Contrasting xylem vessel constraints on hydraulic conductivity between native and non-native woody understory species

Frontiers in Plant Science

Volumn 4, Issue NOV, 2013, Pages

  Smith, Maria S ^a   Fridley, Jason D ^b   Yin, Jingjing ^a   Bauerle, Taryn L ^a  

^a Department of Obstetrics Gynecology   (United States)

^b SYRACUSE UNIVERSITY   (United States)

Author keywords

Efficiency vs. Safety; Embolism vulnerability; Exotic woody plants; Hydraulic conductivity; Vessel connectivity; Xylem anatomy

Indexed keywords

EID: 84900861635     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00486     Document Type: Article

References (58)

1. Aref, I. M., Ahmed, A. I., Khan, P. R., El-Atta, H. A., and Iqbal, M. (2013). Drought-induced adaptive changes in the seedling anatomy of Acacia ehrenbergiana and Acacia tortilis subsp raddiana. Trees 27, 959-971. doi: 10.1007/s00468-013-0848-2
2. Baas, P. (1986). "Ecological patterns of xylem anatomy, " in On the Economy of Plant Form and Function, ed T. J. Givinish. (Cambridge: Cambridge University Press), 327-351.
3. Bauerle, T. L., Centinari, M., and Bauerle, W. L. (2011). Shifts in xylem vessel diameter and embolisms in grafted apple trees of differing rootstock growth potential in response to drought. Planta 234, 1045-1054. doi: 10.1007/s00425-011-1460-6
4. Becker, P., Tyree, M. T., and Tsuda, M. (1999). Hydraulic conductances of angiosperms versus conifers: similar transport sufficiency at the whole-plant level. Tree Physiol. 19, 445-452. doi: 10.1093/treephys/19.7.445
5. Brodribb, T. J., Holbrook, N. M., and Gutiérrez, M. V. (2002). Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees. Plant Cell and Environ. 25, 1435-1444. doi: 10.1046/j.1365-3040.2002.00919.x
6. Caplan, J. S., and Yeakley, J. A. (2010). Water relations advantages for non-native Rubus armeniacus over two native ruderal congeners. Plant Ecol. 210, 169-179. doi: 10.1007/s11258-010-9747-4
7. Carlquist, S. (2009). Non-random vessel distribution in woods: patterns, modes, diversity, correlations. Aliso. 27, 39-58.
8. Carlquist, S. (1977). Ecological factors in wood evolution: a floristic approach. Am. J. Bot. 64, 887-896. doi: 10.2307/2442382
9. Cavaleri, M. A., and Sack, L. (2010). Comparative water use of native and invasive plants at multiple scales: a global meta-analysis. Ecology 91, 2705-2715. doi: 10.1890/09-0582.1
10. Christman, M. A., Sperry, J. S., and Adler, F. R. (2009). Testing the 'rare pit' hypothesis for xylem cavitation resistance in three species of Acer. New Phytologist. 182, 664-674. doi: 10.1111/j.1469-8137.2009.02776.x
11. Christman, M. A., and Sperry, J. S. (2010). Single-vessel flow measurements indicate scalariform perforation plates confer higher flow resistance than previously estimated. Plant Cell and Environ. 33, 431-443. doi: 10.1111/j.1365-3040.2009.02094.x
12. 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
13. Cochard, H., and Tyree, M. T. (1990). Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol. 6, 393-407. doi: 10.1093/treephys/6.4.393
14. Daehler, C. C. (2003). Performance comparisons of co-occuring native and alien plants: Implications for conservation and restoration. Annu. Rev. Ecol. Evol. Syst. 34, 183-211. doi: 10.1146/annurev.ecolsys.34.011802.132403
15. Dale, M. P., and Causton, D. R. (1992). The ecophysiology of Veronica chamaedrys, V. Montana and V. officinalis. II. The interaction of irradiance and water regime. J. Ecol. 80, 493-504. doi: 10.2307/2260693
16. Davis, S. D., Sperry, J. S., and Hacke, U. G. (1999). The relationship between xylem conduit diameter and cavitation caused by freezing. Am. J. Bot. 86, 1367-1372. doi: 10.2307/2656919
17. Davis, M. A., Grime, J. P., and Thompson, K. (2000). Fluctuating resources in plant communities: a general theory of invisibility. J. Ecol. 88, 528-534. doi: 10.1046/j.1365-2745.2000.00473.x
18. Drenovsky, R. E., Khasanova, A., and James, J. J. (2012). Trait convergence and plasticity among native and invasive species in resource-poor environments. Am. J. Bot. 99, 629-639. doi: 10.3732/ajb.1100417
19. Dawson, W., Fischer, M., and van Kleunen, M. (2011). The maximum relative growth rate of common UK plant species is positively associated with their global invasiveness. Glob. Ecol. Biogeogr. 20, 299-306. doi: 10.1111/j.1466-8238.2010.00599.x
20. Fridley, J. D. (2012). Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485, 359-364. doi: 10.1038/nature11056
21. Funk, J. L., and Vitousek, P. M. (2007). Resource-use efficiency and plant invasion in low-resource systems. Nature 446, 1079-1081. doi: 10.1038/nature05719
22. Gilbert, B., Wright, S. J., Muller-Landau, H. C., Kitajima, K., and Hernandez, A. (2006). Life history trade-offs in tropical trees and lianas. Ecology 87, 1281-1288. doi: 10.1890/0012-9658(2006)87[1281:LHTITT]2.0.CO;2
23. 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 species. Funct. Ecol. 26, 343-352. doi: 10.1111/j.1365-2435.2012.01962.x
24. Goldberg, D. (1987). Neighborhood competition in an old field plant community. Ecology 68, 1211-1223. doi: 10.2307/1939205
25. Gonçalves, B., Correia, C., Silva, A., Bacelar, E., 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
26. Grime, J. P. (2001). Plant Strategies, Vegetation Processes, and Ecosystem Properties. New York, NY: John Wiley & Sons Ltd.
27. Grotkopp, E., Rejmanek, M., and Rost, T. L. (2002). Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Am. Nat. 159, 396-419. doi: 10.1086/338995
28. Hacke, U. G., Sperry, J. S., Pockman, W. T., Davis, S. D., and McCulloh, K. A. (2001). Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126, 457-461. doi: 10.1007/s004420100628
29. Hacke, U. G., Sperry, J. S., Wheeler, J. K., and Castro, L. (2006). Scaling of angiosperm xylem xtructure with safety and efficiency. Tree Physiol. 26, 689-701. doi: 10.1093/treephys/26.6.689
30. Jansen, S., Baas, P., Gasson, P., Lens, F., and Smets, E. (2004). Variation in xylem structure from tropics to tundra: Evidence from vestured pits. Proc. Natl. Acad. Sci. 101, 8833-8837. doi: 10.1073/pnas.0402621101
31. Lens, F., Sperry, J. S., Christman, M. A., Choat, B., Rabaey, D., and Jansen, S. (2011). Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol. 190, 709-723. doi: 10.1111/j.1469-8137.2010.03518.x
32. Loepfe, L., Martinez-Vilalta, J., Piñnol, J., and Mencuccini, M. (2007). The relevance of xylem network structure for plant hydraulic efficiency and safety. J. Theor. Biol. 247, 788-803. doi: 10.1016/j.jtbi.2007.03.036
33. Markesteijn, L., Poorter, L., Bongers, F., Paz, H., and Sack, L. (2011). Hydraulics and life history of tropical dry forest tree species: coordination of species' drought and shade tolerance. New Phytol. 191, 480-495. doi: 10.1111/j.1469-8137.2011.03708.x
34. McAlpine, K. G., Linley, J., and Kubien, D. S. (2008). Photosynthesis and water-use efficiency: A comparison between invasive (exotic) and non-invasive (native) species. Austral Ecology 33, 10-19. doi: 10.1111/j.1442-9993.2007.01784.x
35. McCulloh, K., Sperry, J. S., Lachenbruch, B., Meinzer, F. C., Reich, P. B., and 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 Phytol. 186, 439-450. doi: 10.1111/j.1469-8137.2010.03181.x
36. McCully, M. E., Huang, C. X., and Ling, L. E. C. (1998). Daily embolism and refilling of xylem vessels in the roots of field-grown maize. New Phytol. 138, 327-342. doi: 10.1046/j.1469-8137.1998.00101.x
37. McDowell, S. C. L. (2002). Photosynthetic characteristics of invasive and non-invasive species of Rubus (Rosaceae). Am. J. Bot. 89, 1431-1438. doi: 10.3732/ajb.89.9.1431
38. Meinzer, F. C., Clearwater, M. J., and Goldstein, G. (2001). Water transport in trees: current perspectives, new insights and some controversies. Environ. Exp. Bot. 45, 239-262. doi: 10.1016/S0098-8472(01)00074-0
39. Meinzer, F. C., McCulloh, K. A., Lachenbruch, B., Woodruff, D. R., and Johnson, D. M. (2010). The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecologia 164, 287-296. doi: 10.1007/s00442-010-1734-x
40. Pockman, W. T., and Sperry, J. S. (1996). Freezing-induced xylem cavitation and the northern limit of Larrea tridentata. Oecologia 109, 19-27. doi: 10.1007/s004420050053
41. Pockman, W. T., and Sperry, J. S. (2000). Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am. J. Bot. 87, 1287-1299. doi: 10.2307/2656722
42. Pratt, R. B., and Black, R. A. (2006). Do invasive trees have a hydraulic advantage over native trees? Biol. Invasions 8, 1331-1341. doi: 10.1007/s10530-005-0422-y
43. Ruzin, S. E. (1999). Plant Microtechnique and Microscopy. Oxford: Oxford University Press.
44. 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
45. 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.x
46. 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 and Environ. 31, 632-645. doi: 10.1111/j.1365-3040.2007.01765.x
47. 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
48. Steppe, K., and Lemeur, R. (2007). Effects or ring-porous and diffuse-porous stem wood anatomy on the hydraulic parameters used in water flow and storage model. Tree Physiol. 27, 43-52. doi: 10.1093/treephys/27.1.43
49. Taneda, H., and Sperry, J. S. (2008). A case-study of water transport in co-occurring ring-versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol. 28, 1641-1651. doi: 10.1093/treephys/28.11.1641
50. 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.x
51. Tyree, M. T., Sinclair, B., Lu, P., and Granier, A. (1993). Whole shoot hydraulic resistance in Quercus species measured with a new high-pressure flowmeter. Annales des sciences forestières 50, 417-423. doi: 10.1051/forest:19930501
52. Tyree, M. T., Davis, S. D., and Cochard, H. (1994). Biophysical perspectives of xylem evolution-is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction. Iawa J. 15, 335-360.
53. Tyree, M. T, Patiño, S., Bennink, J., and Alexander, J. (1995). Dynamic measurements of root hydraulic conductivity using a high-pressure flowmeter in the laborartory and field. J. Exp. Bot. 282, 83-94. doi: 10.1093/jxb/46.1.83
54. Tyree, M. T., and Zimmermann, M. H. (2002). Xylem Structure and the Ascent of Sap. Berlin: Springer Verlag. doi: 10.1007/978-3-662-04931-0
55. Wheeler, J. W., Sperry, J. S., Hacke, U. G., and Hoang, N. (2005). Inter-vessel pitting and cavitation in woody Rosaceae and other vesseled plants: a basis for a safety vs. efficiency trade-off in xylem transport. Plant Cell and Environ. 28, 800-812.
56. Woodrum, C. L., Ewers, F. W., and Telewski, F. W. (2003). Hydraulic, biomechanical, and anatomical interactions of xylem from five species of Acer (Aceraceae). Am. J. Bot. 90, 693-699. doi: 10.3732/ajb.90.5.693
57. Zanne, A. E., Westoby, M., Falster, D. S., Ackerly, D. D., Loarie, S. R., Arnold, S. E., 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
58. Zimmermann, M. H., and Jeje, A. A. (1981). Vessel length distribution of some American woody plants. Can. J. Bot. 59, 1882-1892. doi: 10.1139/b81-248