Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides

Journal of Ecology

Volumn 101, Issue 4, 2013, Pages 981-989

  Blonder, Benjamin ^a,b,c   Violle, Cyrille ^a,d   Enquist, Brian J ^a,b,e  

^a University of Arizona   (United States)

^b ROCKY MOUNTAIN BIOLOGICAL LABORATORY   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d CNRS   (France)

^e SANTA FE INSTITUTE   (United States)

Author keywords

Aspen; Clone; Ecophysiology; Functional trait; Leaf economics spectrum; Populus tremuloides; Structural equation modelling; Vein density; Venation network

Indexed keywords

ADAPTATION; ASSESSMENT METHOD; CORRELATION; DECIDUOUS TREE; ECONOMIC ANALYSIS; ECOPHYSIOLOGY; INTERSPECIFIC INTERACTION; NUMERICAL MODEL; PHYSIOLOGY; THEORETICAL STUDY; TRADE-OFF; WATER AVAILABILITY;

EID: 84879568886     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12102     Document Type: Article

References (67)

1. Albert, C.H., Thuiller, W., Yoccoz, N.G., Soudant, A., Boucher, F., Saccone, P. & Lavorel, S. (2010) Intraspecific functional variability: extent, structure and sources of variation. Journal of Ecology, 98, 604-613.
2. Amiard, V., Mueh, K.E., Demmig-Adams, B., Ebbert, V., Turgeon, R. & Adams, W.W. (2005) Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proceedings of the National Academy of Sciences of the United States of America, 102, 12968-12973.
3. Atkinson, L.J., Campbell, C.D., Zaragoza-Castells, J., Hurry, V. & Atkin, O.K. (2010) Impact of growth temperature on scaling relationships linking photosynthetic metabolism to leaf functional traits. Functional Ecology, 24, 1181-1191.
4. Barnes, B. (1969) Natural variation and delineation of clones of Populus tremuloides and P. grandidentata in northern Lower Michigan. Silvae Genetica, 18, 130-142.
5. Blonder, B., Violle, C., Bentley, L.P. & Enquist, B.J. (2011) Venation networks and the origin of the leaf economics spectrum. Ecology Letters, 14, 91-100.
6. de Boer, H.J., Eppinga, M.B., Wassen, M.J. & Dekker, S.C. (2012) A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution. Nature Communications, 3, 1221.
7. Bonser, S.P., Ladd, B., Monro, K., Hall, M.D. & Forster, M.A. (2010) The adaptive value of functional and life-history traits across fertility treatments in an annual plant. Annals of Botany, 106, 979-988.
8. Boyce, C.K. & Zwieniecki, M.A. (2012) Leaf fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm evolution. Proceedings of the National Academy of Sciences, 109, 10403-10408.
9. Boyce, C., Brodribb, T., Feild, T.S. & Zwieniecki, M.A. (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B, 276, 1771-1776.
10. Brodribb, T., Feild, T. & Jordan, G. (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology, 144, 1890.
11. Brodribb, T., Feild, T.S. & Sack, L. (2010) Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology, 37, 1-11.
12. Brodribb, T. & Jordan, G.J. (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytologist, 192, 437-448.
13. Carins Murphy, M.R., Jordan, G.J. & Brodribb, T.J. (2012) Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell & Environment, 35, 1407-1418.
14. Castro-Diez, P., Puyravaud, J. & Cornelissen, J. (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia, 124, 476-486.
15. Chapin, F. (1980) The mineral nutrition of wild plants. Annual Review of Ecology and Systematics, 11, 233-260.
16. Cornelissen, J., Lavorel, S., Garnier, E., Diaz, S., Buchmann, N., Gurvich, D., Reich, P., Steege, H., Morgan, H. & Van der Heijden, M. (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany, 51, 335-380.
17. Donovan, L.A., Maherali, H., Caruso, C.M., Huber, H. & de Kroon, H. (2011) The evolution of the worldwide leaf economics spectrum. Trends in Ecology & Evolution, 26, 88-95.
18. Dunbar-Co, S., Sporck, M.J. & Sack, L. (2009) Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation. International Journal of Plant Sciences, 170, 61-75.
19. Edwards, E.J. (2006) Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae). New Phytologist, 172, 479-789.
20. Falster, D.S., Reich, P.B., Ellsworth, D.S., Wright, I.J., Westoby, M., Oleksyn, J. & Lee, T.D. (2011) Lifetime return on investment increases with leaf lifespan among 10 Australian woodland species. New Phytologist, 193, 409-419.
21. Givnish, T.J., Pires, J.C., Graham, S.W., McPherson, M.A., Prince, L.M., Patterson, T.B. et al. (2005) Repeated evolution of net venation and fleshy fruits among monocots in shaded habitats confirms a priori predictions: evidence from an ndhF phylogeny. Proceedings of the Royal Society B, 272, 1481-1490.
22. Granier, C. & Tardieu, F. (1999) Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in the sunflower leaf. Plant, Cell & Environment, 22, 1365-1376.
23. Grime, J. & Hunt, R. (1975) Relative growth-rate: its range and adaptive significance in a local flora. Journal of Ecology, 63, 393-422.
24. Héroult, A., Lin, Y.-S., Bourne, A., Medlyn, B.E. & Ellsworth, D.S. (2012) Optimal stomatal conductance in relation to photosynthesis in climatically contrasting Eucalyptus species under drought. Plant, Cell & Environment, 36, 262-274.
25. Hodgson, J.G., Montserrat-Marté, G., Charles, M., Jones, G., Wilson, P., Shipley, B. et al. (2011) Is leaf dry matter content a better predictor of soil fertility than specific leaf area? Annals of Botany, 108, 1337-1345.
26. Jenny, H. & Leonard, C. (1934) Functional Relationships Between Soil Properties and Rainfall. Soil Science, 38, 363-382.
27. Kattge, J., Díaz, S., Lavorel, S., Prentice, I.C., Leadley, P., Bönisch, G. et al. (2011) TRY - a global database of plant traits. Global Change Biology, 17, 2905-2935.
28. Kikuzawa, K. & Lechowicz, M.J. (2006) Toward synthesis of relationships among leaf longevity, instantaneous photosynthetic rate, lifetime leaf carbon gain, and the gross primary production of forests. The American Naturalist, 168, 373-383.
29. Lichtenthaler, H., Buschmann, C., Döll, M., Fietz, H.J., Bach, T., Kozel, U., Meier, D. & Rahmsdorf, U. (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynthesis Research, 2, 115-141.
30. Lloyd, J., Bloomfield, K., Domingues, T. & Farquhar, G. (2013) Photosynthetically relevant foliar traits correlating better on a mass vs an area basis: of ecophysiological relevance or just a case of mathematical imperatives and statistical quicksand? New Phytologist, in press.
31. Lusk, C.H., Reich, P.B., Montgomery, R.A., Ackerly, D.D. & Cavender-Bares, J. (2008) Why are evergreen leaves so contrary about shade? Trends in Ecology & Evolution, 23, 299-303.
32. Martin, R.E., Asner, G.P. & Sack, L. (2007) Genetic variation in leaf pigment, optical and photosynthetic function among diverse phenotypes of Metrosideros polymorpha grown in a common garden. Oecologia, 151, 387-400.
33. McKown, A.D., Cochard, H. & Sack, L. (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. The American Naturalist, 175, 447-460.
34. McMurtrie, R.E. & Dewar, R.C. (2011) Leaf-trait variation explained by the hypothesis that plants maximize their canopy carbon export over the lifespan of leaves. Tree Physiology, 31, 1007-1023.
35. Milla, R. & Reich, P. (2011) Multi-trait interactions, not phylogeny, fine-tune leaf size reduction with increasing altitude. Annals of Botany, 107, 455-465.
36. Mitton, J. & Grant, M. (1996) Genetic variation and the natural history of quaking aspen. BioScience, 46, 25-31.
37. Mock, K.E., Rowe, C.A., Hooten, M.B., Dewoody, J. & Hipkins, V.D. (2008) Clonal dynamics in western North American aspen (Populus tremuloides). Molecular Ecology, 17, 4827-4844.
38. Nardini, A., Pedà, G. & Rocca, N.L. (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytologist, 196, 788-798.
39. Niinemets, U. (2001) Global-Scale Climatic Controls of Leaf Dry Mass per Area, Density, and Thickness in Trees and Shrubs. Ecology, 82, 453-469.
40. Noblin, X., Mahadevan, L., Coomaraswamy, I.A., Weitz, D.A., Holbrook, N.M. & Zwieniecki, M.A. (2008) Optimal vein density in artificial and real leaves. Proceedings of the National Academy of Sciences, 105, 9140-9144.
41. Ordoñez, J.C., Van Bodegom, P.M., Witte, J.-P.M., Wright, I.J., Reich, P.B. & Aerts, R. (2009) A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Global Ecology and Biogeography, 18, 137-149.
42. Osnas, J.L.D., Lichstein, J.W., Reich, P.B. & Pacala, S.W. (2013) Global Leaf Trait Relationships: Mass, Area, and the Leaf Economics Spectrum. Science, in press.
43. Pantin, F., Simonneau, T., Rolland, G., Dauzat, M. & Muller, B. (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiology, 156, 803-815.
44. Peppe, D.J., Royer, D.L., Cariglino, B., Oliver, S.Y., Newman, S., Leight, E. et al. (2011) Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytologist, 190, 724-739.
45. Poorter, H., Niinemets, Ü., Poorter, L., Wright, I.J. & Villar, R. (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist, 182, 565-588.
46. Prieto, J.A., Louarn, G., Perez PeÑA, J., Ojeda, H., Simonneau, T. & Lebon, E. (2012) A leaf gas exchange model that accounts for intra-canopy variability by considering leaf nitrogen content and local acclimation to radiation in grapevine (Vitis vinifera L.). Plant, Cell & Environment, 35, 1313-1328.
47. Reich, P., Walters, M. & Ellsworth, D. (1997) From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences, 94, 13730-13734.
48. Reich, P., Ellsworth, D., Walters, M., Vose, J., Gresham, C., Volin, J. & Bowman, W. (1999) Generality of leaf trait relationships: a test across six biomes. Ecology, 80, 1955-1969.
49. Roth-Nebelsick, A., Uhl, D., Mosbrugger, V. & Kerp, H. (2001) Evolution and function of leaf venation architecture: a review. Annals of Botany, 87, 553-566.
50. Sack, L. & Frole, K. (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology, 87, 483-491.
51. Sack, L. & Holbrook, N.M. (2006) Leaf hydraulics. Annual Review of Plant Biology, 57, 361-381.
52. Sack, L., Cowan, P., Jaikumar, N. & Holbrook, N. (2003) The 'hydrology' of leaves: co-ordination of structure and function in temperate woody species. Plant Cell and Environment, 26, 1343-1356.
53. Sack, L., Scoffoni, C., McKown, A.D., Frole, K., Rawls, M., Havran, J.C., Tran, H. & Tran, T. (2012) Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications, 3, 837.
54. Santiago, L. & Kim, S. (2009) Correlated evolution of leaf shape and physiology in the woody Sonchus alliance (Asteraceae: Sonchinae) in Macaronesia. International Journal of Plant Sciences, 170, 83-92.
55. Satorra, A. & Bentler, P. (2001) A scaled difference chi-square test statistic for moment structure analysis. Psychometrika, 66, 507-514.
56. 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 Physiology, 156, 832-843.
57. Shipley, B. (2000) Cause and Correlation in bioLogy: A User's Guide to Path Analysis, Structural Equations and Causal Inference. Cambridge University Press, Cambridge, UK.
58. Shipley, B., Lechowicz, M.J., Wright, I. & Reich, P.B. (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology, 87, 535-541.
59. Simonin, K.A., Limm, E.B. & Dawson, T.E. (2012) Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain. New Phytologist, 193, 939-947.
60. Spirtes, P., Glymour, C. & Scheines, R. (2000) Causation, Prediction, and Search. MIT Press, Cambridge, MA.
61. Tumanow, J. (1927) Ungenügende Wasserversorgung und das welken der pflanzen als mittel zur erhöhung ihrer dürreresistenz. Planta; archiv für wissenschaftliche botanik, 3, 391-480.
62. Uhl, D. & Mosbrugger, V. (1999) Leaf venation density as a climate and environmental proxy: a critical review and new data. Paleogeography Paleoclimatology Paleoecology, 149, 15-26.
63. Vasseur, F., Violle, C., Enquist, B., Granier, C. & Vile, D. (2012) A common genetic basis to the origin of the leaf economics spectrum and metabolic scaling allometry. Ecology Letters, 15, 1149-1157.
64. Wright, J.P. & Sutton-Grier, A. (2012) Does the leaf economic spectrum hold within local species pools across varying environmental conditions? Functional Ecology, 26, 1390-1398.
65. Wright, I., Reich, P., Westoby, M., Ackerly, D., Baruch, Z., Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, J. & Diemer, M. (2004) The worldwide leaf economics spectrum. Nature, 428, 821-827.
66. Wright, I., Reich, P., Cornelissen, J., Falster, D., Groom, P., Hikosaka, K. et al. (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography, 14, 411-421.
67. Zomer, R.J., Trabucco, A., Bossio, D.A., van Straaten, O. & Verchot, L.V. (2008) Climate Change Mitigation: A Spatial Analysis of Global Land Suitability for Clean Development Mechanism Afforestation and Reforestation. Agriculture, Ecosystems and Environment, 126, 67-80.