Skip to main content
Log in

Premature losses of leaf area in response to drought and insect herbivory through a leaf lifespan gradient

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abràmoff M, Magalhães P, Ram S (2004) Image processing with imageJ. Biophoton Int 11:36–42

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558:531–539

    Article  CAS  PubMed  Google Scholar 

  • Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Emberger L (1932) Sur une formule climatique et ses applications en botanique. La Métereologie 92–93:1–10

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kozlowski TT, Kramer PJ, Pallardy SG (1991) The physiological ecology of woody plants. Academic Press, San Diego, p 657

    Google Scholar 

  • Larcher W (1995) Ecophysiology and stress physiology of functional groups. In: Larcher W (ed) Physiological plant ecology. Springer Verlag, Berlin, pp 340–353

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Martínez-Vilalta J, Sala A, Piñol J (2004) The hydraulic architecture of Pinaceae: a review. Plant Ecol 171:3–13

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran Desert vegetation. Am J Bot 87:1287–1299

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • West AG, Hultine KR, Burtch KG, Ehleringer JR (2008) Seasonal variations in moisture use in a pinon–juniper woodland. Oecologia 153:787–798

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Zhang Y, Ma K (2017) The association of leaf lifespan and background insect herbivory at the interspecific level. Ecology 98:425–432

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Teresa Malvar-Ferreras for her help in the analysis of the samples.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alfonso Escudero.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Project funding: This research received financial support from the Regional Government of Castilla-León (Project No. SA126G18).

The online version is available at http://www.springerlink.com.

Corresponding editor: Yanbo Hu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-021-01351-7

Keywords

Navigation