescence of two dominant woody species in a holm oak forest. Flora 198, 132-141. http://dx.doi.org/10.1078/0367-2530-00085

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

Oliveira G., Peñuelas J., 2000. Comparative photochemical and phenomorphological responses to winter stress of an evergreen (Quercus ilex) and a semi-deciduous (Cistus albidus) Mediterranean woody species. Acta Oecol 21, 97-107. http://dx.doi.org/10.1016/S1146-609X(00)00121-1

Oliveira G., Peñuelas J., 2001. Allocation of absorbed light energy into photochemistry and dissipation in a semi-deciduous and an evergreen Mediterranean woody species during winter. Aust J Plant Physiol 28, 471-480.

Oliveira G., Peñuelas J., 2004. The effect of winter cold stress on photosynthesis and photochemical efficiency of PSII of two Mediterranean woody species- Cistus albidus and Quercus ilex. Plant Ecol 175, 179-191. http://dx.doi.org/10.1007/s11258-005-4876-x

Öquist G., Gardeström P., Huner N.P.A., 2001 Metabolic changes during cold acclimation and subsequent freezing and thawing. In: Conifer cold hardiness (Bigras F.J., Colombo S.J., eds). Kluwer Academic Publishers, Dordrecht,The Netherlands. pp. 137-163.

Panek J.A., Goldstein A.H., 2001. Response of stomatal conductance to drought in ponderosa pine: implications for carbon and ozone uptake. Tree Physiol 21, 337-344. http://dx.doi.org/10.1093/treephys/21.5.337 PMid:11262925

Pardos M., Ruiz Del Castillo J., Cañellas I., Montero G., 2005. Ecophysiology of natural regeneration of forest stands in Spain. Invest Agrar: Sist Recur For 14, 434-445.

Peñuelas J., Llusiá J., 2002. Linking photorespiration, monoterpenes and plant termotolerance. New Phytol 155, 227-237. http://dx.doi.org/10.1046/j.1469-8137.2002.00457.x

Peñuelas J., Prieto P., Beier C. et al. 2007. Response of plant species richness and primary productivity in shrublands along a north-south gradient in Europe to seven years of experimental warming and drought. Reductions in primary productivity in the heat and drought year of 2003. Glob Change Biol 13, 2563-2581. http://dx.doi.org/10.1111/j.1365-2486.2007.01464.x

Petropoulou Y., Kyparissis A., Nikolopoulos D., Manetas Y., 1995. Enhanced UV-B radiation alleviates the adverse effects of summer drought in two Mediterranean pines under field conditions. Physiol Plantar 94, 37-44. http://dx.doi.org/10.1111/j.1399-3054.1995.tb00781.x

Poyatos R., Llorens P., Piñol J., Rubio C., 2008. Response of Scots pine (Pinus sylvestris L.) and pubescent oak (Quercus pubescens Willd.) to soil and atmospheric water deficits under Mediterranean mountain climate. Ann For Sci 65, 306. http://dx.doi.org/10.1051/forest:2008003

Powers M.D., Pregitzer K.S., Palik B.J., Webster C.R., 2009. Water relations of pine seedlings in contrasting overstory environments. For Ecol Managem 258, 1442-1448.

Prieto P., Peñuelas J., Llusià J., Asensio D., Estiarte M., 2009. Effects of long-term experimental night-time warming and drought on photosynthesis, Fv/Fm and stomatal conductance in the dominant species of a Mediterranean shrubland. Acta Physiol Plant 31, 729-739. http://dx.doi.org/10.1007/s11738-009-0285-4

Rodríguez-Calcerrada J., Pardos J.A., Gil L., Aranda I., 2007. Summer field performance of Quercus petraea (Matt.) Liebl and Quercus pyrenaica Willd seedlings, planted in three sites with contrasting canopy cover. New Forests 33, 67-80. http://dx.doi.org/10.1007/s11056-006-9014-7

Resco De Dios V., Fishcher C., Colinas C., 2007. Climate change effects on mediterranean forests and preventive measurements. New Forests 33, 29-40. http://dx.doi.org/10.1007/s11056-006-9011-x

SAS Institute, 1988. SAS/STAT users guide. Release 6.03 edition. Cary, USA.

Savé R., Castell C., Terradas J., 1999. Gas exchange and water relations. In: Ecology of Mediterranean evergreen oak forests (Rodá F., Retana J., Gracia C.A., Bellot J., eds). Springer-Verlag, Berlin. pp. 135-147. http://dx.doi.org/10.1007/978-3-642-58618-7_10

Tenhunen J.D., Serra A.S., Harley P.C., Dougherty R.L., Reynolds J.F., 1990. Factors influencing carbon fixation and water-use by Mediterranean sclerophyll shrubs during summer drought. Oecologia 82, 381-393. http://dx.doi.org/10.1007/BF00317487

Tenhunen J.D., Lange O.L., Braun M., 1981. Midday stomatal closure in mediterranean type sclerophylls under simulated habitat conditions in an environmental chamber. II. Effect of the complex of leaf temperature and air humidity on gas exchange of Arbutus unedo and Quercus ilex. Oecologia 50, 5-11. http://dx.doi.org/10.1007/BF00378788

Thomas S.C., 2010. Photosynthetic capacity peaks at intermediate size in temperate deciduos trees. Tree Physiol 30, 555-573. http://dx.doi.org/10.1093/treephys/tpq005 PMid:20335160

Thomas M.S.C., Annaz D., Ansari D., Serif G., Jarrold C., Karmiloff-Smith A., 2009. Using developmental trajectories to understand developmental disorders. J Speech, Language, and Hearing Res 52, 336-358. http://dx.doi.org/10.1044/1092-4388(2009/07-0144)

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

Valladares F., Dobarro I., Sánchez-Gómez D., Pearcy R.W., 2005. Photoinhibition and drought in mediterranean woody saplings: scaling effects and interactions in sun and shade phenotypes. J Exp Bot 56, 483-494. http://dx.doi.org/10.1093/jxb/eri037 PMid:15569705

Werner C., Correia O., Beyschlag W., 1999. Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecol 20, 15-23. http://dx.doi.org/10.1016/S1146-609X(99)80011-3

Zunzunegui M., Fernández-Baco L., Díazbarradas M.C., García.Novo F., 1999. Seasonal changes in photochemical efficiency in leaves of Halimium halimifolium, a Mediterranean semideciduous shrub. Photosynthetica 31, 17-31. http://dx.doi.org/10.1023/A:1007058611140

Zweifel R., Zimmermann L., Newbery D.M., 2005. Modelling tree water deficit from microclimate: an approach to quantifying drought stress. Tree Physiol 25, 147-156 http://dx.doi.org/10.1093/treephys/25.2.147 PMid:15574396




DOI: 10.5424/fs/2010193-9102

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