Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Leaf longevity and drought: avoidance of the costs and risks of early leaf abscission as inferred from the leaf carbon isotopic composition

Alfonso Escudero A C , Sonia Mediavilla A and Hermann Heilmeier B
+ Author Affiliations
- Author Affiliations

A Departamento de Ecología, Universidad de Salamanca, E-37071 Salamanca, Spain.

B AG Biologie/Ökologie, Interdisziplinäres Ökologisches Zentrum, TU Bergakademie Freiberg, D-09599 Freiberg, Germany.

C Corresponding author. Email: ecoescu@usal.es

Functional Plant Biology 35(8) 705-713 https://doi.org/10.1071/FP08037
Submitted: 27 February 2008  Accepted: 25 July 2008   Published: 19 September 2008

Abstract

Plant species with longer leaf longevity tend to maintain lower photosynthetic rates. Among other factors, differences in stomatal limitation have been proposed to explain the negative effects of leaf longevity on photosynthesis, although it is not yet clear why stomatal limitations should be stronger in species with longer leaf longevity. We measured carbon isotopic composition (δ13C) in the fresh leaf litter of several Mediterranean woody species to estimate the mean stomatal limitations during the photosynthetically active part of the leaf life. Interspecific differences in δ13C were best explained by a multiple regression including, as independent variables, the maximum leaf longevity and the annual water deficit. For a similar level of water availability, stomatal limitations were higher in species with longer leaf longevity. We hypothesise that stronger stomatal control of transpiration in longer-living leaves arose as a mechanism to reduce the risk of leaf desiccation and to avoid the high costs for the future C assimilation of anticipated leaf mortality in species with a long leaf life expectancy. This stronger sensitivity to drought should be added to the suite of traits accompanying long leaf longevity and contributes decisively to the overall limitations to C assimilation in long-lived leaves.

Additional keywords: leaf internal CO2 concentration, leaf mortality, stomatal conductance, water deficit.


Acknowledgements

This study received financial support from the Spanish Ministry of Education (Project No. BOS2002-02165) and from the Regional Government of Castilla-León (Project No. SA040/03).


References


Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1–67.
Crossref | GoogleScholarGoogle Scholar | open url image1

Arens NC, Jahren AH, Amundson R (2000) Can C3 plants faithfully record the carbon isotopic composition of atmospheric carbon dioxide? Paleobiology 26, 137–164.
Crossref | GoogleScholarGoogle Scholar | open url image1

Begon M , Mortimer A (1986) ‘Population ecology.’ (Blackwell Scientific Publications: Oxford)

Brooks JR, Flanagan LB, Buchmann N, Ehleringer JR (1997) Carbon isotope composition of boreal plants: functional grouping of life forms. Oecologia 110, 301–311.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon isotope discrimination of salt-tolerant (Gossypium hirsutum L.) and salt-sensitive (Phaseolus vulgaris L.) C3 non-halophytes. Plant Physiology 95, 628–635.
PubMed |
open url image1

Buchmann N, Kao W, Ehleringer J (1997) Influence of stand structure on carbon-13 of vegetation, soils, and canopy air within deciduous and evergreen forests in Utah (USA). Oecologia 110, 109–119.
Crossref | GoogleScholarGoogle Scholar | open url image1

Buckley TN (2005) The control of stomata by water balance. New Phytologist 168, 275–292.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cernusak L, Arthur DJ, Pate JS, Farquhar GD (2003) Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiology 131, 1544–1554.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annual Review of Ecology and Systematics 13, 229–259.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought: from genes to the whole plant. Functional Plant Biology 30, 239–264.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cochard H, Coll L, Le Roux X, Améglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiology 128, 282–290.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cowan IR (1982) Regulation of water use in relation to carbon gain in higher plants. In ‘Encyclopedia of plant physiology, vol. 12B. Physiological plant ecology II. Water relations and carbon assimilation’. (Eds OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 589–613. (Springer-Verlag: Berlin)

Damesin C, Rambal S, Joffre R (1998) Seasonal and annual changes in leaf δ13C in two co-occurring Mediterranean oaks: relations to leaf growth and drought progression. Functional Ecology 12, 778–785.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dorronsoro DF (1992) Suelos. In ‘El libro de las dehesas salmantinas’. (Ed. JM Gómez) pp. 71–124. (Junta de Castilla y León: Salamanca)

Ehleringer JR, Cooper TA (1988) Correlations between carbon isotope ratio and microhabitat in desert plants. Oecologia 76, 562–566. open url image1

Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Australian Journal of Plant Physiology 13, 281–292. open url image1

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. open url image1

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137. open url image1

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farquhar GD, Buckley TN, Miller JM (2002) Optimal stomatal control in relation to leaf area and nitrogen content. Silva Fennica 36, 625–637. open url image1

Field C , Mooney HA (1986) The photosynthesis–nitrogen relationship in wild plants. In ‘On the economy of plant form and function’. (Ed. TJ Givnish) pp. 25–55. (University Press: Cambridge)

Fitter AH , Hay RKM (2002) ‘Environmental physiology of plants.’ (Academic Press: London)

Hall AE, Richards RA, Condon AG, Wright GC, Farquhar GD (1994) Carbon isotope discrimination and plant breeding. Plant Breeding Reviews 4, 81–113. open url image1

Hikosaka K (2004) Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes and ecological importance. Journal of Plant Research 117, 481–494.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen-use efficiency in leaves of woody herbaceous species. Functional Ecology 12, 896–905.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jensen ME, Haise HR (1963) Estimating evapotranspiration from solar radiation. Journal of the Irrigation and Drainage Division 89, 15–41. open url image1

Jones HG, Sutherland RA (1991) Stomatal control of xylem embolism. Plant, Cell & Environment 14, 607–612.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kloeppel BD, Gower ST, Treichel IW, Kharuk S (1998) Foliar carbon isotope discrimination in Larix species and sympatric evergreen conifers: a global comparison. Oecologia 114, 153–159.
Crossref | GoogleScholarGoogle Scholar | open url image1

Körner Ch, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74, 623–632.
Crossref | GoogleScholarGoogle Scholar | open url image1

Landsberg JJ (1986) ‘Physiological ecology of forest production.’ (Academic Press: London)

Marshall JD, Zhang J (1994) Carbon isotope discrimination and water-use efficiency in native plants of the north-central Rockies. Ecology 75, 1887–1895.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mediavilla S, Escudero A (2003a) Photosynthetic capacity integrated over the lifetime of a leaf is predicted to be independent of leaf longevity in some tree species. New Phytologist 159, 203–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mediavilla S, Escudero A (2003b) Stomatal responses to drought at a Mediterranean site: a comparative study of co-occurring woody species differing in leaf longevity. Tree Physiology 23, 987–996.
PubMed |
open url image1

Ninyerola M , Pons X , Roure JM (2005) ‘Atlas Climático Digital de la Península Ibérica. Metodología y aplicaciones en bioclimatología y geobotánica.’ (Universidad Autónoma de Barcelona: Bellaterra)

Poorter H, Evans JR (1998) Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 116, 26–37.
Crossref | GoogleScholarGoogle Scholar | open url image1

Poorter H, Farquhar GD (1994) Transpiration, intercellular carbon dioxide concentration and carbon-isotope discrimination of 24 wild species differing in relative growth rate. Plant, Cell & Environment 15, 221–229. open url image1

Read J, Sanson GD (2003) Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types. New Phytologist 160, 81–89.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB (1993) Reconciling apparent discrepancies among studies relating life span, structure and function of leaves in contrasting plant life forms and climates: ‘the blind men and the elephant retold’. Functional Ecology 7, 721–725.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant and stand processes in diverse ecosystems. Ecological Monographs 62, 365–392.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Kloeppel BD, Ellsworth DS, Walters MB (1995) Different photosynthesis–nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104, 24–30.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences of the United States of America 94, 13730–13734.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smedley MP, Dawson TE, Comstock JP, Donovan LA, Sherrill DE, Cook CS, Ehleringer JR (1991) Seasonal carbon isotope discrimination in a grassland community. Oecologia 85, 314–320.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sperry JS (2004) Coordinating stomatal and xylem functioning – an evolutionary perspective. New Phytologist 162, 568–570.
Crossref | GoogleScholarGoogle Scholar | open url image1

Stewart GR, Turnbull MH, Schmidt S, Erskine PD (1995) 13C natural abundance in plant communities along a rainfall gradient: a biological integrator of water availability. Australian Journal of Plant Physiology 22, 51–55. open url image1

Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell & Environment 27, 1047–1054.
Crossref | GoogleScholarGoogle Scholar | open url image1

Terwilliger VJ, Kitajima K, Le Roux-Swarthout DJ, Mulkley S, Wright SJ (2001) Intrinsic water-use efficiency and heterotrophic investment in tropical leaf growth of two Neotropical pioneer tree species as estimated from δ13C values. New Phytologist 152, 267–281.
Crossref | GoogleScholarGoogle Scholar | open url image1

Turner IM (1994) Sclerophylly: primarily protective? Functional Ecology 8, 669–675.
Crossref | GoogleScholarGoogle Scholar | open url image1

Valentini R, Mugnozza GES, Ehleringer JR (1992) Hydrogen and carbon isotope ratios of selected species of Mediterranean macchia ecosystem. Functional Ecology 6, 627–631.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vesk PA, Westoby M (2003) Drought damage and recovery – a conceptual model. New Phytologist 160, 1–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vitousek PM, Field CB, Matson PA (1990) Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84, 362–370. open url image1

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Functional Ecology 6, 469–475.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warren CR, Adams MA (2000) Trade-offs between the persistence of foliage productivity in two Pinus species. Oecologia 124, 487–494.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warren CR, Adams MA (2006) Internal conductance does not scale with photosynthetic capacity: implications for carbon isotopic discrimination and the economics of water and nitrogen use in photosynthesis. Plant, Cell & Environment 29, 192–201.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Warren CR, McGrath JF, Adams MA (2001) Water availability and carbon isotope discrimination in conifers. Oecologia 127, 476–486.
Crossref | GoogleScholarGoogle Scholar | open url image1

Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33, 125–159.
Crossref | GoogleScholarGoogle Scholar | open url image1

Williams DG, Ehleringer JR (2000) Intra- and interspecific variation for summer precipitation use in Pinyon – Juniper woodlands. Ecological Monographs 70, 517–537. open url image1

Wright IJ, Cannon K (2001) Relationships between leaf lifespan structural defences in a low nutrient sclerophyll flora. Functional Ecology 15, 351–359.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. Journal of Ecology 90, 534–543.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z , et al. (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yoshie F (1986) Intercellular CO2 concentration and water-use efficiency of temperate plants with different life-forms and from different microhabitats. Oecologia 68, 370–374.
Crossref | GoogleScholarGoogle Scholar | open url image1