Skip to main content
Log in

Adjustment of leaf anatomical and hydraulic traits across vertical canopy profiles of young broadleaved forest stands

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

No evidence of coordination between leaf hydraulic function and stomatal characteristics was observed in young hybrid aspen stands attributable to the near-anisohydric behaviour and the fast-growing nature of this species.

Abstract

Within forest canopies, there are environmental gradients that enhance water losses in the direction of treetops. Therefore, the foliar morpho-anatomical plasticity, which allows plant acclimation to environmental variations, is of great importance, but empirical information about the relationship between leaf structural and functional traits is inconsistent, varying with ecological requirements and the life strategy of the species. In this study, leaf hydraulic conductance, anatomical structure, and stomatal morphology were investigated in young hybrid aspen (Populus tremula × P. tremuloides) stands to elucidate the coordination between structural and hydraulic traits within the canopy. Stomatal size and density demonstrated opposite trends with respect to leaf location, leading to a relatively uniform spatial distribution of potential gas exchange capacity in the canopy. The hydraulic system of branches was adjusted to maximise the potential water supply in the midcanopy, containing nearly half of the trees’ total photosynthetic surface. Most vascular traits in both the petioles and laminae demonstrated stronger development towards the treetop that should enhance the water supply of the upper foliage, which is exposed to higher irradiance and atmospheric evaporative demand. Small increases in the total vein density expressed per unit lamina area in the upper canopy could not compensate for substantial leaf thickening, resulting in decreased vein density expressed per unit lamina volume and increasing the resistance of the leaf extravascular pathway. No solid evidence of coordination was found between leaf hydraulic function and stomatal characteristics attributable to the near-anisohydric behaviour and the fast-growing nature of this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aasamaa K, Sõber A (2012) Light sensitivity of shoot hydraulic conductance in five temperate deciduous tree species. Funct Plant Biol 39:661–669

    Article  CAS  PubMed  Google Scholar 

  • Aasamaa K, Niinemets Ü, Sõber A (2005) Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny. Tree Physiol 25:1409–1418

    Article  PubMed  Google Scholar 

  • Aasamaa K, Kõivik K, Kupper P, Sõber A (2014) Growth environment determines light sensitivity of shoot hydraulic conductance. Ecol Res 29:143–151

    Article  Google Scholar 

  • Abrams MD, Kubiske ME (1990) Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: Influence of light regime and shade-tolerance rank. Forest Ecol Manag 31:245–253

    Article  Google Scholar 

  • Al Afas N, Pellis A, Niinemets Ü, Ceulemans R (2005) Growth and production of a short rotation coppice culture of poplar. II. Clonal and year-to-year differences in leaf and petiole characteristics and stand leaf area index. Biomass Bioenergy 28:536–547

    Article  Google Scholar 

  • Blonder B, Violle C, Enquist BJ (2013) Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides. J Ecol 101:981–989

    Article  Google Scholar 

  • Boonman CCF, Benítez-López A, Schipper AM et al (2020) Assessing the reliability of predicted plant trait distributions at the global scale. Glob Ecol Biogeogr 29:1034–1051

    Article  PubMed  PubMed Central  Google Scholar 

  • Bréda N, Soudani K, Bergonzini J-C (2002) Mesure de l’indice foliaire en forêt. Ecofor, Paris

    Google Scholar 

  • Brodribb TJ, Field TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley TN, Grace PJ, Scoffoni C, Sack L (2015) How does leaf anatomy influence water transport outside the xylem? Plant Physiol 168:1616–1635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell GS, Norman JM (1989) The description and measurement of plant canopy structure. In: Russell G, Marshall B, Jarvis PG (eds) Plant canopies: their growth, form and function society for experimental biology. Seminar series 31. Cambridge University Press, Cambridge, pp 1–19

    Google Scholar 

  • Carins Murphy MR, Jordan GJ, Brodribb TJ (2014) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant Cell Environ 37:124–131

    Article  CAS  PubMed  Google Scholar 

  • Carins Murphy MR, Jordan GJ, Brodribb TJ (2017) Ferns are less dependent on passive dilution by cell expansion to coordinate leaf vein and stomatal spacing than angiosperms. PLoS ONE 12(9):e0185648

    Article  PubMed  PubMed Central  Google Scholar 

  • Casella E, Ceulemans R (2002) Spatial distribution of leaf morphological and physiological characteristics in relation to local radiation regime within the canopies of 3-year-old Populus clones in coppice culture. Tree Physiol 22:1277–1288

    Article  CAS  PubMed  Google Scholar 

  • Caudullo G, de Rigo D (2016) Populus tremula in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz J, de Rigo D, Caudullo G, Houston Durrant T, Mauri A (eds) European atlas of forest tree species. Publication Office of the EU, Luxembourg, pp 138–139

    Google Scholar 

  • Chazdon RL, Kaufmann S (1993) Plasticity of leaf anatomy of two rain forest shrubs in relation to photosynthetic light acclimation. Funct Ecol 7:385–394

    Article  Google Scholar 

  • Coble AP, Cavaleri MA (2014) Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest. Tree Physiol 34:146–158

    Article  CAS  PubMed  Google Scholar 

  • Coble AP, Cavaleri MA (2015) Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment. Oecologia 177:1131–1143

    Article  PubMed  Google Scholar 

  • Couso LL, Fernández RJ (2012) Phenotypic plasticity as an index of drought tolerance in three Patagonian steppe grasses. Ann Bot 110:849–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Silveira TI, Boeger MRT, Maranho LT, de Melo JC, Soffiatti P (2015) Functional leaf traits of 57 woody species of the Araucaria Forest, Southern Brazil. Braz J Bot 38:357–366

    Article  Google Scholar 

  • Dietrich L, Hoch G, Kahmen A, Körner C (2018) Losing half the conductive area hardly impacts the water status of mature trees. Sci Rep 8:15006

    Article  PubMed  PubMed Central  Google Scholar 

  • Dow GJ, Berry JA, Bergmann DC (2014) The physiological importance of developmental mechanisms that enforce proper stomatal spacing in Arabidopsis thaliana. New Phytol 201:1205–1217

    Article  CAS  PubMed  Google Scholar 

  • Du Q, Liu T, Jiao X, Song X, Zhang J, Li J (2019) Leaf anatomical adaptations have central roles in photosynthetic acclimation to humidity. J Exp Bot 70:4949–4961

    Article  CAS  PubMed  Google Scholar 

  • Durand M, Brendel O, Buré C, Le Thiec D (2019) Altered stomatal dynamics induced by changes in irradiance and vapour-pressure deficit under drought: impacts on the whole-plant transpiration efficiency of poplar genotypes. New Phytol 222:1789–1802

    Article  CAS  PubMed  Google Scholar 

  • Eensalu E, Kupper P, Sellin A, Rahi M, Sõber A, Kull O (2008) Do stomata operate at the same relative opening range along a canopy profile of Betula pendula? Funct Plant Biol 35:103–110

    Article  PubMed  Google Scholar 

  • Fichot R, Chamaillard S, Depardieu C et al (2011) Hydraulic efficiency and coordination with xylem resistance to cavitation, leaf function, and growth performance among eight unrelated Populus deltoides × Populus nigra hybrids. J Exp Bot 62:2093–2106

    Article  CAS  PubMed  Google Scholar 

  • Flores-Moreno H, Fazayeli F, Banerjee A et al (2019) Robustness of trait connections across environmental gradients and growth forms. Glob Ecol Biogeogr 28:1806–1826

    Article  Google Scholar 

  • Franks PJ, Farquhar GD (2001) The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol 125:935–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franks PJ, Drake PL, Beerling DJ (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

    Article  PubMed  Google Scholar 

  • Gamage HK, Ashton MS, Singhakumara BMP (2003) Leaf structure of Syzygium spp. (Myrtaceae) in relation to site affinity within a tropical rain forest. Bot J Linn Soc 141:365–377

    Article  Google Scholar 

  • Hale SE, Edwards C (2002) Comparison of film and digital hemispherical photography across a wide range of canopy densities. Agric For Meteorol 112:51–56

  • Hanba YT, Kogami H, Terashima I (2002) The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant Cell Environ 25:1021–1030

    Article  Google Scholar 

  • Hansen EA (1991) Poplar woody biomass yields: a look to the future. Biomass Bioenergy 1:1–7

    Article  Google Scholar 

  • Harayama H, Kitao M, Agathokleous E, Ishida A (2019) Effects of major vein blockage and aquaporin inhibition on leaf hydraulics and stomatal conductance. Proc R Soc B 286:20190799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaagus J, Mändla K (2014) Climate change scenarios for Estonia based on climate models from the IPCC Fourth Assessment Report. Estonian J Earth Sci 63:166–180

    Article  Google Scholar 

  • Jacob D, Petersen J, Eggert B et al (2014) EURO-CORDEX: new high-resolution climate change projections for European impact research. Reg Environ Change 14:563–578

    Article  Google Scholar 

  • Jasińska AK, Alber M, Tullus A, Rahi M, Sellin A (2015) Impact of elevated atmospheric humidity on anatomical and hydraulic traits of xylem in hybrid aspen. Funct Plant Biol 42:565–578

    Article  Google Scholar 

  • Johansson T (2013) Biomass production of hybrid aspen growing on former farm land in Sweden. J For Res 24:237–246

  • Kangur O, Steppe K, Schreel J, von der Crone J, Sellin A (2021) Variation in nocturnal stomatal conductance and development of predawn disequilibrium between soil and leaf water potentials in nine temperate deciduous tree species. Funct Plant Biol 48:483–492

    Article  CAS  PubMed  Google Scholar 

  • Kolb KJ, Sperry JS (1999) Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata). Ecology 80:2373–2384

    Article  Google Scholar 

  • Kumagai T, Kuraji K, Noguchi H, Tanaka Y, Tanaka K, Suzuki M (2001) Vertical profiles of environmental factors within tropical rainforest, Lambir Hills National Park, Sarawak, Malaysia. J For Res 6:257–264

  • Kupper P, Sõber J, Sellin A et al (2011) An experimental facility for free air humidity manipulation (FAHM) can alter water flux through deciduous tree canopy. Environ Exp Bot 72:432–438

    Article  Google Scholar 

  • Kupper P, Ivanova H, Sõber A, Rohula-Okunev G, Sellin A (2018) Night and daytime water relations in five fast-growing tree species: Effects of environmental and endogenous variables. Ecohydrology 11:e1927

    Article  Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:87–261

    Google Scholar 

  • Lambers H, Chapin FS III, Pons TL (2006) Plant physiological ecology. Springer, New York

    Google Scholar 

  • Legner N, Fleck S, Leuschner C (2013) Low light acclimation in five temperate broad-leaved tree species of different successional status: the significance of a shade canopy. Ann For Sci 70:557–570

  • Lewis AM, Boose ER (1995) Estimating volume flow rates through xylem conduits. Am J Bot 82:1112–1116

    Article  Google Scholar 

  • Li L, McCormack ML, Ma C et al (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18:899–906

    Article  CAS  PubMed  Google Scholar 

  • Li F, McCulloh KA, Sun S, Bao W (2018) Linking leaf hydraulic properties, photosynthetic rates, and leaf lifespan in xerophytic species: a test of global hypotheses. Am J Bot 105:1858–1868

    Article  CAS  PubMed  Google Scholar 

  • Lihavainen J, Ahonen V, Keski-Saari S, Sõber A, Oksanen E, Keinänen M (2017) Low vapor pressure deficit reduces glandular trichome density and modifies the chemical composition of cuticular waxes in silver birch leaves. Tree Physiol 37:1166–1181

    Article  CAS  PubMed  Google Scholar 

  • Mandre M, Tullus H, Tamm Ü (1998) The partitioning of carbohydrates and the biomass of leaves in Populus tremula L. canopy. Trees 12:160–166

    Google Scholar 

  • Martínez-Vilalta J, Garcia-Forner N (2017) Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant Cell Environ 40:962–976

    Article  PubMed  Google 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. Am Nat 175:447–460

    Article  PubMed  Google Scholar 

  • Mediavilla S, Martín I, Escudero A (2020) Vein and stomatal traits in leaves of three co-occurring Quercus species differing in leaf life span. Eur J For Res 139:829–840

  • Messier J, McGill BJ, Enquist BJ, Lechowicz MJ (2017) Trait variation and integration across scales: is the leaf economic spectrum present at local scales? Ecography 40:685–697

    Article  Google Scholar 

  • Monclus R, Dreyer E, Villar M et al (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra. New Phytol 169:765–777

    Article  PubMed  Google Scholar 

  • Monsi M, Saeki T (2005) On the factor light in plant communities and its importance for matter production. Ann Bot 95:549–567

    Article  PubMed  PubMed Central  Google Scholar 

  • Nardini A, Pedá G, Salleo S (2012) Alternative methods for scaling leaf hydraulic conductance offer new insights into the structure–function relationships of sun and shade leaves. Funct Plant Biol 39:394–401

    Article  PubMed  Google Scholar 

  • Nardini A, Õunapuu-Pikas E, Savi T (2014) When smaller is better: leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes. Funct Plant Biol 41:972–982

    Article  PubMed  Google Scholar 

  • Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469

    Article  Google Scholar 

  • Niinemets Ü, Kull O, Tenhunen JD (1999) Variability in leaf morphology and chemical composition as a function of canopy light environment in coexisting deciduous trees. Int J Plant Sci 160:837–848

    Article  CAS  PubMed  Google Scholar 

  • Niinemets Ü, Ellsworth DS, Lukjanova A, Tobias M (2001) Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. Tree Physiol 21:1231–1244

    Article  CAS  PubMed  Google Scholar 

  • Niinemets Ü, Keenan TF, Hallik L (2015) A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol 205:973–993

    Article  CAS  PubMed  Google Scholar 

  • Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant Cell Environ 28:916–927

    Article  Google Scholar 

  • Õunapuu E, Sellin A (2013) Daily dynamics of leaf and soil-to-branch hydraulic conductance in silver birch (Betula pendula) measured in situ. Plant Physiol Biochem 68:104–110

    Article  PubMed  Google Scholar 

  • Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

    Article  PubMed  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50

    Article  CAS  PubMed  Google Scholar 

  • Proietti P, Palliotti A, Famiani F et al (2000) Influence of leaf position, fruit and light availability on photosynthesis of two chestnut genotypes. Sci Hortic 85:63–73

    Article  CAS  Google Scholar 

  • Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, Oxford

    Google Scholar 

  • Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87:483–491

    Article  PubMed  Google Scholar 

  • Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26:1343–1356

    Article  Google Scholar 

  • Sack L, Melcher PJ, Liu WH, Middleton E, Pardee T (2006) How strong is intracanopy leaf plasticity in temperate deciduous trees? Am J Bot 93:829–839

    Article  PubMed  Google Scholar 

  • Sack L, Scoffoni C, John GP et al (2013) How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. J Exp Bot 64:4053–4080

    Article  CAS  PubMed  Google Scholar 

  • Sack L, Scoffoni C, Johnson DM, Buckley TN, Brodribb TJ (2015) The anatomical determinants of leaf hydraulic function. In: Hacke U (ed) Functional and ecological xylem anatomy. Springer, Heidelberg, pp 255–271

    Chapter  Google Scholar 

  • 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 Physiol 156:832–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott P (2008) Physiology and behaviour of plants. Wiley, Chichester

    Google Scholar 

  • Sellin A, Kupper P (2005) Effects of light availability versus hydraulic constraints on stomatal responses within a crown of silver birch. Oecologia 142:388–397

    Article  PubMed  Google Scholar 

  • Sellin A, Kupper P (2006) Spatial variation in sapwood area to leaf area ratio and specific leaf area within a crown of silver birch. Trees 20:311–319

    Article  Google Scholar 

  • Sellin A, Kupper P (2007) Effects of enhanced hydraulic supply for foliage on stomatal responses in little-leaf linden (Tilia cordata Mill.). Eur J For Res 126:241–251

  • Sellin A, Õunapuu E, Kaurilind E, Alber M (2012) Size-dependent variability of leaf and shoot hydraulic conductance in silver birch. Trees 26:821–831

    Article  Google Scholar 

  • Sellin A, Tullus A, Niglas A, Õunapuu E, Karusion A, Lõhmus K (2013) Humidity-driven changes in growth rate, photosynthetic capacity, hydraulic properties and other functional traits in silver birch (Betula pendula). Ecol Res 28:523–535

    Article  CAS  Google Scholar 

  • Sellin A, Alber M, Kupper P (2017) Increasing air humidity influences hydraulic efficiency but not functional vulnerability of xylem in hybrid aspen. J Plant Physiol 219:28–36

    Article  CAS  PubMed  Google Scholar 

  • Sellin A, Taneda H, Alber M (2019) Leaf structural and hydraulic adjustment with respect to air humidity and canopy position in silver birch (Betula pendula). J Plant Res 132:369–381

    Article  CAS  PubMed  Google Scholar 

  • Smith EA, Collette SB, Boynton TA et al (2011) Developmental contributions to phenotypic variation in functional leaf traits within quaking aspen clones. Tree Physiol 31:68–77

    Article  PubMed  Google Scholar 

  • Tullus A, Rytter L, Tullus T, Weih M, Tullus H (2012) Short-rotation forestry with hybrid aspen (Populus tremula L. × P. tremuloides Michx.) in Northern Europe. Scand J For Res 27:10–29

  • Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360

  • Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Xiong D, Flexas J, Yu T, Peng S, Huang J (2017) Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytol 213:572–583

    Article  CAS  PubMed  Google Scholar 

  • Yin Q, Wang L, Lei M et al (2018) The relationships between leaf economics and hydraulic traits of woody plants depend on water availability. Sci Total Environ 621:245–252

    Article  CAS  PubMed  Google Scholar 

  • Zhang R, Li Y, Ni Y, Gui X, Lian J, Ye W (2019) Intraspecific variation of leaf functional traits along the vertical layer in a subtropical evergreen broad-leaved forest of Dinghushan. Biodiv Sci 27:1279–1290

    Article  Google Scholar 

  • Zhang L, Liu L, Zhao H, Jiang Z, Cai J (2020) Differences in near isohydric and anisohydric behavior of contrasting poplar hybrids (I-101 (Populus alba L.) × 84K (Populus alba L. × Populus glandulosa Uyeki)) under drought-rehydration treatments. Forests 11:402

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Jaak Sõber for operating the FAHM humidification system, Ingmar Tulva for providing data on the radiation regime, and Märt Rahi for assisting in electron microscopy.

Funding

This study was supported by a grant from the Estonian Research Council (institutional research project IUT34-9).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arne Sellin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 681 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sellin, A., Alber, M., Jasińska, A.K. et al. Adjustment of leaf anatomical and hydraulic traits across vertical canopy profiles of young broadleaved forest stands. Trees 36, 67–80 (2022). https://doi.org/10.1007/s00468-021-02181-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-021-02181-0

Keywords

Navigation