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Plant function and evolutionary biology
RESEARCH ARTICLE

Size dependent associations between tree diameter growth rates and functional traits in an Asian tropical seasonal rainforest

Yu-Mei Yan https://orcid.org/0000-0003-2146-2901 A C , Ze-Xin Fan A B E , Pei-Li Fu https://orcid.org/0000-0001-9092-284X A B , Hui Chen A D and Lu-Xiang Lin A D
+ Author Affiliations
- Author Affiliations

A CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan, 666303, China.

B Centre of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Xishuangbanna, 666303, China.

C University of Chinese Academy of Sciences, Beijing, 100049, China.

D Xishuangbanna Station for Tropical Rain Forest Ecosystem Studies, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan, 666303, China.

E Corresponding author. Email: fanzexin@xtbg.org.cn

Functional Plant Biology 48(2) 231-240 https://doi.org/10.1071/FP20226
Submitted: 30 July 2020  Accepted: 20 September 2020   Published: 30 October 2020

Abstract

Many studies focus on the relationships between plant functional traits and tree growth performances. However, little is known about the ontogenetic shifts of the relationships between functional traits and tree growth. This study examined associations between stem and leaf functional traits and growth rates and their ontogenetic shifts across 20 tropical tree species in a tropical seasonal rainforest in Xishuangbanna, south-west China. For each species, physiological active branches of individual trees belonged to three size classes (i.e. small, diameter at breast height (DBH) 5–10 cm; middle, DBH 10–20 cm; big, DBH >20 cm) were sampled respectively. We measured 18 morphological and structural traits, which characterised plant hydraulic properties or leaf economic spectrum. Associations between diameter growth rates and functional traits were analysed across three size classes. Our results revealed that diameter growth rates of big-sized trees were mainly related to traits related to plant hydraulic efficiency (i.e. theoretical hydraulic conductivity (Ktheo) and leaf vein density (Dvein)), which suggests that the growth of large trees is limited mainly by their xylem water transport capacity. For middle-sized trees, growth rates were significantly related to traits representing leaf economic spectrum (i.e. specific leaf area (SLA), individual leaf mass (ILM), palisade thickness (PT) and spongy thickness (SP)). Diameter growth rates of small-sized trees were not correlated with hydraulic or leaf economic traits. Thus, the associations between tree growth rates and functional traits are size dependent. Our results suggest ontogenetic shift of functional traits which could potential contribute to different growth response to climate change.

Keywords: functional trait, growth rate, hydraulic conductivity, leaf economic spectrum, palisade thickness, size dependent, specific leaf area, stomatal size, theoretical hydraulic conductivity, tree growth, tropical rainforest, vessel density.


References

Baltzer JL, Thomas SC (2007) Physiological and morphological correlates of whole-plant light compensation point in temperate deciduous tree seedlings. Oecologia 153, 209–223.
Physiological and morphological correlates of whole-plant light compensation point in temperate deciduous tree seedlings.Crossref | GoogleScholarGoogle Scholar | 17453256PubMed |

Beerling DJ, Franks PJ (2010) Plant science: the hidden cost of transpiration. Nature 464, 495–496.
Plant science: the hidden cost of transpiration.Crossref | GoogleScholarGoogle Scholar | 20336123PubMed |

Bennett AC, McDowell NG, Allen CD, Anderson-Teixeira KJ (2015) Larger trees suffer most during drought in forests worldwide. Nature Plants 1, 15139
Larger trees suffer most during drought in forests worldwide.Crossref | GoogleScholarGoogle Scholar | 27251391PubMed |

Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B: Biological Sciences 276, 1771–1776.
Angiosperm leaf vein evolution was physiologically and environmentally transformative.Crossref | GoogleScholarGoogle Scholar | 19324775PubMed |

Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13, 175–183.
Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification.Crossref | GoogleScholarGoogle Scholar | 19968696PubMed |

Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
Leaf maximum photosynthetic rate and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 17556506PubMed |

Cao M, Zhang J (1997) Tree species diversity of tropical forest vegetation in Xishuangbanna, SW China. Biodiversity and Conservation 6, 995–1006.

Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecology Letters 12, 351–366.
Towards a worldwide wood economics spectrum.Crossref | GoogleScholarGoogle Scholar | 19243406PubMed |

De Micco V, Carrer M, Rathgeber CBK, Camarero J, Voltas J, Cherubini P, Battipaglia G (2019) From xylogenesis to tree rings: wood traits to investigate tree response to environmental changes. International Association of Wood Anatomists Journal 40, 155–182.
From xylogenesis to tree rings: wood traits to investigate tree response to environmental changes.Crossref | GoogleScholarGoogle Scholar |

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.
A general integrative model for scaling plant growth, carbon flux, and functional trait spectra.Crossref | GoogleScholarGoogle Scholar | 17851525PubMed |

Falster DS, Westoby M (2003) Leaf size and angle vary widely across species: what consequences for light interception? New Phytologist 158, 509–525.
Leaf size and angle vary widely across species: what consequences for light interception?Crossref | GoogleScholarGoogle Scholar |

Fan ZX, Zhang SB, Hao GY, Ferry Slik JW, Cao KF (2012) Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density. Journal of Ecology 100, 732–741.
Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density.Crossref | GoogleScholarGoogle Scholar |

Gibert A, Gray EF, Westoby M, Wright IJ, Falster DS (2016) On the link between functional traits and growth rate: meta-analysis shows effects change with plant size, as predicted. Journal of Ecology 104, 1488–1503.
On the link between functional traits and growth rate: meta-analysis shows effects change with plant size, as predicted.Crossref | GoogleScholarGoogle Scholar |

Givnish TJ (1995) Plant stems: biomechanical adaptation for energy capture and influence on species distributions. In ‘Plant stems physiology and functional morphology’. (Ed. BL Gartner) pp. 3–49. (Academic Press: San Diego)

Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, et al. (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79, 259–281.
Integrated screening validates primary axes of specialisation in plants.Crossref | GoogleScholarGoogle Scholar |

Hietz P, Rosner S, Hietz-Seifert U, Wright SJ (2017) Wood traits related to size and life history of trees in a Panamanian rainforest. New Phytologist 213, 170–180.
Wood traits related to size and life history of trees in a Panamanian rainforest.Crossref | GoogleScholarGoogle Scholar | 27533709PubMed |

Hoeber S, Leuschner C, Köhler L, Arias-Aguilar D, Schuldt B (2014) The importance of hydraulic conductivity and wood density to growth performance in eight tree species from a tropical semi-dry climate. Forest Ecology and Management 330, 126–136.
The importance of hydraulic conductivity and wood density to growth performance in eight tree species from a tropical semi-dry climate.Crossref | GoogleScholarGoogle Scholar |

Iida Y, Poorter L, Sterck F, Kassim AR, Matthew DP, Kubo T, Takashi SK (2014a) Linking size-dependent growth and mortality with architectural traits across 145 co-occurring tropical tree species. Ecology 95, 353–363.
Linking size-dependent growth and mortality with architectural traits across 145 co-occurring tropical tree species.Crossref | GoogleScholarGoogle Scholar | 24669729PubMed |

Iida Y, Kohyama TS, Swenson NG, Su SH, Chen CT, Chiang JM, Sun IF, Zuidema P (2014b) Linking functional traits and demographic rates in a subtropical tree community: the importance of size dependency. Journal of Ecology 102, 641–650.
Linking functional traits and demographic rates in a subtropical tree community: the importance of size dependency.Crossref | GoogleScholarGoogle Scholar |

Jamir A, Schiavini I, Vagner S, Raymundo D, Sergio F, Poorter L (2016) Functional traits shape size-dependent growth and mortality rates of dry forest tree species. Journal of Plant Ecology 10, 895–906.

Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch 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, et al. (2011) TRY – a global database of plant traits. Global Change Biology 17, 2905–2935.
TRY – a global database of plant traits.Crossref | GoogleScholarGoogle Scholar |

Kerkhoff AJ, Enquist BJ (2009) Multiplicative by nature: why logarithmic transformation is necessary in allometry. Journal of Theoretical Biology 257, 519–521.
Multiplicative by nature: why logarithmic transformation is necessary in allometry.Crossref | GoogleScholarGoogle Scholar |

King DA (2011) Size-related changes in tree proportions and their potential influence on the course of height growth. In ‘Size- and age-related changes in tree structure and function’. (Eds FC Meinzer, B Lachenbruch, TE Dawson). pp. 165–192. (Springer: New York)

Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428, 851–854.
The limits to tree height.Crossref | GoogleScholarGoogle Scholar | 15103376PubMed |

Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23, 283–362.

Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. Journal of Statistical Software 25, 1–18.
FactoMineR: an R package for multivariate analysis.Crossref | GoogleScholarGoogle Scholar |

Markesteijn L, Poorter L, Paz H, Sack L, Bongers F (2011) Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits. Plant, Cell & Environment 34, 137–148.
Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits.Crossref | GoogleScholarGoogle Scholar |

McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21, 178–185.
Rebuilding community ecology from functional traits.Crossref | GoogleScholarGoogle Scholar |

McKown AD, Cochard H, Sack L (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. American Naturalist 175, 447–460.
Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution.Crossref | GoogleScholarGoogle Scholar | 20178410PubMed |

Mouillot D, Graham NA, Villeger S, Mason NW, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends in Ecology & Evolution 28, 167–177.
A functional approach reveals community responses to disturbances.Crossref | GoogleScholarGoogle Scholar |

Niinemets U, Valladares F (2004) Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Plant Biology 6, 254–268.
Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints.Crossref | GoogleScholarGoogle Scholar | 15143434PubMed |

Paine CET, Amissah L, Auge H, Baraloto C, Baruffol M, Bourland N, Bruelheide H, Daïnou K, de Gouvenain RC, Doucet J-L, Doust S, Fine PVA, Fortunel C, Haase J, Holl KD, Jactel H, Li X, Kitajima K, Koricheva J, Martínez-Garza C, et al. (2015) Globally, functional traits are weak predictors of juvenile tree growth, and we do not know why. Journal of Ecology 103, 978–989.
Globally, functional traits are weak predictors of juvenile tree growth, and we do not know why.Crossref | GoogleScholarGoogle Scholar |

Phillips OL, van der Heijden G, Lewis SL, Lopez-Gonzalez G, Aragao LE, Lloyd J, Malhi Y, Monteagudo A, Almeida S, Davila EA, Amaral I, Andelman S, Andrade A, Arroyo L, Aymard G, Baker TR, Blanc L, Bonal D, de Oliveira AC, Chao KJ, et al. (2010) Drought-mortality relationships for tropical forests. New Phytologist 187, 631–646.
Drought-mortality relationships for tropical forests.Crossref | GoogleScholarGoogle Scholar | 20659252PubMed |

Poorter L (2009) Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests. New Phytologist 181, 890–900.
Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests.Crossref | GoogleScholarGoogle Scholar | 19140935PubMed |

Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87, 1733–1743.
Leaf traits are good predictors of plant performance across 53 rain forest species.Crossref | GoogleScholarGoogle Scholar | 16922323PubMed |

Poorter L, Wright SJ, Paz H, Ackerly D, Condit R, Ibarra-Manríquez G, Harms K, Licona J, Martínez-Ramos M, Mazer S (2008) Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89, 1908–1920.
Are functional traits good predictors of demographic rates? Evidence from five neotropical forests.Crossref | GoogleScholarGoogle Scholar | 18705377PubMed |

Poorter L, van der Sande MT, Arets EJMM, Ascarrunz N, Enquist BJ, Finegan B, Licona JC, Martínez-Ramos M, Mazzei L, Meave JA, Muñoz R, Nytch CJ, de Oliveira AA, Pérez-García EA, Prado-Junior J, Rodríguez-Velázques J, Ruschel AR, Salgado-Negret B, Schiavini I, Swenson NG, et al. (2017) Biodiversity and climate determine the functioning of neotropical forests. Global Ecology and Biogeography 26, 1423–1434.
Biodiversity and climate determine the functioning of neotropical forests.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2018) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing, Vienna, Austria) Available at https://www.R-project.org/ [Verified 28 September 2020]

Reich P, Walters M, Ellsworth D (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs 62, 365–392.
Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Wright I-BJ, Craine JM, Oleksyn J (2003) The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164, S143–S164.
The evolution of plant functional variation: traits, spectra, and strategies.Crossref | GoogleScholarGoogle Scholar |

Rowland L, da Costa AC, Galbraith DR, Oliveira RS, Binks OJ, Oliveira AA, Pullen AM, Doughty CE, Metcalfe DB, Vasconcelos SS, Ferreira LV, Malhi Y, Grace J, Mencuccini M, Meir P (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528, 119–122.
Death from drought in tropical forests is triggered by hydraulics not carbon starvation.Crossref | GoogleScholarGoogle Scholar | 26595275PubMed |

Rüger N, Wirth C, Wright SJ, Condit R (2012) Functional traits explain light and size response of growth rates in tropical tree species. Ecology 93, 2626–2636.
Functional traits explain light and size response of growth rates in tropical tree species.Crossref | GoogleScholarGoogle Scholar | 23431593PubMed |

Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant, Cell & Environment 29, 367–381.
The hydraulic limitation hypothesis revisited.Crossref | GoogleScholarGoogle Scholar |

Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140, 543–550.
Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees.Crossref | GoogleScholarGoogle Scholar | 15232729PubMed |

Sperry JS, Hacke UG, Jarmila P (2006) Size and function in conifer tracheids and angiosperm vessels. American Journal of Botany 93, 1490–1500.
Size and function in conifer tracheids and angiosperm vessels.Crossref | GoogleScholarGoogle Scholar | 21642096PubMed |

Sterck FJ, Bongers F (2001) Crown development in tropical rain forest trees: patterns with tree height and light availability. Journal of Ecology 89, 1–13.
Crown development in tropical rain forest trees: patterns with tree height and light availability.Crossref | GoogleScholarGoogle Scholar |

Sterck F, Martinéz-Ramos M, Dyer-Leal G, Rodríguez-Velazquez J, Poorter L (2003) The consequences of crown traits for the growth and survival of tree saplings in a Mexican lowland rainforest. Functional Ecology 17, 194–200.
The consequences of crown traits for the growth and survival of tree saplings in a Mexican lowland rainforest.Crossref | GoogleScholarGoogle Scholar |

Thomas SC (2011) Age-related changes in tree growth and functional biology: the role of reproduction. In ‘Size- and age-related changes in tree structure and function’. (Eds FC Meinzer, B Lachenbruch, TE Dawson) pp. 33–64. (Springer: New York)

Visser MD, Bruijning M, Wright SJ, Muller-Landau HC, Jongejans E, Comita LS, de Kroon H (2016) Functional traits as predictors of vital rates across the life cycle of tropical trees. Functional Ecology 30, 168–180.
Functional traits as predictors of vital rates across the life cycle of tropical trees.Crossref | GoogleScholarGoogle Scholar |

Voltas J, Camarero JJ, Carulla D, Aguilera M, Ortiz A, Ferrio JP (2013) A retrospective, dualisotope approach reveals individual predispositions to winter-drought induced tree dieback in the southernmost distribution limit of Scots pine. Plant, Cell & Environment 36, 1435–1448.
A retrospective, dualisotope approach reveals individual predispositions to winter-drought induced tree dieback in the southernmost distribution limit of Scots pine.Crossref | GoogleScholarGoogle Scholar |

Wright I, Westoby M (1999) Differences in seedling growth behaviour among species trait correlations across species and trait shifts along nutrient compared to rainfall gradients. Journal of Ecology 87, 85–97.
Differences in seedling growth behaviour among species trait correlations across species and trait shifts along nutrient compared to rainfall gradients.Crossref | GoogleScholarGoogle Scholar |

Wright IJ, Reich PB, Mark W, Ackerly DD, Zdravko B, Frans B, Jeannine C-B, Terry C, Cornelissen JHC, Matthias D, Jaume F, Eric G, Groom PK, Javier G, Kouki H, Lamont BB, Tali L, William L, Christopher L, Midgley JJ, et al. (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 15103368PubMed |

Wright IJ, Falster DS, Pickup M, Westoby M (2006) Cross-species patterns in the coordination between leaf and stem traits, and their implications for plant hydraulics. Physiologia Plantarum 127, 445–456.
Cross-species patterns in the coordination between leaf and stem traits, and their implications for plant hydraulics.Crossref | GoogleScholarGoogle Scholar |

Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ, Bunker DE, Richard C, Dalling JW, Davies SJ, Sandra D (2010) Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91, 3664–3674.
Functional traits and the growth-mortality trade-off in tropical trees.Crossref | GoogleScholarGoogle Scholar | 21302837PubMed |

Wright IJ, Cooke J, Cernusak LA, Hutley LB, Scalon MC, Tozer WC, Lehmann CER (2019) Stem diameter growth rates in a fire-prone savanna correlate with photosynthetic rate and branch-scale biomass allocation, but not specific leaf area. Austral Ecology 44, 339–350.
Stem diameter growth rates in a fire-prone savanna correlate with photosynthetic rate and branch-scale biomass allocation, but not specific leaf area.Crossref | GoogleScholarGoogle Scholar |

Yang J, Cao M, Swenson NG (2018) Why functional traits do not predict tree demographic rates. Trends in Ecology & Evolution 33, 326–336.
Why functional traits do not predict tree demographic rates.Crossref | GoogleScholarGoogle Scholar |

Yang J, Song XY, Zambrano J, Chen YX, Cao M, Deng XB, Zhang WF, Yang XF, Zhang GC, Tang Y, Swenson NG (2020) Intra-specific variation in tree growth responses to neighborhood composition and seasonal drought in a tropical forest. Journal of Ecology
Intra-specific variation in tree growth responses to neighborhood composition and seasonal drought in a tropical forest.Crossref | GoogleScholarGoogle Scholar |

Yoda K (1974) Three-dimensional distribution of light intensity in a tropical rain forest of west Malaysia. Japanese Journal of Ecology 24, 247–254.