Skip to main content
Log in

How timing of stem girdling affects needle xylem structure in Scots pine

  • Original Paper
  • Published:
European Journal of Forest Research Aims and scope Submit manuscript

Abstract

While needles represent a proportionally large fraction of whole-plant hydraulic resistance, no studies to date have investigated how source–sink disturbances affect needle xylem structure. In this study, we evaluated structural changes in xylem in current-year needles of Scots pine 227 and 411 days after stem girdling (hereafter referred to as DAG). Maximum and minimum tracheid lumen diameters and therefore also the size of tracheid lumen areas increased in needles 227 DAG compared to control needles. In contrast, tracheid dimensions were similar in needles 411 DAG as in the control needles, but smaller xylem area and lower number of tracheids resulted in the lower theoretical needle hydraulic conductivity of those needles. Several needle xylem parameters were intercorrelated in both control and girdled trees. These observed changes provide a new understanding of the processes that occur following a source–sink disturbance. Considering anatomical parameters such as the number of tracheids, tracheid dimension, or needle xylem area, which are rarely described in physiological studies, could be helpful, for example, in understanding to tree hydraulic systems or for modeling gas exchange. Finally, empirical equations were developed to calculate needle theoretical hydraulic conductivity and the number of tracheids in needles using an easily measurable parameter of needle xylem area.

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

Similar content being viewed by others

References

  • Aulen G (1991) Increasing insect abundance by killing deciduous trees: a method of improving the food situation for endangered woodpeckers. Holarct Ecol 14:68–80

    Google Scholar 

  • Baldwin HI (1934) Some physiological effects of girdling northern hardwoods. Bull Torrey Bot Club 61:249–257

    Article  Google Scholar 

  • Bongard-Pierce DK, Evans MMS, Poethig RS (1996) Heteroblastic features of leaf anatomy in maize and their genetic regulation. Int J Plant Sci 157:331–340

    Article  Google Scholar 

  • Čermák J, Deml M, Penka M (1973) A new method of sap flow rate determination in trees. Biol Plant 15:171–178

    Article  Google Scholar 

  • Cernusak LA, Marshall JD (2001) Responses of foliar δ13C, gas exchange and leaf morphology to reduced hydraulic conductivity in Pinus monticola branches. Tree Physiol 21:1215–1222

    Article  PubMed  CAS  Google Scholar 

  • Charra-Vaskou K, Mayr S (2011) The hydraulic conductivity of the xylem in conifer needles (Picea abies and Pinus mugo). J Exp Bot 62:4383–4390

    Article  PubMed  CAS  Google Scholar 

  • Charra-Vaskou K, Badel E, Burlett R, Cochard H, Delzon S, Mayr S (2012) Hydraulic efficiency and safety of vascular and non-vascular components in Pinus pinaster leaves. Tree Physiol 32:1161–1170

    Article  PubMed  CAS  Google Scholar 

  • Cochard H, Froux F, Mayr S, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cruiziat P, Cochard H, Améglio T (2002) Hydraulic architecture of trees: main concepts and results. Ann For Sci 59:723–725

    Article  Google Scholar 

  • Dale JE (1988) The control of leaf expansion. Annu Rev Plant Physiol Plant Mol Biol 39:267–295

    Article  Google Scholar 

  • De Schepper V, Steppe K (2011) Tree girdling responses simulated by a water and carbon transport model. Ann Bot-Lond 108:1147–1154

    Article  CAS  Google Scholar 

  • Domec JC, Pruyn ML (2008) Bole girdling affects metabolic properties and root, trunk and branch hydraulics of young ponderosa pine trees. Tree Physiol 28:1493–1504

    Article  PubMed  Google Scholar 

  • Ewers BE, Oren R, Kim H et al (2007) Effects of hydraulic architecture and spatial variation in light on mean stomatal conductance of tree branches. Plant Cell Environ 30:483–496

    Article  PubMed  CAS  Google Scholar 

  • Fajstavr M, Vavrcik H, Gryc V, Giagli K, Urban J (2017) Stem girdling stress effect on Scots pine: above and below girdled area cell differentiation process. Silva Fennica (accepted)

  • Froux F, Huc R, Ducrey M, Dreyer E (2002) Xylem hydraulic efficiency versus vulnerability in seedlings of four contrasting Mediterranean tree species (Cedrus atlantica, Cupressus sempervirens, Pinus halepensis and Pinus nigra). Ann For Sci 59:409–418

    Article  Google Scholar 

  • Gebauer R, Čermák J, Plichta R, Špinlerová Z, Urban J, Volařík D, Ceulemans R (2015) Within canopy variation in needle morphology and anatomy of vascular tissues in a sparse Scots pine forest. Trees-Struct Funct 29:1447–1457

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pittermann J (2005) Efficiency versus safety tradeoffs for water conduction in angiosperm vessels versus gymnosperm tracheids. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier Academic Press, New York, pp 333–354

    Chapter  Google Scholar 

  • Hartmann H, Ziegler W, Kolle O, Trumbore S (2013a) Thirst beats hunger—declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200:340–349

    Article  PubMed  CAS  Google Scholar 

  • Hartmann H, Ziegler W, Trumbore S (2013b) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427

    Article  Google Scholar 

  • Kawade K, Horiguchi G, Usami T, Hirai MY, Tsukaya H (2013) ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Curr Biol 23:788–792

    Article  PubMed  CAS  Google Scholar 

  • Kučera J, Čermák J, Penka M (1977) Improved thermal method of continual recording the transpiration flow rate dynamics. Biol Plant 19:413–420

    Article  Google Scholar 

  • Kučera J, Brito P, Jiménez MS, Urban J (2017) Direct Penman–Monteith parameterization for estimating stomatal conductance and modeling sap flow. Trees 31:873–885

    Article  Google Scholar 

  • López R, Brossa R, Gil L, Pita P (2015) Stem girdling evidences a trade-off between cambial activity and sprouting and dramatically reduces plant transpiration due to feedback inhibition of photosynthesis and hormone signaling. Front Plant Sci 6:285

    Article  PubMed  PubMed Central  Google Scholar 

  • Martre P, Durand JL, Cochard H (2000) Changes in axial hydraulic conductivity along elongating leaf blades in relation to xylem maturation in tall feste. New Phytol 146:235–247

    Article  Google Scholar 

  • Maunoury-Danger F, Fresneau C, Eglin T, Berveiller D, François C, Lelarge-Trouverie C, Damesin C (2010) Impact of carbohydrate supply on stem growth, wood and respired CO2 δ13C: assessment by experimental girdling. Tree Physiol 30:818–830

    Article  PubMed  CAS  Google Scholar 

  • McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meinzer FC, Andrade JL, Goldstein G et al (1997) Control of transpiration from the upper canopy of a tropical forest: the role of stomatal, boundary layer and hydraulic architecture components. Plant Cell Environ 20:1242–1252

    Article  Google Scholar 

  • Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Phys 35:299–319

    Article  Google Scholar 

  • Murakami PF, Schaberg PG, Shane JB (2008) Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiol 28:1467–1473

    Article  PubMed  CAS  Google Scholar 

  • Myers DA, Thomas RB, DeLucia EH (1999) Photosynthetic responses of loblolly pine (Pinus taeda) needles to experimental reduction in sink demand. Tree Physiol 19:235–242

    Article  PubMed  Google Scholar 

  • Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees-Struct Funct 15:14–24

    Article  Google Scholar 

  • Nardini A, Salleo S, Andri S (2005) Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus L. cv Margot). Plant Cell Environ 28:750–759

    Article  CAS  Google Scholar 

  • Negreros-Castillo P, Hall RB (1994) Four methods for partial over story removal in tropical forests in Mexico. J Environ Manag 41:237–243

    Article  Google Scholar 

  • Neirynck J, Janssens IA, Roskams P, Quataert P, Verschelde P, Ceulemans R (2008) Nitrogen biogeochemistry of a mature Scots pine forest subjected to high nitrogen loads. Biogeochemistry 91:201–222

    Article  CAS  Google Scholar 

  • Pariona W, Fredericksen TS, Licona JC (2003) Tree girdling treatments for timber stand improvement in Bolivian tropical forests. J Trop For Sci 15:583–592

    Google Scholar 

  • Phillips N, Oren R (1998) A comparison of daily representations of canopy conductance based on two conditional time-averaging methods and the dependence of daily conductance on environmental factors. Ann Sci For 55:217–235

    Article  Google Scholar 

  • Poorter H, Berkel YJV (2010) Soluble and insoluble sugars - extractions and chemical determinations. http://prometheuswiki.org/tiki-index.php?page=Soluble+and+insoluble+sugars+-+extractions+and+chemical. Accessed 10 Oct 2017

  • Poyatos R, Martínez-Vilalta J, Čermák J, Ceulemans R, Granier A, Irvine J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N et al (2007) Plasticity in hydraulic architecture of Scots pine across Eurasia. Oecologia 153:245–259

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rawlinson H, Dickinson N, Nolan P, Putwain P (2004) Woodland establishment on closed old-style landfill sites in N.W. England. For Ecol Manag 202:265–280

    Article  Google Scholar 

  • Rivas F, Gravina A, Agusti M (2007) Girdling effects on fruit set and quantum yield efficiency of PSII in two Citrus cultivars. Tree Physiol 27:527–535

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sellin A, Niglas A, Õunapuu E, Karusion A (2013) Impact of phloem girdling on leaf gas exchange and hydraulic conductance in hybrid aspen. Biol Plant 57:531–539

    Article  CAS  Google Scholar 

  • Setter TL, Brun WA, Brenner ML (1980) Effect of obstructed translocation of leaf abscisic acid on associated stomatal closure and photosynthesis decline. Plant Physiol 65:1111–1115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500

    Article  PubMed  Google Scholar 

  • Taylor A, Cooper P (2002) The effect of stem girdling on wood quality. Wood Fiber Sci 34:212–220

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Urban L, Alphonsout L (2007) Girdling decreases photosynthetic electron fluxes and induces sustained photoprotection in mango leaves. Tree Physiol 27:345–352

    Article  PubMed  CAS  Google Scholar 

  • Weaver RJ, McCune SB (1959) Girdling: its relation to carbohydrate nutrition and development of Thompson Seedless, Red Malaga and Ribier grapes. Hilgardia 28:421–456

    Article  CAS  Google Scholar 

  • Williams LE, Retzlaff WA, Yang WG, Biscay PJ, Ebisuda N (2000) Effect of girdling on leaf gas exchange, water status, and non-structural carbohydrates of field-grown Vitis vinifera L. (cv. Flame Seedless). Am J Enol Vitic 51:49–54

    CAS  Google Scholar 

  • Wilson BF, Gartner BL (2002) Effects of phloem girdling in conifers on apical control of branches, growth allocation and air in wood. Tree Physiol 22:347–353

    Article  PubMed  Google Scholar 

  • Yan CF, Han SJ, Zhou YM, Wang CG, Dai GH, Xiao WF, Li MH (2012) Needle-age related variability in nitrogen, mobile carbohydrates, and δ 13C within Pinus koraiensis tree crown. PLoS ONE 7:e35076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang SD, Tyree MT (1994) Hydraulic architecture of Acer saccharum and A. rubrum: comparison of branches to whole trees and the contribution of leaves to hydraulic resistance. J Exp Bot 45:179–186

    Article  Google Scholar 

  • Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J et al (2011) Genome wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2:467

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

This work was funded by Czech project MSMT COST LD 13017 under the framework of the COST Action FP1106 network STReESS, Mendel University (Grant IGA 73/2013) and by the project “Indicators of Tree Vitality” (Reg. No. CZ.1.07/2.3.00/20.0265) co-financed by the European Social Fund and the Czech Republic. The authors declare no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roman Gebauer.

Additional information

Communicated by Judy Simon.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10342_2017_1090_MOESM1_ESM.tif

Figure S1. Soil water potential measured by gypsum blocks at three depths (15 cm, 50 cm, and 90 cm) during vegetation season 2014. Data were recorded up to − 1.1 MPa which was the lowest limit of the instrument used (TIFF 282 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gebauer, R., Plichta, R., Bednářová, E. et al. How timing of stem girdling affects needle xylem structure in Scots pine. Eur J Forest Res 137, 57–67 (2018). https://doi.org/10.1007/s10342-017-1090-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10342-017-1090-z

Keywords

Navigation