Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Carbon isotope discrimination as a tracer of functional traits in a mediterranean macchia plant community

Christiane Werner A C and Cristina Máguas B
+ Author Affiliations
- Author Affiliations

A Experimental and Systems Ecology, University of Bielefeld, Universitätsstrasse 25, D-33615 Bielefeld, Germany.

B Centro de Biologia Ambiental, Faculdade de Ciências, Universidade Lisboa, Campo Grande, P-1749-016 Lisbon, Portugal.

C Corresponding author. Email: c.werner@uni-bielefeld.de

Functional Plant Biology 37(5) 467-477 https://doi.org/10.1071/FP09081
Submitted: 10 April 2009  Accepted: 29 December 2009   Published: 30 April 2010

Abstract

Characterising functional plant groups with simple robust parameters of structural and functional traits is an important tool in ecological research. The reliability of carbon isotope discrimination (Δ13C) as an indicator of functional types was assessed in a highly diverse mediterranean macchia comprising drought semi-deciduous malacophylls, evergreen sclerophylls and a gymnosperm. Pronounced differences in Δ13C of 4‰ occurred: semi-deciduous species (Cistus sp. L.) showed the highest and the gymnosperm (Juniperus sp. L.) the lowest Δ13C (20.3 ± 0.5‰ and 16.2 ± 0.18‰, respectively). Across all studied species, Δ13C was correlated with (i) phenology (length of growing period) and (ii) leaf structure (leaf mass and N per area). The correlation of Δ13C with leaf water potentials, an indicator of drought stress, was species-specific and only 6 out of 11 species exhibited a significant relationship. Thus, leaf phenology governs seasonal responsiveness of Δ13C to drought, which constrains its applicability as an indicator of water use efficiency, particularly in evergreen species with short growing periods. Principal components analysis indicated the robustness of Δ13C for the classification of functional groups yielding similar results based on multiple leaf traits or solely on Δ13C. Hence Δ13C provides an ecological tracer of different functional types, integrating structural, functional and phenological attributes.

Additional keywords: drought adaptation, functional groups, phenology, specific leaf mass, stable carbon isotope, water potential, water use efficiency (WUE).


Acknowledgements

Financial support was provided through the European Community’s Human Potential Program under contract HPRN-CT-1999–00059 (NETCARB) to C. Werner. Valuable comments from H. Griffiths, O. Correia and three anonymous referees, and the help of R. Maia and B. Teichner on isotope analysis are gratefully acknowledged.


References


Ackerly D (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecological Monographs 74, 25–44.
CrossRef |

Alessio GA, De Lillis M, Brugnoli E, Lauteri M (2004) Water sources and water-use efficiency in Mediterranean coastal dune vegetation. Plant Biology 6, 350–357.
CrossRef | PubMed |

Bai E, Boutton TW, Liu F, Wu XB, Archer SR (2008) Variation in woody plant δ13C along a topoedaphic gradient in a subtropical savanna parkland. Oecologia 156, 479–489.
CrossRef | PubMed |

Bonal D, Sabatier D, Montpied P, Tremeaux D, Guehl JM (2000) Interspecific variability of δ13C among trees in rainforests of French Guiana: functional groups and canopy integration. Oecologia 124, 454–468.
CrossRef |

Booth MS, Caldwell MM, Stark JM (2003) Overlapping resource use in three Great Basin species: implications for community and vegetation dynamics. Journal of Ecology 91, 36–48.
CrossRef |

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 |

Brugnoli E , Farquhar GD (2000) Photosynthetic fractionation of carbon isotopes. In ‘Photosynthesis: physiology and metabolism’. (Eds RC Leegood, TD Sharkey, SV Caemmerer) pp. 399–434. (Kluwer Akademic Publisher: The Netherlands)

Cerling TE, Ehleringer JR, Harris JM (1998) Carbon dioxide starvation, the development of C4 ecosystems, and mammalian evolution. Philosophical Transactions of the Royal Society of London. B 353, 159–171.
CrossRef |

Cernusak LA, Aranda J, Marshall JD, Winter K (2007) Large variation in whole-plant water use efficiency among tropical tree species. New Phytologist 173, 294–305.
CrossRef | PubMed |

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 |

Correia OA, Catarino FM (1994) Seasonal changes in soil-to-leaf resistance in Cistus sp. and Pistacia lentiscus. Acta Oecologica 15, 289–300.

Correia O , Catarino F , Tenhunen JD , Lange OL (1987) Regulation of water use by four species of Cistus in the scrub vegetation of the Serra da Arrábida, Portugal. In ‘Plant response to stress’. (Eds JD Tenhunen, FM Catarino, OL Lange, WC Oechel) pp. 247–258. (NATO ASI Series, Springer-Verlag: Berlin, Heidelberg)

Correia O, Martins AC, Catarino F (1992) Comparative phenology and seasonal nitrogen variation in mediterranean species of Portugal. Ecologia Mediterranean XVIII, 7–18.

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

de Lillis M, Fontanella A (1992) Comparative phenology and growth in different species of the Mediterranean maquis of central Italy. Vegetatio 99–100, 83–96.
CrossRef |

Díaz Barradas MC, Zunzunegui M, Tirado R, Ain-Lhout F, García Novo F (1999) Plant functional types and ecosystem function in Mediterranean shrubland. Journal of Vegetation Science 10, 709–716.
CrossRef |

Domingues TF, Martinelli LA, Ehleringer J (2007) Ecophysiological traits of plant functional groups in forest and pasture ecosystems from eastern Amazonia, Brazil. Plant Ecology 193, 101–112.
CrossRef |

Donovan L, Dudley SA, Rosenthal DM, Ludwig F (2007) Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers. Oecologia 152, 13–25.
CrossRef | PubMed |

Ehleringer JR (1993) Variation in leaf carbon isotope discrimination in Encelia farinosa: implications for growth, competition, and drought survival. Oecologia 95, 340–346.
CrossRef |

Escudero A, Mediavilla S, Heilmeier H (2008) Leaf longevity and drought: avoidance of the costs and risks of early leaf abscission as inferred from the leaf carbon isotopic composition. Functional Plant Biology 35, 705–713.
CrossRef |

Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Ecology & Evolution 6, 121–126.

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.
CrossRef |

Farquhar GD , Hubick KT , Condon AG , Richards RA (1989 a) Carbon isotope fractionation and plant water-use-efficiency. In ‘Stable isotopes in ecological research’. (Eds PW Rundel, JR Ehleringer, KH Nagy) pp. 21–40. (Springer-Verlag: Berlin)

Farquhar GD, Ehleringer JR, Hubick KT (1989b) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
CrossRef |

Flexas J, Dias-Espejo A, Galmes J, Kaldenhoff R, Medrano H, Ribas-Carbó M (2007) Rapid variations in mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell & Environment 30, 1284–1298.
CrossRef | PubMed |

Foster TE, Brooks JR (2005) Functional groups based on leaf physiology: are they spatially and temporally robust? Oecologia 144, 337–352.
CrossRef | PubMed |

Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 175, 81–93.
CrossRef | PubMed |

García Novo F , Díaz Barradas MC , Zunzunegui M , García Mora R , Gallego Fernández JB (2004) Plant functional types in coastal dune habitats. In ‘Coastal dunes, ecology and conservation in ecological studies 171’. (Eds ML Martínez, NP Psuty) pp. 155–169. (Springer-Verlag: Berlin, Heidelberg)

Ghashghaie J, Badeck F, Lanigan G, Nogúes S, Tcherkez G, Deléens E, Cornic G, Griffiths H (2003) Carbon isotope fractionation during dark respiration and photorespiration in C3 plants. Phytochemistry Reviews 2, 145–161.
CrossRef |

Gratani L, Varone L (2006) Long-time variations in leaf mass and area of Mediterranean evergreen broad-leaf and narrow-leaf maquis species. Photosynthetica 44, 161–168.
CrossRef |

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

Hanba YT, Miyazawa S-H, Terashima I (1999) The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forest. Functional Ecology 13, 632–639.
CrossRef |

Hanba YT, Kogami H, Terashima I (2003) The effect of internal CO2 conductance on leaf carbon isotope ratio. Isotopes in Environmental and Health Studies 39, 5–13.
CrossRef | PubMed |

Harley PC , Tenhunen JD , Lange OL , Beyschlag W (1987) Seasonal and diurnal patterns in leaf gas exchange of Phillyrea angustifolia growing in Portugal. In ‘Plant response to stress. Functional analysis in Mediterranean ecosystems’. (Eds JD Tenhunen, F Catarino, OL Lange, WC Oechel) pp. 329–337. (Springer-Verlag: Berlin)

Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytologist 161, 371–385.
CrossRef |

Lauteri M, Pliura A, Monteverdi MC, Brugnoli E, Villani F, Eriksson G (2004) Genetic variation in carbon isotope discrimination in six European populations of Castanea sativa Mill. originating from contrasting localities. Journal of Evolutionary Biology 17, 1286–1296.
CrossRef | PubMed |

Lavorel S, McIntyre J, Landsberg JJ, Forbes TDA (1997) Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends in Ecology & Evolution 12, 474–478.
CrossRef |

Máguas C , Griffiths H (2003) Applications of stable isotopes in plant ecology. In ‘Progress in botany’. (Eds K Esser, U Lüttge, W Beyschlag, J Murata) pp. 472–505. (Springer-Verlag: Berlin, Heidelberg)

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 |

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

Masle J, Gilmore SR, Farquhar GD (2005) The ERECTA gene regulates plant transpiration efficiency in Arabidopsis. Nature 436, 866–870.
CrossRef | PubMed |

Miller JM, Williams RJ, Farquhar GD (2001) Carbon isotope discrimination by a sequence of Eucalyptus species along a subcontinental rainfall gradient in Australia. Functional Ecology 15, 222–232.
CrossRef |

Monclus R, Dreyer E, Delmotte FM, Villar M, Delay D, Boudouresque E, Petit JM, Marron N, Brechet C, Brignolas F (2005) Productivity, leaf traits and carbon isotope discrimination in 29 Populus deltoides × P. nigra clones. New Phytologist 167, 53–62.
CrossRef | PubMed |

Peñuelas J, Filella I, Terradas J (1999) Variability of plant nitrogen and water use in a 100-m transect of a subdesertic depression of the Ebro valley (Spain) characterized by leaf δ13C and δ15N. Acta Oecologica 20, 119–123.
CrossRef |

Peperkorn R, Werner C, Beyschlag W (2005) Phenotypic plasticity of an invasive Acacia versus two native Mediterranean species. Functional Plant Biology 32, 933–944.
CrossRef |

Ponton S, Flanagan LB, Alstad KP, Johnson BG, Morgenstern K, Kljun N, Black TA, Barr AG (2006) Comparison of ecosystem water-use efficiency among Douglas-fir forest, aspen forest and grassland using eddy covariance and carbon isotope techniques. Global Change Biology 12, 294–310.
CrossRef |

Priault P, Wegener F, Werner C (2009) Pronounced differences in diurnal variation of carbon isotope composition of leaf respired CO2 among functional groups. New Phytologist 181, 400–412.
CrossRef | PubMed |

Rascher KG, Maguas C, Correia O, Werner C (2009) Tracing seasonal changes in water use of an invasive Acacia and a native pine in Southern Portugal by measurement of sap flow. Acta Horticulturae 846, 209–216.

Sala OE , Lauenroth WK , Golluscio RA (1997) Plant functional types in temperate semi-arid regions. In ‘Plant functional types’. (Eds TM Smith, HH Shugart, FI Woodward) pp. 217–233. (Cambridge University Press: Cambridge)

Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125, 350–357.
CrossRef |

Seibt U, Rajabi A, Griffiths H, Berry J (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155, 441–454.
CrossRef | PubMed |

Sperry JS, Tyree MT (1990) Water-stress-induced xylem embolism in three species of conifers. Plant, Cell & Environment 13, 427–436.
CrossRef |

Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant, Cell & Environment 25, 251–263.
CrossRef | PubMed |

Tenhunen JD , Beyschlag W , Lange OL , Harley PC (1987) Changes during summer drought in leaf CO2 uptake rates of macchia shrubs growing in Portugal: Limitations due to photosynthetic capacity, carboxylation efficiency, and stomatal conductance. In ‘Plant responses to stress’. (Eds JD Tenhunen, FM Catarino, OL Lange, WC Oechel) pp. 305–327. (Springer-Verlag: Berlin)

Terwilliger VJ, Kitjajima K, LeRoux-Swarthout DJ, Mulkey 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 |

Valentini R, Scarascia Mugnozza GE, Ehleringer JR (1992) Hydrogen and carbon isotop ratios of selected species of a Mediterranean macchia ecosystem. Functional Ecology 6, 627–631.
CrossRef |

Valladares F, Martínez-Ferri E, Balaguer L, Perez-Corona E, Manrique E (2000) Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytologist 148, 79–91.
CrossRef |

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

Wegener F, Beyschlag W, Werner C (2010) The magnitude of diurnal variation in carbon isotopic composition of leaf dark respired CO2 correlates with the difference between δ13C of leaf and root material. Functional Plant Biology in press. ,

Werner C (2010) Do isotopic respiratory signals trace changes in metabolic fluxes? New Phytologist 186, 569–571.
CrossRef |

Werner C, Correia O (1996) Photoinhibition in cork-oak leaves under stress: influence of the bark-stripping on the chlorophyll fluorescence emission in Quercus suber L. Trees – Structure and Function 10, 288–292.

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 Oecologica 20, 15–23.
CrossRef |

Werner C, Correia OA, Ryel RJ, Beyschlag W (2001a) Structural and functional variability within the canopy and its relevance for carbon gain and stress avoidance. Acta Oecologica 22, 129–138.
CrossRef |

Werner C, Ryel RJ, Correia O, Beyschlag W (2001b) Effects of photoinhibition on whole-plant carbon gain assessed with a photosynthesis model. Plant, Cell & Environment 24, 27–40.
CrossRef |

Werner C , Maia R , Máguas C (2001 c) Are carbon and oxygen isotope compositions of bulk leaf material reliable predictors of water use efficiency in slow-growing drought-adapted species? In ‘PS2001 Proceedings: 12th International Congress on Photosynthesis’. (CSIRO Publishing: Melbourne, Australia)

Werner C, Correia O, Beyschlag W (2002) Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. Functional Plant Biology 29, 999–1011.
CrossRef |

Werner C, Wegener F, Unger S, Nogués S, Priault P (2009) Short-term dynamics of isotopic composition of leaf respired CO2 upon darkening: measurements and implications. Rapid Communications in Mass Spectrometry 23, 2428–2438.
CrossRef | PubMed |

Werner C, Zumkier U, Beyschlag W, Máguas C (2010) High competitiveness of a resource demanding invasive Acacia under low resource supply. Plant Ecology 206, 83–96.
CrossRef |

Woodward FI , Kelly CK (1997) Plant functional types: towards a definition by environmental constraints. In ‘Plant functional types’. (Eds TM Smith, HH Shugart, FI Woodward) pp. 47–65. (Cambridge University Press: Cambridge)

Zunzunegui M, Díaz Barradas MC, Ain-Lhout F, Clavijo A, García Novo F (2005) To live or to survive in Doñana dunes: Adaptive responses of woody species under a Mediterranean climate. Plant and Soil 273, 77–89.
CrossRef |








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