Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Co-ordinated performance of leaf hydraulics and economics in 10 Chinese temperate tree species

Ying Jin A , Chuankuan Wang A B , Zhenghu Zhou A and Zhimin Li A
+ Author Affiliations
- Author Affiliations

A Center for Ecological Research, Northeast Forestry University, 26 Hexing Road, Harbin 150040, China.

B Corresponding author. Email: wangck-cf@nefu.edu.cn

Functional Plant Biology 43(11) 1082-1090 https://doi.org/10.1071/FP16097
Submitted: 14 March 2016  Accepted: 21 June 2016   Published: 3 August 2016

Abstract

Exploring relationships between leaf hydraulics and economic traits is important in understanding the carbon–water coupling and in extending the leaf economics spectrum. In this study, leaf hydraulics, photosynthesis, structural and nutrient traits and photosynthetic resource use efficiency were measured for 10 temperate tree species in the north-eastern China. Leaf hydraulic conductance was positively correlated with photosynthetic traits, specific leaf area, leaf nitrogen concentration, photosynthetic water and nitrogen use efficiencies, suggesting co-ordination between leaf hydraulics and economic traits. Principal component analysis revealed that significant correlations existed among leaf hydraulic, photosynthetic and resource use traits (axis 1), and axis 2 was strongly associated with leaf structural and nutrient traits. The 10 species were distributed along the diagonal line between axis 1 and axis 2. Species displaying the ‘fast’ strategy tended to have higher photosynthetic rates, leaf hydraulic conductance and photosynthetic water and nutrient use efficiencies; however, they also had lower carbon investment and faced a greater risk of embolism. These findings indicate that leaf hydraulics, economics and resource uses together play an important role in determining species ecological strategies, and provide supports for the ‘fast–slow’ leaf economics spectrum.

Additional keywords: leaf economics, leaf hydraulic conductance, nutrient use efficiency, photosynthesis, water use efficiency.


References

Bai KD, He CX, Wan XC, Jiang DB (2015) Leaf economics of evergreen and deciduous tree species along an elevational gradient in a subtropical mountain. AoB Plants 7, plv064
Leaf economics of evergreen and deciduous tree species along an elevational gradient in a subtropical mountain.Crossref | GoogleScholarGoogle Scholar |

Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytologist 188, 1113–1123.
Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms.Crossref | GoogleScholarGoogle Scholar | 20738785PubMed |

Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecology Letters 14, 91–100.
Venation networks and the origin of the leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 21073643PubMed |

Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132, 2166–2173.
Stomatal closure during leaf dehydration, correlation with other leaf physiological traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsVantbc%3D&md5=50f4503d0a82eaf1950814a5e94c1670CAS | 12913171PubMed |

Brodribb TJ, Holbrook NM (2004) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant, Cell & Environment 27, 820–827.
Diurnal depression of leaf hydraulic conductance in a tropical tree species.Crossref | GoogleScholarGoogle Scholar |

Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist 165, 839–846.
Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima.Crossref | GoogleScholarGoogle Scholar | 15720695PubMed |

Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rates and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
Leaf maximum photosynthetic rates and venation are linked by hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=52674169ae1dca1c088306428cad4fedCAS | 1:CAS:528:DC%2BD2sXpsVOgs7s%3D&md5=52674169ae1dca1c088306428cad4fedCAS | 17556506PubMed |

Brodribb TJ, Skelton RP, Mcadam SAM, Lucani CJ, Marmottant P (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209, 1403–1409.
Visual quantification of embolism reveals leaf vulnerability to hydraulic failure.Crossref | GoogleScholarGoogle Scholar | 26742653PubMed |

Bucci SJ, Scholz FG, Campanello PI, Montti L, Jimenez-Castillo M, Rockwell FA, La Manna L, Guerra P, Lopez Bernal P, Troncoso O, Enricci J, Holbrook MN, Goldstein G (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiology 32, 880–893.
Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality?Crossref | GoogleScholarGoogle Scholar | 22684354PubMed |

Feild TS, Balun L (2008) Xylem hydraulic and photosynthetic function of Gnetum (Gnetales) species from Papua New Guinea. New Phytologist 177, 665–675.
Xylem hydraulic and photosynthetic function of Gnetum (Gnetales) species from Papua New Guinea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1altr0%3D&md5=587a7645f8cb3da8d7c4b779638546d9CAS | 18067531PubMed |

Feild TS, Upchurch GR, Chatelet DS, Brodribb TJ, Grubbs KC, Samain MS, Wanke S (2011) Fossil evidence for low gas exchange capacities for early Cretaceous angiosperm leaves. Paleobiology 37, 195–213.
Fossil evidence for low gas exchange capacities for early Cretaceous angiosperm leaves.Crossref | GoogleScholarGoogle Scholar |

Fichot R, Chamaillard S, Depardieu C, Le Thiec D, Cochard H, Barigah TS, Brignolas F (2011) Hydraulic efficiency and co-ordination with xylem resistance to cavitation, leaf function, and growth performance among eight unrelated Populus deltoides × Populus nigra hybrids. Journal of Experimental Botany 62, 2093–2106.
Hydraulic efficiency and co-ordination with xylem resistance to cavitation, leaf function, and growth performance among eight unrelated Populus deltoides × Populus nigra hybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFyjurg%3D&md5=c7e8a6bc3c3126545e9d439684e731b5CAS | 21193576PubMed |

Guo S, Kaldenhoff R, Uehlein N, Sattelmacher B, Brueck H (2007) Relationship between water and nitrogen uptake in nitrate-and ammonium-supplied Phaseolus vulgaris L. plants. Journal of Plant Nutrition and Soil Science 170, 73–80.
Relationship between water and nitrogen uptake in nitrate-and ammonium-supplied Phaseolus vulgaris L. plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtFylu7Y%3D&md5=7f28796512d48b95610a20a3288d1f70CAS |

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.
Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems.Crossref | GoogleScholarGoogle Scholar | 18049826PubMed |

Kikuzawa K, Onoda Y, Wright IJ, Reich PB (2013) Mechanisms underlying global temperature-related patterns in leaf longevity. Global Ecology and Biogeography 22, 982–993.
Mechanisms underlying global temperature-related patterns in leaf longevity.Crossref | GoogleScholarGoogle Scholar |

Li L, McCormack ML, Ma CE, Kong DL, Zhang Q, Chen XY, Zeng H, Niinemets U, Guo DL (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical–subtropical forests. Ecology Letters 18, 899–906.
Leaf economics and hydraulic traits are decoupled in five species-rich tropical–subtropical forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Onsr7I&md5=4cf4084e42abfe4fae7ab50abeef3e73CAS | 26108338PubMed |

McCulloh K, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S (2010) Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. New Phytologist 186, 439–450.
Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests.Crossref | GoogleScholarGoogle Scholar | 20158616PubMed |

McCulloh KA, Meinzer FC, Sperry JS, Lachenbruch B, Voelker SL, Woodruff DR, Domec JC (2011) Comparative hydraulic architecture of tropical tree species representing a range of successional stages and wood density. Oecologia 167, 27–37.
Comparative hydraulic architecture of tropical tree species representing a range of successional stages and wood density.Crossref | GoogleScholarGoogle Scholar | 21445684PubMed |

Nardini A, Luglio J (2014) Leaf hydraulic capacity and drought vulnerability: possible trade-offs and correlations with climate across three major biomes. Functional Ecology 28, 810–818.
Leaf hydraulic capacity and drought vulnerability: possible trade-offs and correlations with climate across three major biomes.Crossref | GoogleScholarGoogle Scholar |

Nardini A, Pedà G, Rocca NL (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. New Phytologist 196, 788–798.
Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences.Crossref | GoogleScholarGoogle Scholar | 22978628PubMed |

Parkhurst DF (1994) Diffusion of CO2 and other gases inside leaves. New Phytologist 126, 449–479.
Diffusion of CO2 and other gases inside leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVequ7c%3D&md5=0de01c617d7d7f0d6d14f3815ecd84efCAS |

Pivovaroff AL, Sack L, Santiago LS (2014) Co-ordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis. New Phytologist 203, 842–850.
Co-ordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis.Crossref | GoogleScholarGoogle Scholar | 24860955PubMed |

Pou A, Medrano H, Flexas J, Tyerman SD (2013) A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering. Plant, Cell & Environment 36, 828–843.
A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and re-watering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjs1eks74%3D&md5=6ea5ba0b29cae77b1ef46e9e0044b8adCAS |

Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275–301.
The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Walters MB, Ellsworth DS (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, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12, 948–958.
Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups.Crossref | GoogleScholarGoogle Scholar |

Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
Leaf hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKhtrs%3D&md5=f7445993b3921033fee6db1a9edd7ae6CAS | 16669766PubMed |

Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytologist 198, 983–1000.
Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future.Crossref | GoogleScholarGoogle Scholar | 23600478PubMed |

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 | 1:STN:280:DC%2BD2cvgsFWhsg%3D%3D&md5=b746882301de4c0610e1cadd29de5539CAS | 15232729PubMed |

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.
Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrk%3D&md5=7701b5b0b59423a7cb4b672db7cae79eCAS | 21511989PubMed |

Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: co-ordination with hydraulic vulnerability and drought tolerance. Plant Physiology 164, 1772–1788.
Leaf shrinkage with dehydration: co-ordination with hydraulic vulnerability and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmsV2js70%3D&md5=3f38333a05335ab748e3bb2637829898CAS | 24306532PubMed |

Shiflett SA, Zinnert JC, Young DR (2014) Co-ordination of leaf N, anatomy, photosynthetic capacity, and hydraulics enhances evergreen expansive potential. Trees 28, 1635–1644.
Co-ordination of leaf N, anatomy, photosynthetic capacity, and hydraulics enhances evergreen expansive potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVeqtL7E&md5=f3c632b04d1473aa43a7c279dd67ef69CAS |

Simonin KA, Limm EB, Dawson TE (2012) Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain. New Phytologist 193, 939–947.
Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain.Crossref | GoogleScholarGoogle Scholar | 22224403PubMed |

Soudzilovskaia NA, Elumeeva TG, Onipchenko VG, Shidakov II, Salpagarova FS, Khubiev AB, Tekeev DK, Cornelissen JHC (2013) Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proceedings of the National Academy of Sciences of the United States of America 110, 18180–18184.
Functional traits predict relationship between plant abundance dynamic and long-term climate warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVSmurnP&md5=999825099329179966df345b8a4d32bcCAS | 24145400PubMed |

Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13–23.
Hydraulic constraints on plant gas exchange.Crossref | GoogleScholarGoogle Scholar |

Sperry JS, Hacke UG, Pittermann J (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 |

Terashima I, Hirosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant, Cell & Environment 18, 1111–1128.
Comparative ecophysiology of leaf and canopy photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23, 267–282.
The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique.Crossref | GoogleScholarGoogle Scholar |

Villagra M, Campanello PI, Bucci SJ, Goldstein G (2013) Functional relationships between leaf hydraulics and leaf economic traits in response to nutrient addition in subtropical tree species. Tree Physiology 33, 1308–1318.
Functional relationships between leaf hydraulics and leaf economic traits in response to nutrient addition in subtropical tree species.Crossref | GoogleScholarGoogle Scholar | 24284866PubMed |

Wang C (2006) Biomass allometric equations for 10 co-occurring tree species in Chinese temperate forests. Forest Ecology and Management 222, 9–16.
Biomass allometric equations for 10 co-occurring tree species in Chinese temperate forests.Crossref | GoogleScholarGoogle Scholar |

Wang CK, Yi H, Chen JQ, Wang XC, Zhang QZ, Bond-Lamberty B (2013) Seasonality of soil CO2 efflux in a temperate forest: biophysical effects of snowpack and spring freeze-thaw cycles. Agricultural and Forest Meteorology 177, 83–92.
Seasonality of soil CO2 efflux in a temperate forest: biophysical effects of snowpack and spring freeze-thaw cycles.Crossref | GoogleScholarGoogle Scholar |

Westoby M, Reich PB, Wright IJ (2013) Understanding ecological variation across species: area-based vs mass-based expression of leaf traits. New Phytologist 199, 322–323.
Understanding ecological variation across species: area-based vs mass-based expression of leaf traits.Crossref | GoogleScholarGoogle Scholar | 23692294PubMed |

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, et al (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=d60b0f91594517529da250089e292021CAS | 15103368PubMed |

Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytologist 166, 485–496.
Assessing the generality of global leaf trait relationships.Crossref | GoogleScholarGoogle Scholar | 15819912PubMed |

Xiong DL, Yu TT, Zhang T, Li Y, Peng SB, Huang JL (2015a) Leaf hydraulic conductance is co-ordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza. Journal of Experimental Botany 66, 741–748.
Leaf hydraulic conductance is co-ordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGisLfO&md5=7030c33498c34f2627f3987b2943470cCAS |

Xiong DL, Yu TT, Liu X, Li Y, Peng SB, Huang JL (2015b) Heterogeneity of photosynthesis within leaves is associated with alteration of leaf structural features and leaf N content per leaf area in rice. Functional Plant Biology 42, 687–696.
Heterogeneity of photosynthesis within leaves is associated with alteration of leaf structural features and leaf N content per leaf area in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXps1Okurg%3D&md5=dbd0f912af2d17470fdb29c73aa71f77CAS |

Zhang JL, Cao KF (2009) Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Functional Ecology 23, 658–667.
Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species.Crossref | GoogleScholarGoogle Scholar |

Zhang YJ, Cao KF, Sack L, Li N, Wei XM, Goldstein G (2015) Extending the generality of leaf economic design principles in the cycads, an ancient lineage. New Phytologist 206, 817–829.
Extending the generality of leaf economic design principles in the cycads, an ancient lineage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvFCksLg%3D&md5=0ca2c02f851fe27bc91328e08010902dCAS | 1:CAS:528:DC%2BC2MXkvFCksLg%3D&md5=0ca2c02f851fe27bc91328e08010902dCAS | 25622799PubMed |

Zhu SD, Song JJ, Li RH, Ye Q (2013) Plant hydraulics and photosynthesis of 34 woody species from different successional stages of subtropical forests. Plant, Cell & Environment 36, 879–891.
Plant hydraulics and photosynthesis of 34 woody species from different successional stages of subtropical forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjs1eksro%3D&md5=c63857f8a94f5b7c1fd5ccf6a3d7f89dCAS | 1:CAS:528:DC%2BC3sXjs1eksro%3D&md5=c63857f8a94f5b7c1fd5ccf6a3d7f89dCAS |

Zhu SD, Chen YJ, Cao KF, Ye Q (2015) Interspecific variation in branch and leaf traits among three Syzygium tree species from different successional tropical forests. Functional Plant Biology 42, 423–432.
Interspecific variation in branch and leaf traits among three Syzygium tree species from different successional tropical forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXksVSmsbY%3D&md5=ca717457dbefdc5053aa3be55668abdcCAS | 1:CAS:528:DC%2BC2MXksVSmsbY%3D&md5=ca717457dbefdc5053aa3be55668abdcCAS |

Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM (2002) Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25, 1445–1450.
Hydraulic architecture of leaf venation in Laurus nobilis L.Crossref | GoogleScholarGoogle Scholar |

Zwieniecki MA, Brodribb TJ, Holbrook NM (2007) Hydraulic design of leaves: insights from rehydration kinetics. Plant, Cell & Environment 30, 910–921.
Hydraulic design of leaves: insights from rehydration kinetics.Crossref | GoogleScholarGoogle Scholar |