Abstract
Vessel grouping in angiosperms may improve hydraulic integration and increase the spread of cavitations through redundancy pathways. Although disputed, it is increasingly attracting research interest as a potentially significant hydraulic trait. However, the variation of vessel grouping in a tree is poorly understood. I measured the number of solitary and grouped vessels in the xylem of Betula platyphylla Roth. from the pith to the bark along the water flow path. The vessel grouping parameters included the mean number of vessels per vessel group (VG), percentage of solitary vessels (SVP), percentage of radial multiple vessels (MVP), and percentage of cluster vessels (CVP). The effects of cambial age (CA) and flow path-length (PL) on the vessel grouping were analyzed using a linear mixed model.VG and CVP increased nonlinearly, SVP decreased nonlinearly with PL. In trunks and branches, VG and CVP decreased nonlinearly, and SVP increased nonlinearly with CA. In roots, the parameters had no change with CA. MVP was almost constant with PL or CA. The results suggest that vessel grouping has a nonrandom variation pattern, which is affected deeply by cambial age and water flow path.
Similar content being viewed by others
References
Aloni R (2001) Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J Plant Growth Regul 20:22–34
Aloni R (2013) The role of hormones in controlling vascular differentiation. Cellular Aspects of Wood Formation. Springer, New York, pp 99–139
Aloni R (2015) Ecophysiological implications of vascular differentiation and plant evolution. Trees 29:1–16
Baas P (1982) Systematic, phylogenetic, and ecological wood anatomy-history and perspectives. New perspectives in wood anatomy. Springer, The Hague, pp 23–58
Baas P, Carlquist S (1985) A comparison of the ecological wood anatomy of the floras of southern California and Israel. IAWAJ 6:349–354
Carlquist S (1966) Wood anatomy of Compositae: a summary, with comments on factors controlling wood evolution. Aliso 6:25–44
Carlquist S (1984) Vessel grouping in dicotyledon wood: significance and relationship to imperforate tracheary elements. Aliso 10:505–525
Carlquist S, Eckhart VM, Michener DC (1983) Wood anatomy of hydrophyllaceae. I. Eriodictyon. Aliso 10:397–412
Carrer M, von Arx G, Castagneri D, Petit G (2015) Distilling allometric and environmental information from time series of conduit size: the standardization issue and its relationship to tree hydraulic architecture. Tree Physiol 35:27–33
Christman MA, Sperry JS (2010) Single-vessel flow measurements indicate scalariform perforation plates confer higher flow resistance than previously estimated. Plant Cell Environ 33:431–443
De Micco V, Aronne G, Baas P (2008) Wood anatomy and hydraulic architecture of stems and twigs of some Mediterranean trees and shrubs along a mesic-xeric gradient. Trees 22:643–655
Domec J-C, Warren JM, Meinzer FC, Lachenbruch B (2009) Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA J 30:101–120
Ewers FW, Ewers JM, Jacobsen AL, Lopez-Portillo J (2007) Vessel redundancy: modeling safety in numbers. IAWA J 28:373–388
Fan ZX, Cao KF, Becker P (2009) Axial and radial variations in xylem anatomy of angiosperm and conifer trees in Yunnan, China. IAWA J 30:1–13
Fromm J (2013) Xylem development in trees: from cambial divisions to mature wood cells. Cellular aspects of wood formation, vol 20. Springer, Berlin Heidelberg, pp 3–39
Gartner BL (1995) Hydraulic and mechanical consequences. Academic Press, San Diego
Gasson P (1987) Interpretation and choice of vessel characters in the IAWA standard list. IAWA J 8:233–235
Goldstein H (2011) Multilevel statistical models. John Wiley & Sons, Chichester
Gupta MC, Iqbal M (2005) Ontogenetic histological changes in the wood of mango (Mangifera indica L. cv Deshi) exposed to coal-smoke pollution. Environ Exp Bot 54:248–255
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701
Helińska-Raczkowska L (1994) Variation of vessel lumen diameter in radial direction as an indication of the juvenile wood growth in oak (Quercus petraea Liebl). Ann For Sci 51:283–290
Hölttä T, Cochard H, Nikinmaa E, Mencuccini M (2009) Capacitive effect of cavitation in xylem conduits: results from a dynamic model. Plant, Cell Environ 32:10–21
Jacobsen AL, Pratt RB, Ewers FW, Davis SD (2007) Cavitation resistance among 26 chaparral species of southern California. Ecol Monogr 77:99–115
Jansen S, Gortan E, Lens F, Lo Gullo MA, Salleo S, Scholz A, Stein A, Trifilò P, Nardini A (2011) Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? New Phytol 189:218–228
Jasinska A, 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
Leal S, Sousa VB, Pereira H (2007) Radial variation of vessel size and distribution in cork oak wood (Quercus suber L.). Wood Sci Technol 41:339–350
Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723
Lintunen A, Kalliokoski T (2010) The effect of tree architecture on conduit diameter and frequency from small distal roots to branch tips in Betula pendula, Picea abies and Pinus sylvestris. Tree Physiol 30:1433–1447
Loepfe L, Martinez-Vilalta J, Pinol J, Mencuccini M (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. J Theor Biol 247:788–803
Mencuccini M, Martinez-Vilalta J, Piñol J, Loepfe L, Burnat M, Alvarez X, Camacho J, Gil D (2010) A quantitative and statistically robust method for the determination of xylem conduit spatial distribution. Am J Bot 97:1247–1259
Olson ME, Anfodillo T, Rosell JA, Petit G, Crivellaro A, Isnard S, León-Gómez C, Alvarado-Cárdenas LO, Castorena M (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates. Ecol Lett 17:988–997
Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant physiol 127:1513–1523
Psaras GK, Sofroniou I (2004) Stem and root wood anatomy of the shrub Phlomis fruticosa (Labiatae). IAWA J 25:71–78
Rathgeber C, Rossi S, Bontemps J (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot-london 108:429–438
Robert EMR, Koedam N, Beeckman H, Schmitz N (2009) A safe hydraulic architecture as wood anatomical explanation for the difference in distribution of the mangroves Avicennia and Rhizophora. Funct Ecol 23:649–657
Rood SB, Patiño S, Coombs K, Tyree MT (2000) Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods. Trees 14:248–257
Rosell JA, Olson ME, Aguirre-HerNández R, Carlquist S (2007) Logistic regression in comparative wood anatomy: tracheid types, wood anatomical terminology, and new inferences from the Carlquist and Hoekman southern Californian data set. Bot J Linn Soc 154:331–351
Rossi S, Deslauriers A, Anfodillo T, Carrer M (2008) Age-dependent xylogenesis in timberline conifers. New Phytol 177:199–208
Schuldt B, Leuschner C, Brock N, Horna V (2013) Changes in wood density, wood anatomy and hydraulic properties of the xylem along the root-to-shoot flow path in tropical rainforest trees. Tree Physiol 33:161–174
Sorce C, Giovannelli A, Sebastiani L, Anfodillo T (2013) Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees. Plant Cell Rep 32:1–14
Sperry JS, Saliendra NZ (1994) Intra- and inter- plant variation in xylem cavitation in Betula occidentalis. Plant, Cell Environ 17:1233–1241
Spicer R, Gartner BL (2001) The effects of cambial age and position within the stem on specific conductivity in Douglas-fir (Pseudotsuga menziesii) sapwood. Trees 15:222–229
Trifilò P, Barbera PM, Raimondo F, Nardini A, Gullo MAL (2014) Coping with drought-induced xylem cavitation: coordination of embolism repair and ionic effects in three Mediterranean evergreens. Tree Physiol 34:109–122
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Biol 40:19–36
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer Verlag, Berlin
von Arx G, Kueffer C, Fonti P (2013) Quantifying plasticity in vessel grouping-added value from the image analysis tool RoXAS. IAWA J 34:433–445
Yu HP, Liu YX, Zhi CY, Liu ZB (2008) Measurement of wood microstructural parameters on transverse section by binary morphology. Mater Sci Tech 16:107–111
Zach A, Schuldt B, Brix S, Horna V, Culmsee H, Leuschner C (2010) Vessel diameter and xylem hydraulic conductivity increase with tree height in tropical rainforest trees in Sulawesi, Indonesia. Flora 205:506–512
Zhao X (2015) Effects of cambial age and flow path-length on vessel characteristics in birch. J Forest Res-Jph 20:175–185
Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291:1059–1062
Acknowledgments
The author thanks Professor. C.K. Wang and his colleagues from the Maoershan Forest Ecosystem Research Station for Granting permission to collect the tree samples, and is grateful to students of Henan University of Science and Technology for their processing the samples. The financial support of the Natural Science Foundation of China (31000265, 41401063) is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhao, X. Spatial variation of vessel grouping in the xylem of Betula platyphylla Roth. J Plant Res 129, 29–37 (2016). https://doi.org/10.1007/s10265-015-0768-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-015-0768-x