Patterns in hydraulic architecture from roots to branches in six tropical tree species from cacao agroforestry and their relation to wood density and stem growth

Frontiers in Plant Science

Volumn 6, Issue MAR, 2015, Pages 1-16

  Kotowska, Martyna M ^a   Hertel, Dietrich ^a   Rajab, Yasmin Abou ^a   Barus, Henry ^b   Schuldt, Bernhard ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b Tadulaku University   (Indonesia)

Author keywords

Aboveground productivity; Foliar nitrogen; Hydraulic conductivity; Perhumid climate; References; Shade tree; Vessel diameter; Wood density

Indexed keywords

THEOBROMA CACAO;

EID: 84928045650     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00191     Document Type: Article

References (99)

1. Achard, F., Eva, H. D., Stibig, H. J., Mayaux, P., Gallego, J., Richards, T., et al. (2002). Determination of deforestation rates of the world's humid tropical forests. Science 297, 999-1002. doi: 10.1126/science.1070656
2. Aloni, R. (1987). Differentiation of Vascular Tissues. Annu. Rev. Plant Physiol. PlantMol. Biol. 38, 179-204. doi: 10.1146/annurev.arplant.38.1.179
3. Anfodillo, T., Carraro, V., Carrer, M., Fior, C., and Rossi, S. (2006). Convergent tapering of xylem conduits in different woody species. New Phytol. 169, 279290. doi: 10.1111/j.1469-8137.2005.01587
4. Anfodillo, T., Petit, G., and Crivellaro, A. (2013). Axial conduit widening in woody species: a still neglected anatomical pattern. IAWA J. 34, 352-364. doi: 10.1163/22941932-00000030
5. Awad, H., Barigah, T., Badel, E., Cochard, H., and Herbette, S. (2010). Poplar vul- nerabilityto xylem cavitation acclimates to drier soil conditions. Physiol. Plant. 139,280-288. doi: 10.1111/j.1399-3054.2010.01367
6. Baas, P. (1982). Systematic, phylogenetic and ecological wood anatomy-history and perspectives. Acta Bot. Neerl. 31, 501-501.
7. Brodersen, C. R., McElrone, A. J., Choat, B., Matthews, M. A., and Shackel, K. A. (2010). The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol. 154, 1088-1095. doi: 10.1104/pp.110.162396
8. Brodribb, T. J., Holbrook, N. M., and Gutierrez, M. V. (2002). Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees. Plant Cell Environ. 25, 1435-1444. doi: 10.1046/j.1365-3040.2002.00919
9. Brown, S. (1997). Estimating Biomass and Biomass Change of Tropical Forests: A Primer. Rome: FAO.
10. Bucci, S. J., Goldstein, G., Meinzer, F. C., Scholz, F. G., Franco, A. C., and Bustamante, M. (2004). Functional convergence in hydraulic architecture and water relations of tropical savanna trees: from leaf to whole plant. Tree Physiol. 24, 891-899. doi: 10.1093/treephys/24.8.891
11. Burnham, K. P., and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A PracticalInformation-TheoreticApproach. New York, NY: Springer.
12. Cai, J., Hacke, U., Zhang, S., and Tyree, M. T. (2010). What happens when stems are embolized in a centrifuge? Testing the cavitron theory. Physiol. Plant. 140, 311-320. doi: 10.1111/j.1399-3054.2010.01402
13. Carlquist, S. (1994). Wood and bark anatomy of Gnetum gnemon L. Bot. J. Linn. Soc. 116,203-221. doi: 10.1006/bojl.1994.1060
14. Carr, M. K. V., and Lockwood, G. (2011). The water relations and irrigation requirements of cocoa (Theobroma cacao L.). Rev. Exp. Agric. 47, 653-676. doi: 10.1017/s0014479711000421
15. Chave, J., Andalo, C., Brown, S., Cairns, M. A., Chambers, J. Q., Eamus, D., et al. (2005). Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia 145, 87-99. doi: 10.1007/s00442-005-0100
16. Chenlemuge, T., Hertel, D., Dulamsuren, C., Khishigjargal, M., Leuschner, C., and Hauck, M. (2013). Extremely low fine root biomass in Larix sibirica forests at the southern drought limit of the boreal forest. Flora 208, 488-496. doi: 10.1016/j.flora.2013.08.002
17. Chiba, Y. (1998). Architectural analysis of relationship between biomass and basal area based on pipe model theory. Ecol. Modell. 108, 219-225. doi: 10.1016/s0304-3800(98)00030-1
18. Chitarra, W., Balestrini, R., Vitali, M., Pagliarani, C., Perrone, I., Schubert, A., et al. (2014). Gene expression in vessel-associated cells upon xylem embolism repair in Vitis vinifera L. Planta 239,887-899. doi: 10.1007/s00425-013-2017-7
19. Choat, B., Cobb, A. R., and Jansen, S. (2008). Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol. 177, 608-625. doi: 10.1111/j.1469-8137.2007.02317.x
20. da Silva, E. C., Silva, M. F. A., Nogueira, R. J. M. C., and Albuquerque, M. B. (2010). Growth evaluation and water relations of Erythrina velutina seedlings in response to drought stress. Braz. J. Plant Physiol. 22, 225-233. doi: 10.1590/S1677-04202010000400002
21. Domec, J.-C., Schaefer, K., Oren, R., Kim, H. S., and McCarthy, H. R. (2010). Variable conductivity and embolism in roots and branches of four contrasting tree species and their impacts on whole-plant hydraulic performance under future atmospheric CO2 concentration. Tree Physiol. 30, 1001-1015. doi: 10.1093/treephys/tpq054
22. Domec, J.-C., Warren, J. M., Meinzer, F. C., and 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. doi: 10.1163/22941932-90000207
23. Enquist, B. J., West, G. B., Charnov, E. L., and Brown, J. H. (1999). Allometric scaling of production and life-history variation in vascular plants. Nature 401, 907-911. doi: 10.1038/44819
24. Espino, S., and Schenk, H. J. (2011). Mind the bubbles: achieving stable measurements of maximum hydraulic conductivity through woody plant samples. J. Exp. Bot. 62, 1119-1132. doi: 10.1093/jxb/erq338
25. Fagbola, O., Osonubi, O., Mulongoy, K., and Odunfa, S. A. (2001). Effects of drought stress and arbuscular mycorrhiza on the growth of Gliricidia sepium (Jacq). Walp, and Leucaena leucocephala (Lam.) de Wit. in simulated eroded soil conditions. Mycorrhiza 11, 215-223. doi: 10.1007/s005720100114
26. Fan, Z.-X., Zhang, S.-B., Hao, G.-Y., Slik, J. W. F., and Cao, K.-F. (2012). Hydraulic conductivity traits predict growth rates and adult stature of 40 Asian tropical tree species better than wood density. J. Ecol. 100,732-741. doi: 10.1111/j.1365-2745.2011.01939
27. FAO, and JRC. (2012). “Global forest land-use change 1990-2005" in FAO Forestry Paper No. 169, eds E. J. Lindquist, R. D'annunzio, A. Gerrand, K. Macdicken, F. Achard, R. Beuchle et al. (Rome: Food and Agriculture Organization of the United Nations and European CommissionJoint Research Centre).
28. Fisher, J. B., and Ewers, F. W. (1995). Vessel dimensions in liana and tree species of vessel dimensions Gnetum (Gnetales). Am. J. Bot. 82, 1350-1357. doi: 10.2307/2445861
29. Fortunel, C., Ruelle, J., Beauchene, J., Fine, P. V.A., and Baraloto, C. (2013). Wood specific gravity and anatomy of branches and roots in 113 Amazonian rainforest tree species across environmental gradients. New Phytol. 202, 79-94. doi: 10.1111/nph.12632
30. Gaul, D., Hertel, D., Borken, W., Matzner, E., and Leuschner, C. (2008). Effects of experimental drought on the fine root system of mature Norway spruce. For. Ecol. Manage. 256, 1151-1159. doi: 10.1016/j.foreco.2008.06.016
31. Gleason, S. M., Butler, D. W., and Waryszak, P. (2013). Shifts in leaf and stem hydraulic traits across aridity gradients in Eastern Australia. Int. J. Plant Sci. 174, 1292-1301. doi: 10.1086/673239
32. Gleason, S. M., Butler, D. W., Zieminska, K., Waryszak, P., and Westoby, M. (2012). Stem xylem conductivity is key to plant water balance across Australian angiosperm species. Funct. Ecol. 26, 343-352. doi: 10.1111/j.1365-2435.2012.01962
33. Goncalves, B., Correia, C. M., Silva, A. P., Bacelar, E. A., Santos, A., Ferreira, H., et al. (2007). Variation in xylem structure and function in roots and stems of scion-rootstock combinations of sweet cherry tree (Prunus avium L.). Trees 21, 121-130. doi: 10.1007/s00468-006-0102-2
34. Gonzalez-Benecke, C. A., Martin, T. A., and Peter, G. F. (2010). Hydraulic architecture and tracheid allometry in mature Pinuspalustris and Pinus elliottii trees. TreePhysiol. 30,361-375.doi: 10.1093/treephys/tpp129
35. Hajek, P., Leuschner, C., Hertel, D., Delzon, S., and Schuldt, B. (2014). Trade-offs between xylem hydraulic properties, wood anatomy and yield in Populus. Tree Physiol. 34, 744-756. doi: 10.1093/treephys/tpu048
36. Hansen, M. C., Stehman, S. V., Potapov, P. V., Loveland, T. R., Townshend, J. R. G., Defries, R. S., et al. (2008). Humid tropical forest clearing from 2000 to 2005 quantified by using multitemporal and multiresolution remotely sensed data. Proc. Natl. Acad. Sci. U.S.A. 105, 9439-9444. doi: 10.1073/pnas.0804042105
37. Herberich, E., Sikorski, J., and Hothorn, T. (2010).Arobust procedure for comparing multiple means under heteroscedasticity in unbalanced designs. PLoS ONE 5:e9788. doi: 10.1371/journal.pone.0009788
38. Hertel, D., Moser, G., Culmsee, H., Erasmi, S., Horna, V., Schuldt, B., et al. (2009). Below-and above-ground biomass and net primary productionin a paleotropical natural forest (Sulawesi, Indonesia) as compared to neotropical forests. For. Ecol. Manage. 258, 1904-1912. doi: 10.1016/j.foreco.2009.07.019
39. Hertel, D., Strecker, T., Muller-Haubold, H., and Leuschner, C. (2013). Fine root biomass and dynamics in beech forests across a precipitation gradient-is optimal resource partitioning theory applicable to water-limited mature trees? J. Ecol. 101, 1183-1200. doi: 10.1111/1365-2745.12124
40. Hietz, P., Valencia, R., and Joseph Wright, S. (2013).Strongradialvariation in wood densityfollows a uniform pattern in two neotropical rain forests. Funct. Ecol. 27, 684-692. doi: 10.1111/1365-2435.12085
41. Hoeber, S., Leuschner, C., Kohler, L., Arias-Aguilar, D., and Schuldt, B. (2014). The importance of hydraulic conductivity and wood density to growth performance in eight tree species from a tropical semi-dry climate. For. Ecol. Manage. 330, 126-136. doi: 10.1016/j.foreco.2014.06.039
42. Jacobsen, A. L., Ewers, F. W., Pratt, R. B., Paddock, W. A., and Davis, S. D. (2005). Do xylem fibers affect vessel cavitation resistance? PlantPhysiol. 139, 546-556. doi: 10.1104/pp.104.058404
43. Jacobsen, A. L., Pratt, R. B., Ewers, F. W., and Davis, S. D. (2007). Cavitation resistance among 26 chaparral species of southern California. Ecol. Monogr. 77, 99-115. doi: 10.1890/05-1879
44. King, D. A., Davies, S. J., Supardi, M. N. N., and Tan, S. (2005). Tree growth is related to light interception and wood density in two mixed dipterocarp forests of Malaysia. Funct. Ecol. 19, 445-453. doi: 10.1111/j.1365-2435.2005.00982
45. King, D. A., Davies, S. J., Tan, S., and Noor, N. S. M. (2006). The role of wood density and stem support costs in the growth and mortality of tropical trees. J. Ecol. 94, 670-680. doi: 10.1111/j.1365-2745.2006.01112
46. Kocher, P., Horna, V., Beckmeyer, I., and Leuschner, C. (2012). Hydraulic properties and embolism in small-diameter roots of five temperate broad-leaved tree species with contrasting drought tolerance. Ann. For. Sci. 69, 693-703. doi: 10.1007/s13595-012-0189-0
47. Leuschner, C., Wiens, M., Harteveld, M., Hertel, D., and Tjitrosemito, S. (2006). Patterns of fine root mass and distribution along a disturbance gradient in a tropical montane forest, central Sulawesi (Indonesia). Plant Soil 283, 163-174. doi: 10.1007/s11104-006-6638-5
48. Lintunen, A., and 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. doi: 10.1093/treephys/tpq085
49. Lovisolo, C., Perrone, I., Hartung, W., and Schubert, A. (2008). An abscisic acid-related reduced transpiration promotes gradual embolism repair when grapevines are rehydrated after drought. New Phytol. 180, 642-651. doi: 10.1111/j.1469-8137.2008.02592.x
50. Lovisolo, C., Schubert, A., and Sorce, C. (2002). Are xylem radial development and hydraulic conductivity in downwardly-growing grapevine shoots influenced by perturbed auxin metabolism? New Phytol. 156, 65-74. doi: 10.1046/j.1469-8137.2002.00492.x
51. Machado, S. R., Rodella, R. A., Angyalossy, V., and Marcati, C. R. (2007). Structural variations in root and stem wood of Styrax (Styracaceae) from Brazilian forest and cerrado. IAWA J. 28, 173-188. doi: 10.1163/2294193290001632
52. Maherali, H., Moura, C. F., Caldeira, M. C., Willson, C. J., and Jackson, R. B. (2005). Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees. Plant Cell Environ. 29, 571-583. doi: 10.1111/j.1365-3040.2005.01433
53. Maherali, H., Pockman, W. T., and Jackson, R. B. (2004). Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184-2199. doi: 10.1890/02-0538
54. Manoharan, P. T., Shanmugaiah, V., Balasubramanian, N., Gomathinayagam, S., Sharma, M. P., and Muthuchelian, K. (2010). Influence of AM fungi on the growth and physiological status of Erythrina variegata Linn. grown under different water stress conditions. Eur. J. Soil Biol. 46, 151-156. doi: 10.1016/j.ejsobi.2010.01.001
55. Martinez-Cabrera, H. I., Jones, C. S., Espino, S., and Schenk, H. J. (2009). Wood anatomy and wood density in shrubs: responses to varying aridity along transcontinental transects. Am. J. Bot. 96, 1388-1398. doi: 10.3732/ajb.0800237
56. Martinez-Vilalta, J., Prat, E., Oliveras, I., and Pinol, J. (2002). Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133, 19-29. doi: 10.1007/s00442-002-1009-2
57. McCulloh, K. A., Meinzer, F. C., Sperry, J. S., Lachenbruch, B., Voelker, S. L., Woodruff, D. R., et al. (2011). Comparative hydraulic architecture of tropical tree species representing a range of successional stages and wood density. Oecologia 167, 27-37. doi: 10.1007/s00442-011-1973-5
58. McCulloh, K. A., and Sperry, J. S. (2005). The evaluation of Murray's law in Psilotum nudum (Psilotaceae), an analogue of ancestral vascular plants. Am. J. Bot. 92, 985-989. doi: 10.3732/ajb.92.6.985
59. McCulloh, K. A., Sperry, J. S., and Adler, F. R. (2003). Water transport in plants obeys Murray's law. Nature 421, 939-942. doi: 10.1038/nature01444
60. McCulloh, K. A., Sperry, J. S., Lachenbruch, B., Meinzer, F. C., Reich, P. B., and Voelker, S. L. (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 Phytol. 186, 439-450. doi: 10.1111/j.1469-8137.2010.03181
61. McElrone, A. J., Pockman, W. T., Martinez-Vilalta, J., and Jackson, R. B. (2004). Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytol. 163, 507-517. doi: 10.1111/j.1469-8137.2004.01127
62. Meinzer, F. C., Campanello, P. I., Domec, J.-C., Gatti, M. G., Goldstein, G., Villalobos-Vega, R., et al. (2008). Constraints on physiological function associated with branch architecture and wood density in tropical forest trees. Tree Physiol. 28, 1609-1617. doi: 10.1093/treephys/28.11.1609
63. Meinzer, F. C., James, S. A., Goldstein, G., and Woodruff, D. (2003). Whole-tree water transport scales with sapwood capacitance in tropical forest canopy trees. Plant CellEnviron. 26, 1147-1155. doi: 10.1046/j.1365-3040.2003.01039
64. Moser, G., Leuschner, C., Hertel, D., Hoelscher, D., Koehler, M., Leitner, D., et al. (2010). Response of cocoa trees (Theobroma cacao) to a 13-month desiccation period in Sulawesi, Indonesia. Agroforest. Syst. 79, 171-187. doi: 10.1007/s10457-010-9303-9301
65. Motamayor, J. C., Lachenaud, P., Mota, J., Loor, R., Kuhn, D. N., Brown, J. S., et al. (2008). Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L). PLoS ONE 3:e3311. doi: 10.1371/jour-nal.pone.0003311
66. Mrema, A. F., Granhall, U., and Sennerbyforsse, L. (1997). Plant growth, leaf water potential, nitrogenase activity and nodule anatomy in Leucaena leuco- cephala as affected by water stress and nitrogen availability. Trees 12, 42-48. doi: 10.1007/pl00009695
67. Pinheiro, J. C., and Bates, D. M. (2000). Mixed-Effects Models in S and S-PLUS. New York, NY: Springer. doi: 10.1007/978-1-4419-0318-1
68. Poorter, L., Mcdonald, I., Alarcon, A., Fichtler, E., Licona, J.-C., Pena-Claros, M., et al. (2010). The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. NewPhytol. 185,481-492. doi: 10.1111/j.1469-8137.2009.03092
69. Pratt, R. B., Jacobsen, A. L., Ewers, F. W., and Davis, S. D. (2007). Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytol. 174, 787-798. doi: 10.1111/j.1469-8137.2007.02061
70. Preston, K. A., Cornwell, W. K., and Denoyer, J. L. (2006). Wood density and vessel traits as distinct correlates of ecological strategy in 51 California coast range angiosperms. New Phytol. 170, 807-818. doi: 10.1111/j.1469-8137.2006.01712
71. R Development Core Team. (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org
72. Rice, R. A., and Greenberg, R. (2000). Cacao cultivation and the conservation of biological diversity. Ambio 29, 167-173.
73. Richardson, S. J., Allen, R. B., Buxton, R. P., Easdale, T. A., Hurst, J. M., Morse, C. W., et al. (2013). Intraspecific relationships among wood density, leaf structural traits and environment in four co-occurring species of Nothofagus in New Zealand. PLoS ONE 8:e58878. doi: 10.1371/journal.pone.0058878
74. Russo, S. E., Jenkins, K. L., Wiser, S. K., Uriarte, M., Duncan, R. P., and Coomes, D. A. (2010). Interspecific relationships among growth, mortality and xylem traits of woody species from New Zealand. Funct. Ecol. 24, 253-262. doi: 10.1111/j.1365-2435.2009.01670
75. Schroth, G., and Harvey, C. A. (2007). Biodiversity conservation in cocoa production landscapes: an overview. Biodivers. Conserv. 16, 2237-2244. doi: 10.1007/s10531-007-9195-1
76. Schuldt, B., Leuschner, C., Brock, N., and 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. doi: 10.1093/treephys/tps122
77. Shinozaki, K., Yoda, K., Hozumi, K., and Kira, T. (1964). A quantitative analysis of plant form-the pipe model theory II. Further evidence of the theory and its application in forest ecology. Jpn. J. Ecol. 14, 133-139.
78. Sperry, J. S. (2000). Hydraulic constraints on plant gas exchange. Agric. For. Meteorol. 104, 13-23. doi: 10.1016/s0168-1923(00)00144-1
79. Sperry, J. S., Donnelly, J. R., and Tyree, M. T. (1988). A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ. 11, 35-40. doi: 10.1111/j.1365-3040.1988.tb01774
80. Sperry, J. S., Hacke, U. G., Oren, R., and Comstock, J. P. (2002). Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ. 25, 251-263. doi: 10.1046/j.0016-8025.2001.00799.x
81. Sperry, J. S., Meinzer, F. C., and McCulloh, K. A. (2008). Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ. 31, 632-645. doi: 10.1111/j.1365-3040.2007.01765
82. Sperry, J. S., Nichols, K. L., Sullivan, J. E. M., and Eastlack, S. E. (1994). Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75, 1736-1752. doi: 10.2307/1939633
83. Sperry, J. S., Smith, D. D., Savage, V. M., Enquist, B. J., McCulloh, K. A., Reich, P. B., et al. (2012). A species-level model for metabolic scaling in trees I. Exploring boundaries to scaling space within and across species. Funct. Ecol. 26, 1054-1065. doi: 10.1111/j.1365-2435.2012.02022
84. Spicer, R., and Gartner, B. L. (2001). The effects of cambial age and position within the stem on specific conductivity in Douglas-fir (Pseudotsuga menziesii) sapwood. Trees 15,222-229. doi: 10.1007/s004680100093
85. Sterck, F. J., Martinez-Vilalta, J., Mencuccini, M., Cochard, H., Gerrits, P., Zweifel, R., et al. (2012). Understanding trait interactions and their impacts on growth in Scots pine branches across Europe. Funct. Ecol. 26, 541-549. doi: 10.1111/j.1365-2435.2012.01963
86. Steudle, E. (2000). Water uptake by roots: effects of water deficit. J. Exp. Bot. 51, 1531-1542. doi: 10.1093/jexbot/51.350.1531
87. Swenson, N. G., and Enquist, B. J. (2007). Ecological and evolutionary determinants of a key plant functional trait: wood density and its community- wide variation across latitude and elevation. Am. J. Bot. 94, 451-459. doi: 10.3732/ajb.94.3.451
88. Thomas, D. S., Montagu, K. D., and Conroy, J. P. (2007). Temperature effects on wood anatomy, wood density, photosynthesis and biomass partitioning of Eucalyptus grandis seedlings. Tree Physiol. 27, 251-260. doi: 10.1093/treep-hys/27.2.251
89. Tscharntke, T., Clough, Y., Bhagwat, S. A., Buchori, D., Faust, H., Hertel, D., et al. (2011). Multifunctional shade-tree management in tropical agroforestry landscapes-a review. J. Appl. Ecol. 48, 619-629. doi: 10.1111/j.1365-2664.2010.01939
90. Tyree, M. T. (2003). Hydraulic limits on tree performance: transpiration, carbon gain and growth of trees. Trees 17, 95-100. doi: 10.1007/s00468-002-0227
91. Tyree, M. T., and Ewers, F. W. (1991). The hydraulic architecture of trees and other woody plants. New Phytol. 119, 345-360. doi: 10.1111/j.1469-8137.1991.tb00035
92. Tyree, M. T., and Zimmermann, M. H. (2002). Xylem Structure and The Ascent of Sap. Berlin: Springer. doi: 10.1007/978-3-662-04931-0
93. West, G. B., Brown, J. H., and Enquist, B. J. (1999). A general model for the structure and allometry of plant vascular systems. Nature 400, 664-667. doi: 10.1038/23251
94. Wheeler, J. K., Sperry, J. S., Hacke, U. G., and Hoang, N. (2005). Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ. 28, 800-812. doi: 10.1111/j.1365-3040.2005.01330
95. White, F. M. (1991). Viscous Fluid Flow, 2ndEdn. New York: McGraw-Hill, Inc.
96. Wurth, M. K. R., Pelaez-Riedl, S., Wright, S. J., and Korner, C. (2005). Non- structural carbohydrate pools in a tropical forest. Oecologia 143, 11-24. doi: 10.1007/s00442-004-1773-2
97. Zanne, A. E., Westoby, M., Falster, D. S., Ackerly, D. D., Loarie, S. R., Arnold, S. E. J., et al. (2010). Angiosperm wood structure: global patterns in vessel anatomy and their relation to wood density and potential conductivity. Am. J. Bot. 97, 207-215. doi: 10.3732/ajb.0900178
98. Zhang, J.-L., and Cao, K.-F. (2009). Stem hydraulics mediates leaf water status, carbon gain, nutrient use efficiencies and plant growth rates across dipterocarp species. Funct. Ecol. 23, 658-667. doi: 10.1111/j.1365-2435.2009.01552
99. Zufferey, V., Cochard, H., Ameglio, T., Spring, J.-L., and Viret, O. (2011). Diurnal cycles of embolism formation and repair in petioles of grapevine (Vitis vinifera cv. Chasselas). J. Exp. Bot. 62, 3885-3894. doi: 10.1093/jxb/err081