Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests

Ecology Letters

Volumn 18, Issue 9, 2015, Pages 899-906

  Li, Le ^a,b   McCormack, M Luke ^a   Ma, Chengen ^a,b   Kong, Deliang ^c   Zhang, Qian ^d   Chen, Xiaoyong ^d   Zeng, Hui ^c   Niinemets, Ülo ^e,f   Guo, Dali ^a  

^a INSTITUTE OF GEOGRAPHIC SCIENCES AND NATURAL RESOURCES RESEARCH   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c PEKING UNIVERSITY   (China)

^d EAST CHINA NORMAL UNIVERSITY   (China)

^e ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^f ESTONIAN ACADEMY OF SCIENCES   (Estonia)

Author keywords

Functional divergence; Leaf carbon isotope composition ( 13C); Leaf dry mass per area; Leaf economics spectrum; Leaf hydraulics; Leaf nitrogen concentration; Stomatal density; Vein density; Woody angiosperms

Indexed keywords

ADAPTATION; ANGIOSPERM; CARBON ISOTOPE; COEXISTENCE; CONCENTRATION (COMPOSITION); DIVERGENCE; FACILITATION; ISOTOPIC COMPOSITION; LEAF AREA; LIGHT INTENSITY; NICHE; NITROGEN; PHOTOSYNTHESIS; SPECIES RICHNESS; SUBTROPICAL REGION; TROPICAL FOREST;

MAGNOLIOPHYTA;

NITROGEN; WATER;

ANATOMY AND HISTOLOGY; ANGIOSPERM; CHEMISTRY; CHINA; EVAPOTRANSPIRATION; FOREST; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; PLANT LEAF; PLANT STOMA; TROPIC CLIMATE;

ANGIOSPERMS; CHINA; FORESTS; NITROGEN; PHOTOSYNTHESIS; PHYLOGENY; PLANT LEAVES; PLANT STOMATA; PLANT TRANSPIRATION; TROPICAL CLIMATE; WATER;

EID: 84938979330     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/ele.12466     Document Type: Article

References (50)

1. Abouheif, E. (1999). A method for testing the assumption of phylogenetic independence in comparative data. Evol. Ecol. Res., 1, 895-909.
2. Ackerly, D. (2004). Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecol. Monogr., 74, 25-44.
3. Adler, P.B., Fajardo, A., Kleinhesselink, A.R. & Kraft, N.J. (2013). Trait-based tests of coexistence mechanisms. Ecol. Lett., 16, 1294-1306.
4. Baraloto, C., Timothy Paine, C.E., Poorter, L., Beauchene, J., Bonal, D., Domenach, A.M. et al. (2010). Decoupled leaf and stem economics in rain forest trees. Ecol. Lett., 13, 1338-1347.
5. Beerling, D.J. (2005). Leaf evolution: gases, genes and geochemistry. Ann. Bot., 96, 345-352.
6. Blomberg, S.P., Garland, T. & Ives, A.R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717-745.
7. Blonder, B., Violle, C., Bentley, L.P. & Enquist, B.J. (2011). Venation networks and the origin of the leaf economics spectrum. Ecol. Lett., 14, 91-100.
8. Brodribb, T.J. & Feild, T.S. (2010). Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol. Lett., 13, 175-183.
9. Brodribb, T.J., Feild, T.S. & Jordan, G.J. (2007). Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol., 144, 1890-1898.
10. Brodribb, T.J., Jordan, G.J. & Carpenter, R.J. (2013). Unified changes in cell size permit coordinated leaf evolution. New Phytol., 199, 559-570.
11. Carins Murphy, M.R., Jordan, G.J. & Brodribb, T.J. (2012). Differential leaf expansion can enable hydraulic acclimation to sun and shade. Plant, Cell Environ., 35, 1407-1418.
12. Carins Murphy, M.R., Jordan, G.J. & Brodribb, T.J. (2014). Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant, Cell Environ., 37, 124-131.
13. Casson, S.A. & Hetherington, A.M. (2010). Environmental regulation of stomatal development. Curr. Opin. Plant Biol., 13, 90-95.
14. Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol., 29, 1969-1973.
15. Farquhar, G.D., Hubick, K.T., Condon, A.G. & Richards, R.A. (1989). Carbon isotope fractionation and plant water-use efficiency. In: Stable Isotopes in Ecological Research (eds Rundel, P.W., Ehleringer, J.R., Nagy, K.A.). Springer-Verlag, Berlin Heidelberg, New York, pp. 21-40.
16. Feild, T.S. & Brodribb, T.J. (2013). Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytol., 199, 720-726.
17. Field, C.H. & Mooney, H.A. (1986). Photosynthesis-nitrogen relationship in wild plants. In: On the Economy of Plant Form and Function: Proceedings of the Sixth Maria Moors Cabot Symposium, Evolutionary Constraints on Primary Productivity, Adaptive Patterns of Energy Capture in Plants, Harvard Forest, August 1983 (ed Givnish, T.J.). Cambridge University Press, Cambridge, UK, pp. 25-50.
18. 2 effects on stomatal size and density over geologic time. Proc. Natl Acad. Sci., 106, 10343-10347.
19. Franks, P.J., Drake, P.L. & Beerling, D.J. (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.
20. Givnish, T.J. (1987). Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytol., 106, 131-160.
21. Han, Q. (2011). Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. Tree Physiol., 31, 976-984.
22. Huang, J., Chen, B., Liu, C., Lai, J., Zhang, J. & Ma, K. (2012). Identifying hotspots of endemic woody seed plant diversity in China. Divers. Distrib., 18, 673-688.
23. Kraft, N.J., Valencia, R. & Ackerly, D.D. (2008). Functional traits and niche-based tree community assembly in an Amazonian forest. Science, 322, 580-582.
24. Laughlin, D.C. (2014). The intrinsic dimensionality of plant traits and its relevance to community assembly. J. Ecol., 102, 186-193.
25. Lloyd, J., Bloomfield, K., Domingues, T.F. & Farquhar, G.D. (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 Phytol., 199, 311-321.
26. Marks, C.O. & Lechowicz, M.J. (2006). Alternative designs and the evolution of functional diversity. Am. Nat., 167, 55-66.
27. Niinemets, Ü. & Sack, L. (2006). Structural determinants of leaf light-harvesting capacity and photosynthetic potentials. In: Progress in Botany (eds Esser, K., Lüttge, U., Beyschlag, W., Murata, J.). Springer-Verlag, Berlin Heidelberg, New York, pp. 385-419.
28. Niinemets, Ü., Keenan, T.F. & Hallik, L. (2015). Tansley review. A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol., 205, 973-993.
29. Nosil, P., Harmon, L.J. & Seehausen, O. (2009). Ecological explanations for (incomplete) speciation. Trends Ecol. Evol., 24, 145-156.
30. Osnas, J.L., Lichstein, J.W., Reich, P.B. & Pacala, S.W. (2013). Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science, 340, 741-744.
31. Parkhurst, D. & Givnish, T.J. (1986). Internal leaf structure: a three-dimensional perspective. In: On the Economy of Plant Form and Function: Proceedings of the Sixth Maria Moors Cabot Symposium, Evolutionary Constraints on Primary Productivity, Adaptive Patterns of Energy Capture in Plants, Harvard Forest, August 1983 (ed Givnish, T.J.). Cambridge University Press, Cambridge, UK, pp. 215-249.
32. Pillar, V.D., Blanco, C.C., Müller, S.C., Sosinski, E.E., Joner, F. & Duarte, L.D.S. (2013). Functional redundancy and stability in plant communities. J. Veg. Sci., 24, 963-974.
33. Poorter, H., Niinemets, Ü., Poorter, L., Wright, I.J. & Villar, R. (2009). Causes and consequences of variation in leaf dry mass per area (LMA): a meta-analysis. New Phytol., 182, 565-588.
34. Posada, D. (2008). jModelTest: phylogenetic model averaging. Mol. Biol. Evol., 25, 1253-1256.
35. R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URLhttp://www.R-project.org/.RCore Team (2013).
36. Reich, P.B. (2014). The world-wide 'fast-slow' plant economics spectrum: a traits manifesto. J. Ecol., 102, 275-301.
37. Richardson, S.J., Peltzer, D.A., Allen, R.B. & McGlone, M.S. (2005). Resorption proficiency along a chronosequence: responses among communities and within species. Ecology, 86, 20-25.
38. Sack, L. & Frole, K. (2006). Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology, 87, 483-491.
39. 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.
40. 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 Environ., 26, 1343-1356.
41. Sack, L., Scoffoni, C., John, G.P., Poorter, H., Mason, C.M., Mendez-Alonzo, R. et al. (2013). How do leaf veins influence the worldwide leaf economics spectrum? Review and synthesis. J. Exp. Bot., 64, 4053-4080.
42. Sack, L., Scoffoni, C., John, G.P., Poorter, H., Mason, C.M., Mendez-Alonzo, R. et al. (2014). Leaf mass per area is independent of vein length per area: avoiding pitfalls when modelling phenotypic integration (reply to). J. Exp. Bot., 65, 5115-5123.
43. Soudzilovskaia, N.A., Elumeeva, T.G., Onipchenko, V.G., Shidakov, I.I., Salpagarova, F.S., Khubiev, A.B. et al. (2013). Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proc. Natl Acad. Sci., 110, 18180-18184.
44. Sterck, F., Markesteijn, L., Schieving, F. & Poorter, L. (2011). Functional traits determine trade-offs and niches in a tropical forest community. Proc. Natl Acad. Sci., 108, 20627-20632.
45. Stewart, A.J.A., John, E.A. & Hutchings, M.J. (2000). The world is heterogeneous: ecological consequences of living in a patchy environment. In: The Ecological Consequences of Environmental Heterogeneity: 40th Symposium of the British Ecological Society (eds Hutchings, M.J., John, E.A., Stewart, A.J.). Cambridge University Press, Cambridge, UK, pp. 1-8.
46. Tanaka, Y., Sugano, S.S., Shimada, T. & Hara-Nishimura, I. (2013). Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol., 198, 757-764.
47. Westoby, M., Falster, D.S., Moles, A.T., Vesk, P.A. & Wright, I.J. (2002). Plant ecological strategies: some leading dimensions of variation between species. Annu. Rev. Ecol. Syst., 33, 125-159.
48. Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F. et al. (2004). The worldwide leaf economics spectrum. Nature, 428, 821-827.
49. Zhang, S.B., Guan, Z.J., Sun, M., Zhang, J.J., Cao, K.F. & Hu, H. (2012). Evolutionary association of stomatal traits with leaf vein density in Paphiopedilum. Orchidaceae. PloS One, 7, e40080.
50. Zwieniecki, M.A. & Boyce, C.K. (2014). Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proc. R. Soc. B, 281, 20132829.