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Vein and stomatal traits in leaves of three co-occurring Quercus species differing in leaf life span

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Abstract

We analyzed vein and stomatal traits (vein density and vein volume per leaf area, stomatal density, stomatal pore length and pore index) and their relationships with other morphological traits [leaf area, leaf thickness and leaf mass per unit area (LMA)] of three co-occurring Mediterranean tree species with contrasting leaf habits [Quercus faginea Lam., Q. suber L. and Q. ilex L. subsp. ballota (Desf.) Samp.]. The results showed that leaf size, thickness and LMA varied among the species in parallel with the differences in leaf longevity. By contrast, the traits most related to water use showed inconsistent differences among the three species. Stomatal pore index was lowest in the species with intermediate leaf life span. The species with longest leaf longevity had highest vein density but minimum vein volume per area. Vein and stomatal traits also varied independently from other leaf traits within each species. The absence of association between LMA and vein volume suggests that a large LMA is the result of the accumulation of other tissues, and not necessarily veins. We concluded that in contrast with most economic leaf traits that tend to vary in parallel with leaf life span, traits related to water use varied inconsistently with leaf duration in the three species studied. Stomatal and vein traits, in addition, were not related to the maximum stomatal conductance of the different species.

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References

  • Aasamaa K, Sober A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Aust J Plant Physiol 28:765–774

    Google Scholar 

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

    Google Scholar 

  • Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJ (2013) Trait-based tests of coexistence mechanisms. Ecol Lett 16:1294–1306

    PubMed  Google Scholar 

  • Albert CH, Grassein F, Schurr FM, Vieilledent G, Violle C (2011) When and how should intraspecific variability be considered in trait-based plant ecology? Perspect Plant Ecology 13:217–225

    Google Scholar 

  • Beerling DJ, Kelly CK (1996) Evolutionary comparative analyses of the relationship between leaf structure and function. New Phytol 134:35–51

    Google Scholar 

  • Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecol Lett 14:91–100

    PubMed  Google Scholar 

  • Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846

    PubMed  Google Scholar 

  • Brodribb T, Feild T, Jordan G (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brodribb TJ, Feild TS, Sack L (2010) Viewing leaf structure and evolution from a hydraulic perspective. Funct Plant Biol 37:1–11

    Google Scholar 

  • Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytol 199:559–570

    PubMed  Google Scholar 

  • Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–234

    Google Scholar 

  • Cooley AM, Reich A, Rundel P (2004) Leaf support biomechanics of neotropical understory herbs. Am J Bot 91:573–581

    PubMed  Google Scholar 

  • Del Río-García T, Mediavilla S, Silla F, Escudero A (2015) Differences in the environmental control of leaf senescence of four Quercus species coexisting in a Mediterranean environment. Forest Syst 24(2):e027

    Google Scholar 

  • Delaney KJ, Higley LG (2006) An insect countermeasure impacts plant physiology: midrib vein cutting, defoliation and leaf photosynthesis. Plant, Cell Environ 29:1245–1258

    Google Scholar 

  • Dorronsoro F (1992) El medio físico-químico: suelos. In: Gómez-Gutiérrez JM (ed) El Libro de las Dehesas Salmantinas. Junta de Castilla y León, Salamanca, pp 71–124

    Google Scholar 

  • Dunbar-Co S, Sporck MJ, Sack L (2009) Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. Int J Plant Sci 170:61–75

    Google Scholar 

  • Escudero A, Mediavilla S, Olmo M, Villar R, Merino J (2017) Coexistence of deciduous and evergreen oak species in Mediterranean environments: costs associated with the leaf and root traits of both habits. In: Gil-Pelegrín E, Peguero-Pina JJ, Sancho-Knapik D (eds) Oaks physiological ecology. Exploring the functional diversity of genus Quercus L. Springer, Cham, pp 195–237

    Google Scholar 

  • Flexas J, Medrano H (2002) Photosynthetic responses of C3 plants to drought. In: Hemantaranjan A (ed) Advances in plant physiology IV. Scientific Publishers, Jodhpur, pp 1–56

    Google Scholar 

  • Franks PJ, Drake PL, Beerling DJ (2009) Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus. Plant, Cell Environ 32:1737–1748

    Google Scholar 

  • Gil-Pelegrín E, Saz MA, Cuadrat JM, Peguero-Pina JJ, Sancho-Knapik D (2017) Oaks under Mediterranean-type climates: functional response to summer aridity. In: Gil-Pelegrín E, Peguero-Pina JJ, Sancho-Knapik D (eds) Oaks physiological ecology. Exploring the functional diversity of genus Quercus L. Springer, Cham, pp 137–193

    Google Scholar 

  • Hao GY, Hoffmann WA, Scholz FG, Bucci SJ, Meinzer FC, Franco AC, Cao KF, Goldstein G (2008) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155:405–415

    PubMed  Google Scholar 

  • Hao GY, Sack L, Wang AY, Cao KF, Goldstein G (2010) Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Funct Ecol 24:731–740

    Google Scholar 

  • John GP, Scoffoni C, Buckley TN, Villar R, Poorter H, Sack L (2017) The anatomical and compositional basis of leaf mass per area. Ecol Lett 20:412–425

    PubMed  Google Scholar 

  • Jung V, Violle C, Mondy C, Hoffmann L, Muller S (2010) Intraspecific variability and trait-based community assembly. J Ecol 98:1134–1140

    Google Scholar 

  • Jung V, Albert CH, Violle C, Kunstler G, Loucougaray G, Spiegelberger T (2014) Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol 102:45–53

    Google Scholar 

  • Katifori E, Szollosi GJ, Magnasco MO (2010) Damage and fluctuations induce loops in optimal transport networks. Phys Rev Lett 104:048704

    PubMed  Google Scholar 

  • Kawai K, Okada N (2020) Leaf vascular architecture in temperate dicotyledons: correlations and link to functional traits. Planta 251:17. https://doi.org/10.1007/s00425-019-03295-z

    Article  CAS  Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261

    CAS  Google Scholar 

  • Leaf Architecture Working Group (1999) Manual of leaf architecture: morphological description and categorization of dicotyledonous and net-veined monocotyledonous angiosperms. Smithsonian Institution, Washington

    Google Scholar 

  • Li L, McCormack ML, Ma CH, Kong D, Zhang Q, Chen X, Zeng H, Niinemets U, Gua D (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18:899–906

    CAS  PubMed  Google Scholar 

  • Liu C, Li Y, Xu L, Chen Z, He N (2019) Variation in leaf morphological, stomatal, and anatomical traits and their relationships in temperate and subtropical forests. Sci Rep 9:5803

    PubMed  PubMed Central  Google Scholar 

  • Maherali H, Reid CD, Polley HW, Johnson HB, Jachson RB (2002) Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant, Cell Environ 25:557–566

    CAS  Google Scholar 

  • 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 Phytol 159:203–211

    Google Scholar 

  • 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 Physiol 23:987–996

    PubMed  Google Scholar 

  • Mediavilla S, García-Ciudad A, García-Criado B, Escudero A (2008) Testing the correlations between leaf life span and leaf structural reinforcement in 13 species of European Mediterranean woody plants. Funct Ecol 22:787–793

    Google Scholar 

  • Mediavilla S, Babiano J, Martínez-Ortega MM, Escudero A (2018) Ontogenetic changes in anti-herbivore defensive traits in leaves of four Mediterranean co-occurring Quercus species. Ecol Res 33:1093–1102

    CAS  Google Scholar 

  • Méndez-Alonzo R, Ewers FW, Sack L (2013) Ecological variation in leaf biomechanics and its scaling with tissue structure across three Mediterranean climate plant communities. Funct Ecol 27:544–554

    Google Scholar 

  • Messier J, McGill BJ, Enquist BJ, Lechowicz MJ (2017) Trait variation and integration across scales: is the leaf economic spectrum present at local scales? Ecography 40:685–697

    Google Scholar 

  • Mooney HA, Gulmon L (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32:198–206

    CAS  Google Scholar 

  • Nardini A, Peda G, La Rocca N (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytol 196:788–798

    PubMed  Google Scholar 

  • Niinemets Ü (1999) Differences in chemical composition relative to functional differentiation between petioles and laminas of Fraxinus excelsior. Tree Physiol 19:39–45

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Peguero-Pina JJ, Sancho-Knapik D, Morales F, Flexas J, Gil-Pelegrín E (2009) Differential photosynthetic performance and photoprotection mechanisms of three Mediterranean evergreen oaks under severe drought stress. Funct Plant Biol 35:453–462

    Google Scholar 

  • Pérez-Harguindeguy N, Diaz S, Garnier E et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234

    Google Scholar 

  • Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Google Scholar 

  • Richardson SJ, Allen RB, Buxton RP, Easdale TA, Hurst JM, Morse CW, Smissen RD, Peltzer DA (2013) Intraspecific relationships among wood density, leaf structural traits and environment in four co-occurring species of Nothofagus in New Zealand. PLoS ONE 8(3):e58878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rockwell FE, Holbrook NM (2017) Leaf hydraulic architecture and stomatal conductance: a functional perspective. Plant Physiol 174:1996–2007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H (2001) Evolution and function of leaf venation architecture: a review. Ann Bot 87:553–566

    Google Scholar 

  • Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    CAS  PubMed  Google Scholar 

  • Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198:983–1000

    PubMed  Google Scholar 

  • Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell Environ 26:1343–1356

    Google Scholar 

  • Sack L, Dietrich EM, Streeter CM, Sanchez-Gomez D, Holbrook NM (2008) Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proc Natl Acad Sci USA 105:1567–1572

    CAS  PubMed  Google Scholar 

  • Sack L, Scoffoni C, McKown AD, Frole K, Rawls M, Havran JC, Tran T (2012) Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nat Commun 3:1–10

    Google Scholar 

  • Sack L, Scoffoni C, John GP, Poorter H, Mason CM, Mendez-Alonso R, Donovan LA (2013) How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. J Exp Bot 64:4053–4080

    CAS  PubMed  Google Scholar 

  • Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011) Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiol 156:832–843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siefert A, Fridley JD, Ritchie ME (2014) Community functional responses to soil and climate at multiple spatial scales: when does intraspecific variation matter? PLoS ONE 9(10):e111189

    PubMed  PubMed Central  Google Scholar 

  • Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A et al (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol Lett 18:1406–1419

    PubMed  Google Scholar 

  • Tian M, Yu GR, He NP, Hou JH (2016) Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors. Sci Rep 6:19703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uhl D, Mosbrugger V (1999) Leaf venation density as a climate environmental proxy: a critical review and new data. Palaeogeogr Palaeoclimatol Palaeoecol 149:15–26

    Google Scholar 

  • van Ommen Kloeke AEE, Douma JC, Ordoñez JC, Reich PB, van Bodegom PM (2012) Global quantification of contrasting leaf life span strategies for deciduous and evergreen species in response to environmental conditions. Global Ecol Biogeogr 21:224–235

    Google Scholar 

  • Vaz M, Pereira JS, Gazarini LC, David TS, David JS, Rodrigues A, Maroco J, Chaves MM (2010) Drought-induced photosynthetic inhibition and autumn recovery in two Mediterranean oak species (Quercus ilex and Quercus suber). Tree Physiol 30:946–956

    CAS  PubMed  Google Scholar 

  • Wright I, Reich P, Westoby M, Ackerly D, Baruch Z, Bongers F et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    CAS  PubMed  Google Scholar 

  • Yin Q, Wang L, Lei M, Dang H, Quan J, Tian T, Chai Y, Yue M (2018) The relationships between leaf economics and hydraulic traits of woody plants depend on water availability. Sci Total Environ 621:245–252

    CAS  PubMed  Google Scholar 

  • Zhang SB, Guan ZJ, Sun M, Zhang JJ, Cao KF, Hu H (2012) Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum. Orchidaceae. PLoS ONE 7(6):e40080

    CAS  PubMed  Google Scholar 

  • Zhang L, Yang J, Huang Y, Jia Z, Fang Y (2018) Leaf venation variation and phenotypic plasticity in response to environmental heterogeneity in Parrotia subaequalis (H. T. Chang) R. M. Hao et H. T. Wei, an endemic and endangered tree species from China. Forests 9:247

    Google Scholar 

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Acknowledgements

This article has received financial support from the Spanish Ministerio de Ciencia e Innovación—EU-FEDER (Project No. CGL2016-79861-P). We thank to Marta Ortiz and to the Electron Microscopy Facilities-NUCLEUS of the University of Salamanca for his help in the analysis of stomata density.

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Correspondence to S. Mediavilla.

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Communicated by Judy Simon.

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Mediavilla, S., Martín, I. & Escudero, A. Vein and stomatal traits in leaves of three co-occurring Quercus species differing in leaf life span. Eur J Forest Res 139, 829–840 (2020). https://doi.org/10.1007/s10342-020-01290-8

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