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Oecologia

, Volume 191, Issue 1, pp 153–164 | Cite as

Intraspecific variation in traits and tree growth along an elevational gradient in a subtropical forest

  • María Natalia UmañaEmail author
  • Nathan G. Swenson
Community ecology – original research
  • 245 Downloads

Abstract

A conspicuous feature of natural communities is that individuals within species exhibit broad variation in their phenotype. While the phenotypic differences among species are prominent and have received considerable attention in earlier studies, recent findings suggest that about 40% of the trait variation is found within species. How this intraspecific variation is related to underlying environmental gradients and ultimately linked to performance is an outstanding question in ecology and evolution. Here, we study six broadly distributed species across an elevational gradient in a subtropical forest. We focused on five functional traits reflecting plant functional differentiation in stem transport, leaf architecture, and leaf resource acquisition. We found that leaf thickness, leaf toughness, and specific leaf area generally varied with elevation, while wood density and leaf area exhibited constrained variation. Results on multivariate trait axes also showed mixed evidence with the PC1 values (positively related to leaf toughness and negatively related to specific leaf area) shifting with elevation, while PC2 values (negatively related to wood density) did not change with elevation. We also found that, despite the important variation in some traits along the gradient, growth performance did not follow this same trend. This suggests that strong directional changes in traits along the gradient may result in similar levels of demographic performance. The results, therefore, challenge the simple expectation that a trait will correlate with a demographic rate. More nuanced approaches and additional mechanisms must be considered to advance understanding of the performance–trait relationships.

Keywords

Broadly distributed species Demographic performance Dendrometer Multivariate trait dimensions Puerto Rico 

Notes

Acknowledgements

We are grateful to Gabriel Arellano, Olivia Barrera, Seth Rifkin, Jess Zimmerman, Samuel Matta, John Bithorn, and Aaron Hogan for their assistance in the field. Jonathan Myers and three anonymous reviewers provided helpful comments that improved this manuscript.

Author contribution statement

MNU and NGS developed and framed the research question. MNU conducted the analyses and wrote the first draft of the manuscript. NGS oversaw the analyses. NGS contributed substantially to the discussion, writing, and revisions of the manuscript.

Funding

This study was funded by The National Science Foundation, USA (DDIG, DEB-1501341).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2019_4453_MOESM1_ESM.docx (41 kb)
Supplementary material 1 (DOCX 40 kb)

References

  1. Ackerly DD, Cornwell WK (2007) A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components. Ecol Lett 10:135–145.  https://doi.org/10.1111/j.1461-0248.2006.01006.x CrossRefGoogle Scholar
  2. Albert CH, Thuiller W, Yaccoz NG, Soudant A, Boucher F, Saccone P, Lavorel S (2010) Intraspecific functional variability: extent, structure and sources of variation. J Ecol 98:604–613.  https://doi.org/10.1111/j.1365-2745.2010.01651.x CrossRefGoogle Scholar
  3. 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 Ecol Evol Syst 13:217–225.  https://doi.org/10.1016/j.ppees.2011.04.003 CrossRefGoogle Scholar
  4. Alfaro ME, Bolnick DI, Wainwright PC (2005) Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am Nat 165:E140–E154.  https://doi.org/10.1086/429564 CrossRefGoogle Scholar
  5. Arellano G, Umaña MN, Macía MJ, Loza MI, Fuentes A, Cala V, Jørgensen PM (2017) The role of niche overlap, environmental heterogeneity, landscape roughness and productivity in shaping species abundance distributions along the Amazon-Andes gradient. Glob Ecol Biogeogr.  https://doi.org/10.1111/geb.12531 Google Scholar
  6. Armbruster WS, Pelabon C, Bolstad GH, Hansen TF (2014) Integrated phenotypes: understanding trait covariation in plants and animals. Philos Trans R Soc B 369:20130245.  https://doi.org/10.1098/rstb.2013.0245 CrossRefGoogle Scholar
  7. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 361:347–361CrossRefGoogle Scholar
  8. Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529.  https://doi.org/10.1111/j.1469-185X.1968.tb00968.x CrossRefGoogle Scholar
  9. Brown S, Lugo AE, Silander S, Liegel L (1983) Research history and opportunities in the Luquillo experimental forest. General report so-44, United States Department of Agriculture (USDA) Forest ServiceGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  11. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366.  https://doi.org/10.1111/j.1461-0248.2009.01285.x CrossRefGoogle Scholar
  12. Clark JS, Dietze M, Chakraborty S, Agarwal PK, Ibanez I, LaDeau S, Wolosin M (2007) Resolving the biodiversity paradox. Ecol Lett 10:647–659.  https://doi.org/10.1111/j.1461-0248.2007.01041.x CrossRefGoogle Scholar
  13. Conover D, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–252CrossRefGoogle Scholar
  14. Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Ter Steege H, Morgan HD, Van Der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380.  https://doi.org/10.1071/BT02124 CrossRefGoogle Scholar
  15. Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126.  https://doi.org/10.1890/07-1134.1 CrossRefGoogle Scholar
  16. Roches Des S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, Schweitzer JA, Palkovacs EP (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–63.  https://doi.org/10.1038/s41559-017-0402-5 CrossRefGoogle Scholar
  17. Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC, Garnier E, Bönisch G, Westoby M, Poorter H, Reich PB, Moles AT, Dickie J, Gillison AN, Zanne AE, Chave J, Wright SJ, Sheremet’ev SN, Jactel H, Christopher B, Cerabolini B, Pierce S, Shipley B, Kirkup D, Casanoves F, Joswig JS, Günther A, Falczuk V, Rüger N, Mahecha MD, Gorné LD (2015) The global spectrum of plant form and function. Nature 529:1–17.  https://doi.org/10.1038/nature16489 Google Scholar
  18. Dolph GE, Dilcher DL (1980) Variation in leaf size with respect to climate in the tropics of the western hemisphere. Torrey Bot Soc 107:154–162CrossRefGoogle Scholar
  19. Enquist BJ, Kerkhoff AJ, Stark SC, Swenson NG, McCarthy MC, Price CA (2007) A general integrative model for scaling plant growth, carbon flux, and functional trait spectra. Nature 449:218–222.  https://doi.org/10.1038/nature06061 CrossRefGoogle Scholar
  20. Fajardo A (2016) Wood density is a poor predictor of competitive ability among individuals of the same species. For Ecol Manag 372:217–225.  https://doi.org/10.1016/j.foreco.2016.04.022 CrossRefGoogle Scholar
  21. Fajardo A, Piper FI (2011) Intraspecific trait variation and covariation in a widespread tree species (Nothofagus pumilio) in southern Chile. New Phytol 189:259–271CrossRefGoogle Scholar
  22. Fajardo A, Siefert A (2016) Phenological variation of leaf functional traits within species. Oecologia 180:951–959.  https://doi.org/10.1007/s00442-016-3545-1 CrossRefGoogle Scholar
  23. Grether GF (2005) Environmental Change, Phenotypic Plasticity, and Genetic Compensation. 166:Google Scholar
  24. Grime JP (1979) Primary strategies in plants. Trans Bot Soc Edinb 43:151–160.  https://doi.org/10.1080/03746607908685348 CrossRefGoogle Scholar
  25. Hillebrand H, Matthiessen B (2009) Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecol Lett 12:1405–1419.  https://doi.org/10.1111/j.1461-0248.2009.01388.x CrossRefGoogle Scholar
  26. Hirose T, Werger MJA (1995) Canopy structure and photon flux partitioning among species in a herbaceous plant community. Ecology 76:466–474CrossRefGoogle Scholar
  27. Hulshof CM, Violle C, Spasojevic MJ, McGill B, Damschen E, Harrison S, Enquist BJ (2013) Intra-specific and inter-specific variation in specific leaf area reveal the importance of abiotic and biotic drivers of species diversity across elevation and latitude. J Veg Sci 24:921–931.  https://doi.org/10.1111/jvs.12041 CrossRefGoogle Scholar
  28. Jung V, Violle C, Mondy C, Hoffmann L, Muller S (2010) Intraspecific variability and trait-based community assembly. J Ecol 98:1134–1140.  https://doi.org/10.1111/j.1365-2745.2010.01687.x CrossRefGoogle Scholar
  29. Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bonisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, Van Bodegom PM, Reichstein M, Enquist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco CC, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanoves F, Cavender-Bares J, Chambers JQ, Chapin FS, Chave J, Coomes D, Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Fernandez-Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez AG, Hickler T, Higgins SI, Hodgson JG, Jalili A, Jansen S, Joly CA, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kuhn I, Kurokawa H, Laughlin D, Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Llusia J, Louault F, Ma S, Mahecha MD, Manning P, Massad T, Medlyn BE, Messier J, Moles AT, Muller SC, Nadrowski K, Naeem S, Niinemets U, Nollert S, Nuske A, Ogaya R, Oleksyn J, Onipchenko VG, Onoda Y, Ordonez J, Overbeck G, Ozinga WA, Patino S, Paula S, Pausas JG, Penuelas J, Phillips OL, Pillar V, Poorter H, Poorter L, Poschlod P, Prinzing A, Proulx R, Rammig A, Reinsch S, Reu B, Sack L, Salgado-Negret B, Sardans J, Shiodera S, Shipley B, Siefert A, Sosinski E, Soussana JF, Swaine E, Swenson N, Thompson K, Thornton P, Waldram M, Weiher E, White M, White S, Wright SJ, Yguel B, Zaehle S, Zanne AE, Wirth C (2011) TRY—a global database of plant traits. Glob Chang Biol 17:2905–2935.  https://doi.org/10.1111/j.1365-2486.2011.02451.x CrossRefGoogle Scholar
  30. Kitajima K, Poorter L (2010) Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytol 186:708–721CrossRefGoogle Scholar
  31. Körner C (1991) Some often overlooked plant characteristics as determinants of plant growth: a reconsideration. Funct Ecol 5:162–173.  https://doi.org/10.2307/2389254 CrossRefGoogle Scholar
  32. Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574.  https://doi.org/10.1016/j.tree.2007.09.006 CrossRefGoogle Scholar
  33. Körner C, Diemer M (1987) In situ photosynthetic responses to light, temperature and carbon dioxide in herbaceous plants from low and high altitude. Funct Ecol 1:179–194CrossRefGoogle Scholar
  34. Kraft NJB, Valencia R, Ackerly DD (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322:580–582.  https://doi.org/10.1126/science.1160662 CrossRefGoogle Scholar
  35. Kraft NJB, Godoy O, Levine JM (2015) Plant functional traits and the multidimensional nature of species coexistence. Proc Natl Acad Sci 112:797–802.  https://doi.org/10.1073/pnas.1413650112 CrossRefGoogle Scholar
  36. Lasky JR, Uriarte M, Boukili VK, Erickson DL, John Kress W, Chazdon RL (2014) The relationship between tree biodiversity and biomass dynamics changes with tropical forest succession. Ecol Lett.  https://doi.org/10.1111/ele.12322 Google Scholar
  37. Laurance WF, Wills C, Harms KE, Condit RS, King D, Thompson J, He F, Muller-landau HC, Ashton PS, Losos E, Comita L, Hubbell S, Lafrankie J, Bunyavejchewin S, Dattaraja HS (2006) Nonrandom processes maintain diversity in tropical forests. Science 311:527–531.  https://doi.org/10.1126/science.311.5766.1376c CrossRefGoogle Scholar
  38. Liu X, Swenson NG, Lin D, Mi X, Umaña MN, Schmid B, Ma K (2016) Linking individual-level functional traits to tree growth in a subtropical forest. Ecology 97:2396–2405.  https://doi.org/10.1002/ecy.1445 CrossRefGoogle Scholar
  39. Marks CO (2007) The causes of variation in tree seedling traits: the roles of environmental selection versus chance. Evolution (NY) 61:455–469.  https://doi.org/10.1111/j.1558-5646.2007.00021.x CrossRefGoogle Scholar
  40. Marks CO, Lechowicz MJ (2006) Alternative designs and the evolution of functional diversity. Am Nat 167:55–66.  https://doi.org/10.1086/498276 CrossRefGoogle Scholar
  41. Messier J, McGill BJ, Lechowicz MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecol Lett 13:838–848.  https://doi.org/10.1111/j.1461-0248.2010.01476.x CrossRefGoogle Scholar
  42. Messier J, Lechowicz MJ, Mcgill BJ, Violle C, Enquist BJ, Val P (2017) Interspecific integration of trait dimensions at local scales: the plant phenotype as an integrated network. J Ecol 105:1775–1790.  https://doi.org/10.1111/1365-2745.12755 CrossRefGoogle Scholar
  43. Muscarella R, Uriarte M (2016) Do community-weighted mean functional traits reflect optimal strategies? Proc R Soc B 283:20152434.  https://doi.org/10.1098/rspb.2015.2434 CrossRefGoogle Scholar
  44. Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Díaz S, Dominy NJ, Elgart A, Enrico L, Fine PV, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Markesteijn L, Pérez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE, Van Bael SA, Warton DI, Wright JJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312.  https://doi.org/10.1111/j.1461-0248.2010.01582.x CrossRefGoogle Scholar
  45. Paine CET, Baraloto C, Chave J, Hérault B (2011) Functional traits of individual trees reveal ecological constraints on community assembly in tropical rain forests. Oikos 120:720–727.  https://doi.org/10.1111/j.1600-0706.2010.19110.x CrossRefGoogle Scholar
  46. Pál C, Papp B, Lercher MJ, Csermely P, Oliver SG, Hurst LD (2006) Chance and necessity in the evolution of minimal metabolic networks. Nature 440:667–670.  https://doi.org/10.1038/nature04568 CrossRefGoogle Scholar
  47. Poorter L, Rozendaal DMA (2008) Leaf size and leaf display of thirty-eight tropical tree species. Oecologia 158:35–46.  https://doi.org/10.1007/s00442-008-1131-x CrossRefGoogle Scholar
  48. Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytol 174:787–798.  https://doi.org/10.1111/j.1469-8137.2007.02061.x CrossRefGoogle Scholar
  49. Preston KA, Cornwell WK, Denoyer JL, Preston KA (1999) Wood density and vessel traits as distinct correlates of ecological strategy in 51 California coast range angiosperms. New Phytol 170:807–818CrossRefGoogle Scholar
  50. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  51. Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Ecology 94:13730–13734.  https://doi.org/10.1073/pnas.94.25.13730 Google Scholar
  52. Rozendaal DMA, Hurtado VH, Poorter L (2006) Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Funct Ecol 20:207–216.  https://doi.org/10.1111/j.1365-2435.2006.01105.x CrossRefGoogle Scholar
  53. Rüger N, Berger U, Hubbell SP, Vieilledent G, Condit R (2011) Growth strategies of tropical tree species: disentangling light and size effects. PLoS One 6:e25330.  https://doi.org/10.1371/journal.pone.0025330 CrossRefGoogle Scholar
  54. Shipley B, Vile D, Garnier É (2006) From plant traits to plant communities: a statistical mechanistic approach to biodiversity. Science 314:812–814CrossRefGoogle Scholar
  55. Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A, Aarssen LW, Baraloto C, Carlucci MB, Cianciaruso MV, de Dantas LV, de Bello F, Duarte LD, Fonseca CR, Freschet GT, Gaucherand S, Gross N, Hikosaka K, Jackson B, Jung V, Kamiyama C, Katabuchi M, Kembel SW, Kichenin E, Kraft NJB, Lagerström A, Bagousse-Pinguet YL, Mason N, Li Y, Messier J, Nakashizuka T, Overton JM, Peltzer DA, Pérez-Ramos IM, Pillar VD, Prentice HC, Richardson S, Richardson T, Schamp BS, Schob C, Shipley B, Sundqvist M, Sykes MT, Vandewalle M, Wardle DA (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol Lett 18:1406–1419.  https://doi.org/10.1111/ele.12508 CrossRefGoogle Scholar
  56. Spasojevic MJ, Yablon E, Oberle B, Myers JA (2014) Ontogenetic trait variation influences tree community assembly across environmental gradients. Ecosphere 5:1–20.  https://doi.org/10.1890/ES14-000159.1 CrossRefGoogle Scholar
  57. Stratton L, Goldstein G, Meinzer FC (2000) Stem water storage capacity and efficiency of water transport: their functional significance in a Hawaiian dry forest. Plant Cell Environ 23:99–106.  https://doi.org/10.1046/j.1365-3040.2000.00533.x CrossRefGoogle Scholar
  58. Swenson NG, Enquist BJ (2008) The relationship between stem and branch wood specific gravity and the ability of each measure to predict leaf area. Am J Bot 95:516–519.  https://doi.org/10.3732/ajb.95.4.516 CrossRefGoogle Scholar
  59. Swenson NG, Enquist BJ (2009) Opposing assembly mechanisms in a Neotropical dry forest: implications for phylogenetic and functional community ecology. Ecology 90:2161–2170.  https://doi.org/10.1890/08-1025.1 CrossRefGoogle Scholar
  60. Swenson NG, Anglada-Cordero P, Barone JA (2011) Deterministic tropical tree community turnover: evidence from patterns of functional beta diversity along an elevational gradient. Proc R Soc B Biol Sci 278:877–884.  https://doi.org/10.1098/rspb.2010.1369 CrossRefGoogle Scholar
  61. Tello JS, Myers JA, Macía MJ, Fuentes AF, Cayola L, Arellano G, Loza MI, Torrez V, Cornejo M, Miranda TB, Jørgensen PM (2015) Elevational gradients in β-diversity reflect variation in the strength of local community assembly mechanisms across spatial scales. PLoS One 10:1–17.  https://doi.org/10.1371/journal.pone.0121458 CrossRefGoogle Scholar
  62. Umaña MN, Zhang C, Cao M, Lin L, Swenson NG (2018a) Quantifying the role of intra-specific trait variation for allocation and organ-level traits in tropical seedling communities. J Veg Sci 29:276–284.  https://doi.org/10.1111/jvs.12613 CrossRefGoogle Scholar
  63. Umaña MN, Zipkin EF, Zhang C, Cao M, Lin L, Swenson NG (2018b) Individual-level trait variation and negative density dependence affect growth in tropical tree seedlings. J Ecol 106:2446–2455.  https://doi.org/10.1111/1365-2745.13001 CrossRefGoogle Scholar
  64. Uriarte M, Swenson NG, Chazdon RL, Comita LS, John Kress W, Erickson D, Forero-Montaña J, Zimmerman JK, Thompson J (2010) Trait similarity, shared ancestry and the structure of neighbourhood interactions in a subtropical wet forest: implications for community assembly. Ecol Lett 13:1503–1514.  https://doi.org/10.1111/j.1461-0248.2010.01541.x CrossRefGoogle Scholar
  65. Vasseur F, Violle C, Granier C, Vile D (2012) A common genetic basis to the origin of the leaf economics spectrum and metabolic scaling allometry. Ecol Lett 15:1149–1157.  https://doi.org/10.1111/j.1461-0248.2012.01839.x CrossRefGoogle Scholar
  66. Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252.  https://doi.org/10.1016/j.tree.2011.11.014 CrossRefGoogle Scholar
  67. Vitousek PM, Shearer G, Kohl DH (1989) Foliar 15 N natural abundance in Hawaiian rainforest: patterns and possible mechanisms. Oecologia 78:383–388CrossRefGoogle Scholar
  68. Westbrook JW, Kitajima K, Burleigh JG, Kress WJ, Erickson DL, Wright SJ (2011) What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade-tolerant woody species in a neotropical forest. Am Nat 177:800–811.  https://doi.org/10.1086/659963 CrossRefGoogle Scholar
  69. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150452 CrossRefGoogle Scholar
  70. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827.  https://doi.org/10.1038/nature02403 CrossRefGoogle Scholar
  71. Yang J, Cao M, Swenson NG (2018) Why functional traits do not predict tree demographic rates. Trends Ecol Evol 33:326–336.  https://doi.org/10.1016/j.tree.2018.03.003 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of BiologyUniversity of MarylandCollege ParkUSA

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