Abstract
Implications of the differences in leaf life span are still subject to debate in the field of ecophysiology. Since leaf traits associated with these differences may be decisive for determining the distribution of tree species, this topic is particularly relevant in the context of climate change. This study analyzes the effects of the differences in leaf life span on premature losses of leaf area owing to insect herbivory and to abiotic stress. Loss of leaf area may be an important determinant of total leaf carbon assimilation. Seven Mediterranean tree species, distributed on four sites with different climates were studied. The species exhibited strong differences in leaf life span and in leaf traits, especially leaf mass per unit area. Premature leaf area losses were estimated in response to insect herbivory and summer drought over two years. The results revealed that, despite having older leaf cohorts with more damage, species with longer leaf duration had lower area lost to herbivores and less damage due to accelerated senescence during the summer drought. With respect to the predicted increase in water stress, deciduous species are at a disadvantage due to their high premature loss of leaf area and thus loss of photosynthetic capacity.
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Abràmoff M, Magalhães P, Ram S (2004) Image processing with imageJ. Biophoton Int 11:36–42
Agrawal AA, Weber MG (2015) On the study of plant defense and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991
Anjum SA, Xie X, Wang L, Farrukh-Saleem M, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032
Aranda I, Ramírez-Valiente JA, Rodríguez-Calcerrada J (2014) Características funcionales que influyen en la respuesta a la sequía de las especies del género Quercus: variación inter- e intra-específica. Ecosistemas 23:27–36
Barbeta A, Mejía-Chang M, Ogaya R, Voltas J, Dawson TE, Peñuelas J (2015) The combined effects of a long-term experimental drought and an extreme drought on the use of plant-water sources in a Mediterranean forest. Glob Change Biol 21:1213–1225
Buras A, Schunk C, Zeiträg C, Herrmann C, Kaiser L, Lemme H, Straub C, Taeger S, Gößwein S, Klemmt HJ, Menzel A (2018) Are Scots pine forest edges particularly prone to drought-induced mortality? Environ Res Lett 13:025001
Caneva G, Garlotta G, Cancellieri L (2009) Tree roots and damages in the Jewish catacombs of Villa Torlonia (Roma). J Cult Herit 10:53–62
Cano FJ, Sánchez-Gómez D, Rodríguez-Calcerrada J, Warren CR, Gil L, Aranda I (2013) Effects of drought on mesophyll conductance and photosynthetic limitations at different tree canopy layers. Plant Cell Environ 36:1961–1980
Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367
Carnicer J, Barbeta A, Sperlich D, Coll M, Peñuelas J (2013) Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale. Front Plant Sci 4:409
Castell C, Terradas J, Tenhunen JD (1994) Water relations, gas exchange, and growth of resprouts and mature plant shoots of Arbutus unedoL. and Quercus ilex L. Oecologia 98:201–211
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558:531–539
Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536
Edwards EJ, Chatelet DS, Sack L, Donoghue MJ (2014) Leaf life span and the leaf economic spectrum in the context of whole plant architecture. J Ecol 102:328–336
Emberger L (1932) Sur une formule climatique et ses applications en botanique. La Métereologie 92–93:1–10
Falster DS, Reich PB, Ellsworth DS, Wright IJ, Westoby M, Oleksyn J, Lee TD (2011) Lifetime return on investment increases with leaf lifespan among 10 Australian woodland species. New Phytol 193:409–419
Flexas J, Diaz-Espejo A, Gago J, Gallé A, Galmés J, Gulías J, Medrano H (2014) Photosynthetic limitations in Mediterranean plants: a review. Environ Exp Bot 103:12–23
Gea-Izquierdo G, Viguera B, Cabrera M, Cañellas I (2014) Drought induced decline could portend widespread pine mortality at the xeric ecotone in managed Mediterranean pine-oak woodlands. For Ecol Manag 320:70–82
González-Zurdo P, Escudero A, Babiano J, García-Ciudad A, Mediavilla S (2016a) Costs of leaf reinforcement in response to winter cold in evergreen species. Tree Physiol 36:273–286
González-Zurdo P, Escudero A, Nuñez R, Mediavilla S (2016b) Losses of leaf area owing to herbivory and early senescence in three tree species along a winter temperature gradient. Int J Biometeorol 60:1661–1674
Günthardt-Goerg MS, Vollenweider P (2007) Linking stress with macroscopic and microscopic leaf response in 386 trees: New diagnostic perspectives. Environ Pollut 147:467–488
Hammond WM, Yu K, Wilson LA, Will RE, Anderegg WRL, Adams HD (2019) Dead or dying? Quantifying the point of no return hydraulic failure in drought-induced tree mortality. New Phytol 223:1834–1843
Hartmann H, Moura CF, Anderegg WRL, Ruehr NK, Salmon Y, Allen CD, Arndt SK, Breshears DD, Davi H, Galbraith D, Ruthrof KX, Wunder J, Adams HD, Bloemen J, Cailleret M, Cobb R, Gessler A, Grams TEE, Jansen S, Kautz M, Lloret F, O’Brien M (2018) Research frontiers for improving our understanding of drought-induced tree and forest mortality. New Phytol 218:15–28
IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectorial aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, p 1132
Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL (2012) Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiol 160:1719–1727
Jonsson M, Bengtsson J, Gamfeldt L, Moen J, Snäll T (2019) Levels of forest ecosystem services depend on specific mixtures of commercial tree species. Nat Plants 5:141–147
Kaack L, Altaner CM, Carmesin C, Diaz A, Holler M, Kranz C, Neusser G, Odstrcil M, Schenk HJ, Schmidt V, Weber M, Zhang Y, Jansen S (2019) Function and three-dimensional structure of intervessel pit membranes in angiosperms: a review. IAWA J 40:673–702
Kikuzawa K, Lechowicz MJ (2006) Toward synthesis of relationships among leaf longevity, instantaneous photosynthetic rate, lifetime leaf carbon gain, and the gross primary production of forests. Am Nat 168:373–383
Kitajima K, Mulkey S, Samaniego M, Wright J (2002) Decline of photosynthetic capacity with leaf age and position in two tropical pioneer tree species. Am J Bot 89:1925–1932
Kozlov MV, Lanta V, Zverev V, Zvereva EL (2015) Background losses of woody plant foliage to insects show variable relationships with plant functional traits across the globe. J Ecol 103:1519–1528
Kozlowski TT, Kramer PJ, Pallardy SG (1991) The physiological ecology of woody plants. Academic Press, San Diego, p 657
Larcher W (1995) Ecophysiology and stress physiology of functional groups. In: Larcher W (ed) Physiological plant ecology. Springer Verlag, Berlin, pp 340–353
Lawrence R, Potts B, Whitham TG (2003) Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84:1171–1178
Loranger J, Meyer ST, Shipley B, Kattge J, Loranger H, Roscher C, Weisser WW (2012) Predicting invertebrate herbivory from plant traits: evidence from 51 grassland species in experimental monocultures. Ecology 93:2674–2682
Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC, Sohrabi Y (2010) Effect of drought stress on yield, proline and chlorophyll content in three Chickpea cultivars. Aust J Crop Sci 4:580–585
Martínez-Sancho E, VasconezNavas LK, Seidel H, Dorado-Linan I, Menzel A (2017) Responses of contrasting tree functional types to air warming and drought. Forest 8:1–11
Martínez-Vilalta J, Mangiron M, Ogaya R, Sauret M, Serrano L, Peñuelas J, Piñol J (2003) Sap flow of three co-occurring Mediterranean woody species under varying atmospheric and soil water conditions. Tree Physiol 23:747–758
Martínez-Vilalta J, Sala A, Piñol J (2004) The hydraulic architecture of Pinaceae: a review. Plant Ecol 171:3–13
McDowell NN, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DJ, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739
Mediavilla S, Escudero A (2003a) Leaf life span differs from retention time of biomass and nutrients in the crowns of evergreen species. Funct Ecol 1:541–548
Mediavilla S, Escudero A (2003b) Photosynthetic capacity, integrated over the lifetime of a leaf, is predicted to be independent of leaf longevity in some tree species. New Phytol 159:203–211
Mediavilla S, Escudero A (2003c) 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
Mediavilla S, García-Cunchillos I, Andrés-Rivera C, Escudero A (2018a) Losses of leaf area owing to abiotic stress along the leaf economics spectrum: implications for carbon gain at the branch level. Trees 32:559–569
Mediavilla S, Martínez-Ortega MM, Babiano J, Escudero A (2018b) Ontogenetic changes in anti-herbivore defensive traits in leaves of four Mediterranean co-occurring Quercus species. Ecol Res 33:1093–1102
Miller GR, Chen X, Rubin Y, Ma S, Baldocchi DD (2010) Ground water uptake by woody vegetation in a semiarid oak savanna. Water Resour Res 46:W10503
Niinemets U, Poorter L, Wright I, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588
Ogaya R, Peñuelas J (2007) Leaf mass per area ratio in Quercus ilex leaves under a wide range of climatic conditions. The importance of low temperatures. Acta Oecol 31:168–173
Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schäfer KVR (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644
Peñuelas J, Sardans J, Filella I, Estiarte M, Llusià J, Ogaya R, Carnicer J, Bartrons M, Rivas-Ubach A, Grau O, Peguero G, Margalef O, Pla-Rabés S, Stefanescu C, Asensio D, Preece C, Liu L, Verger A, Rico L, Barbeta A, Archotegui-Castells A, Gargallo-Garriga A, Sperlich D, Farré-Armengol G, Fernández-Martínez M, Liu D, Zhang C, Urbina I, Camino M, Vives M, Nadal-Sala D, Sabaté S, Gracia C, Terradas J (2018) Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia. Environ Exp Bot 152:49–59
Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran Desert vegetation. Am J Bot 87:1287–1299
Poyatos R, Aguade D, Galiano L, Mencuccini M, Martinez-Vilalta J (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytol 200:388–401
Rehschuh R, Cecilia A, Zuber M, Farago T, Baumbach T, Hartmann H, Jansen S, Mayrs S, Ruehr N (2020) Drought-induced xylem embolism limits the recovery of leaf gas exchange in Scots pine. Plant Physiol 184:852–864
Senf C, Buras A, Zang CS, Rammig A, Seidl R (2020) Excess forest mortality is consistently linked to drought across Europe. Nat Com 11:6200
Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ 37:153–161
Silva JO, Espírito-Santo MM, Morais HC (2015) Leaf traits and herbivory on deciduous and evergreen trees in a tropical dry forest. Basic Appl Ecol 16:210–219
Sperlich D, Chang CT, Peñuelas J, Gracia C, Sabaté S (2014) Foliar photochemical processes and carbon metabolism under favourable and adverse winter conditions in a Mediterranean mixed forest, Catalonia (Spain). Biogeosciences 11:5657–5674
Trenberth KE, Dai A, van der Schrier G, Jones PD, Barichivich J, Briffa KR, Sheffield J (2014) Global warming and changes in drought. Nat Clim Change 4:17–22
Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683
Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10
West AG, Hultine KR, Burtch KG, Ehleringer JR (2008) Seasonal variations in moisture use in a pinon–juniper woodland. Oecologia 153:787–798
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lusk Ch, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The world-wide leaf economics spectrum. Nature 428:821–882
Zhang S, Zhang Y, Ma K (2017) The association of leaf lifespan and background insect herbivory at the interspecific level. Ecology 98:425–432
Zhang SB, Hu H, Li ZR (2008) Variation of photosynthetic capacity with leaf age in an alpine orchid, Cypripedium flavum. Acta Physiol Plant 30:381–388
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We thank Teresa Malvar-Ferreras for her help in the analysis of the samples.
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Corresponding editor: Yanbo Hu.
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Mediavilla, S., Martínez-Ortega, M., Andrés, S. et al. Premature losses of leaf area in response to drought and insect herbivory through a leaf lifespan gradient. J. For. Res. 33, 39–50 (2022). https://doi.org/10.1007/s11676-021-01351-7
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DOI: https://doi.org/10.1007/s11676-021-01351-7