Stem and leaf hydraulic properties are finely coordinated in three tropical rain forest tree species

Plant Cell and Environment

Volumn 38, Issue 12, 2015, Pages 2652-2661

  Nolf, Markus ^a,b   Creek, Danielle ^b   Duursma, Remko ^b   Holtum, Joseph ^c   Mayr, Stefan ^a   Choat, Brendan ^b  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b WESTERN SYDNEY UNIVERSITY   (Australia)

^c JAMES COOK UNIVERSITY   (Australia)

Author keywords

Hydraulic coordination; Hydraulic vulnerability; Plant water relations; Safety margin; Ultrasonic emissions

Indexed keywords

CLIMATE CHANGE; GLOBAL CLIMATE; HYDRAULIC CONDUCTIVITY; LEAF AREA; PLANT WATER RELATIONS; RAINFOREST; STEM; TREE; TROPICAL FOREST; WATER SUPPLY; XYLEM;

WATER;

AUSTRALIA; ELAEOCARPACEAE; EVAPOTRANSPIRATION; MELIACEAE; PHYSIOLOGY; PLANT LEAF; PLANT STEM; RAIN FOREST; SYZYGIUM; TEMPERATURE; TREE; TROPIC CLIMATE; XYLEM;

AUSTRALIA; ELAEOCARPACEAE; MELIACEAE; PLANT LEAVES; PLANT STEMS; PLANT TRANSPIRATION; RAINFOREST; SYZYGIUM; TEMPERATURE; TREES; TROPICAL CLIMATE; WATER; XYLEM;

EID: 84948387357     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12581     Document Type: Article

References (77)

1. Aitken S.N., Yeaman S., Holliday J.A., Wang T. & Curtis-McLane S. (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications 1, 95-111.
2. Allison I., Bindoff N.L., Bindschadler R.A., Cox P.M., de Noblet N., England M.H., ... Weaver A.J. (2011) The Copenhagen Diagnosis: Updating the World on the Latest Climate Science, Elsevier, Oxford.
3. Blackman C.J., Brodribb T.J. & Jordan G.J. (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytologist 188, 1113-1123.
4. Boland D.J., Brooker M.I.H., Chippendale G., Hall N., Hyland B., Johnston R., ... Turner J. (2006) Forest trees of Australia. (5th ed.). CSIRO publishing, Clayton, VIC, Australia.
5. Brodersen C.R., McElrone A.J., Choat B., Lee E.F., Shackel K.A. & Matthews M.A. (2013) In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiology 161, 1820-1829.
6. Brodribb T.J. & Cochard H. (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149, 575-584.
7. Brodribb T.J. & Holbrook N.M. (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132, 2166-2173.
8. Brodribb T.J. & Holbrook N.M. (2004) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant, Cell and Environment 27, 820-827.
9. Brodribb T.J., Holbrook N.M., Edwards E.J. & Gutiérrez M.V. (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell and Environment 26, 443-450.
10. Brodribb T.J., McAdam S.A., Jordan G.J. & Martins S.C. (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences of the United States of America 111, 14489-14493.
11. Bucci S.J., Scholz F.G., Goldstein G., Meinzer F.C. & Sternberg L.D.L. (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant, Cell and Environment 26, 1633-1645.
12. Bucci S.J., Scholz F.G., Goldstein G., Meinzer F.C., Franco A.C., Zhang Y. & Hao G.-Y. (2008) Water relations and hydraulic architecture in Cerrado trees: adjustments to seasonal changes in water availability and evaporative demand. Brazilian Journal of Plant Physiology 20, 233-245.
13. Bucci S.J., Scholz F.G., Campanello P.I., Montti L., Jimenez-Castillo M., Rockwell F.A., ... Goldstein G. (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiology 32, 880-893.
14. Bucci S.J., Scholz F.G., Peschiutta M.L., Arias N.S., Meinzer F.C. & Goldstein G. (2013) The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought-induced embolism by leaves and roots. Plant, Cell and Environment 26, 2163-2174.
15. Bureau of Meteorology (2013) Climate Data Online, [WWW document] URL http://www.bom.gov.au/climate/data/
16. Chen J.-W., Zhang Q., Li X.-S. & Cao K.-F. (2009) Independence of stem and leaf hydraulic traits in six Euphorbiaceae tree species with contrasting leaf phenology. Planta 230, 459-468.
17. Chen J.W., Zhang Q., Li X.S. & Cao K.F. (2010) Gas exchange and hydraulics in seedlings of Hevea brasiliensis during water stress and recovery. Tree Physiology 30, 876-885.
18. Choat B., Lahr E.C., Melcher P.J., Zwieniecki M.A. & Holbrook N.M. (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant, Cell and Environment 28, 1082-1089.
19. Choat B., Ball M.C., Luly J.G., Donnelly C.F. & Holtum J.A.M. (2006) Seasonal patterns of leaf gas exchange and water relations in dry rain forest trees of contrasting leaf phenology. Tree Physiology 26, 657-664.
20. Choat B., Drayton W.M., Brodersen C., Matthews M.A., Shackel K.A., Wada H. & McElrone A.J. (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant, Cell and Environment 33, 1502-1512.
21. Choat B., Jansen S., Brodribb T.J., Cochard H., Delzon S., Bhaskar R., ... Zanne A.E. (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752-755.
22. Cochard H., Coll L., Le Roux X. & Améglio T. (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiology 128, 282-290.
23. Cochard H., Badel E., Herbette S., Delzon S., Choat B. & Jansen S. (2013) Methods for measuring plant vulnerability to cavitation: a critical review. Journal of Experimental Botany 64, 4779-4791.
24. Cook K.H. & Vizy E.K. (2007) Effects of twenty-first-century climate change on the Amazon rain forest. Journal of Climate 21, 542-560.
25. Duursma R. (2014) Fit vulnerability curves in R (R package) [WWW document] URL https://bitbucket.org/remkoduursma/fitplc/
26. Grace J., Malhi Y., Higuchi N. & Meir P. (2001) Productivity of tropical forests. In Terrestrial Global Productivity (eds J. Roy, B. Saugier & H.A. Mooney ), pp. 401-426. Academic Press, San Diego, CA, USA.
27. Guyot G., Scoffoni C. & Sack L. (2012) Combined impacts of irradiance and dehydration on leaf hydraulic conductance: insights into vulnerability and stomatal control. Plant, Cell and Environment 35, 857-871.
28. Hacke U. & Sauter J. (1996) Drought-induced xylem dysfunction in petioles, branches, and roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Plant Physiology 111, 413-417.
29. Hao G.-Y., Hoffmann W.A., Scholz F.G., Bucci S.J., Meinzer F.C., Franco A.C., ... Goldstein G. (2008) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155, 405-415.
30. Hartmann H., Ziegler W., Kolle O. & Trumbore S. (2013) Thirst beats hunger - declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytologist 200, 340-349.
31. Hyland B.P.M., Whiffin T. & Zich F.A. (2010) Australian tropical rainforest plants. Trees, shrubs and vines. Version 6.1 [WWW document] URL http://keys.trin.org.au/key-server/data/0e0f0504-0103-430d-8004-060d07080d04/media/Html/index.html
32. Johnson D.M., McCulloh K.A., Meinzer F.C., Woodruff D.R. & Eissenstat D.M. (2011) Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species. Tree Physiology 31, 659-668.
33. Johnson D.M., McCulloh K.A., Woodruff D.R. & Meinzer F.C. (2012a) Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Science 195, 48-53.
34. Johnson D.M., McCulloh K.A., Woodruff D.R. & Meinzer F.C. (2012b) Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance. Plant, Cell and Environment 35, 760-769.
35. Kikuta S.B., Lo Gullo M.A., Nardini A., Richter H. & Salleo S. (1997) Ultrasound acoustic emissions from dehydrating leaves of deciduous and evergreen trees. Plant, Cell and Environment 20, 1381-1390.
36. Kim Y.X. & Steudle E. (2007) Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. Journal of Experimental Botany 58, 4119-4129.
37. Kirkham M.B. (2004) Principles of Soil and Plant Water Relations, 1st edn, Elsevier Academic Press, Amsterdam, the Netherlands.
38. Lewis S.L. (2006) Tropical forests and the changing earth system. Philosophical Transactions B 361, 195-210.
39. Liddell M. (2013) Baseline Climate Data 2012, Far North Queensland Rainforest Supersite, Cape Tribulation Node. Document ID lloyd.238.14 [WWW document] URL http://www.tern-supersites.net.au/knb/metacat/lloyd.238.14/html
40. Maherali H., Pockman W.T. & Jackson R.B. (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184-2199.
41. Martorell S., Diaz-Espejo A., Medrano H., Ball M.C. & Choat B. (2014) Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. Plant, Cell and Environment 37, 617-626.
42. Mayr S. & Rosner S. (2011) Cavitation in dehydrating xylem of Picea abies: energy properties of ultrasonic emissions reflect tracheid dimensions. Tree Physiology 31, 59-67.
43. Meinzer F.C., Woodruff D.R., Domec J.-C., Goldstein G., Campanello P.I., Gatti M.G. & Villalobos-Vega R. (2008) Coordination of leaf and stem water transport properties in tropical forest trees. Oecologia 156, 31-41.
44. Meinzer F.C., Johnson D.M., Lachenbruch B., McCulloh K.A. & Woodruff D.R. (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Functional Ecology 23, 922-930.
45. Milburn J.A. & Johnson R.P.C. (1966) The conduction of sap. II. Detection of vibrations produced by sap cavitation in Ricinus xylem. Planta 69, 43-52.
46. Nardini A. & Luglio J. (2014) Leaf hydraulic capacity and drought vulnerability: possible trade-offs and correlations with climate across three major biomes. Functional Ecology 28, 810-818.
47. Nardini A. & Salleo S. (2003) Effects of the experimental blockage of the major veins on hydraulics and gas exchange of Prunus laurocerasus L. leaves. Journal of Experimental Botany 54, 1213-1219.
48. Ogle K., Barber J.J., Willson C. & Thompson B. (2009) Hierarchical statistical modeling of xylem vulnerability to cavitation. New Phytologist 182, 541-554.
49. Phillips O.L., Aragão L.E.O.C., Lewis S.L., Fisher J.B., Lloyd J., López-González G., ... Torres-Lezama A. (2009) Drought sensitivity of the Amazon rainforest. Science 323, 1344-1347.
50. Ponomarenko A., Vincent O., Pietriga A., Cochard H., Badel E. & Marmottant P. (2014) Ultrasonic emissions reveal individual cavitation bubbles in water-stressed wood. Journal of the Royal Society, Interface 11: 20140480, doi: 10.1098/rsif.2014.0480.
51. Prentice I.C., Farquhar G.D., Fasham M.J.R., Goulden M.L., Heimann M., Jaramillo V.J., ... Wallace D.W. (2001) The carbon cycle and atmospheric carbon dioxide. In Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change (eds J.T. Houghton, Y. Ding & D.J. Griggs ), pp. 183-237. Cambridge University Press, Cambridge.
52. R Core Team (2013) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
53. Raven J.A. (2002) Selection pressures on stomatal evolution. New Phytologist 153, 371-386.
54. Ritman K.T. & Milburn J.A. (1988) Acoustic emissions from plants: ultrasonic and audible compared. Journal of Experimental Botany 39, 1237-1248.
55. Rosetto M., Jones R. & Hunter J. (2004) Genetic effects of rainforest fragmentation in an early successional tree (Elaeocarpus grandis). Heredity 93, 610-618.
56. Sack L. & Holbrook N.M. (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361-381.
57. Sack L., Pasquet-Kok J. & PrometheusWiki Contributors (2011) Leaf pressure-volume curve parameters. PrometheusWiki [WWW document] URL http://prometheuswiki.publish.csiro.au/tiki-index.php?page=Leaf+pressure-volume+curve+parameters
58. Salazar L.F., Nobre C.A. & Oyama M.D. (2007) Climate change consequences on the biome distribution in tropical South America. Geophysical Research Letters 34, L09708.
59. Salleo S., Lo Gullo M.A., Raimondo F. & Nardini A. (2001) Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange? Plant, Cell and Environment 24, 851-859.
60. Schneider C.A., Rasband W.S. & Eliceiri K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675.
61. Scholander P., Bradstreet E., Hemmingsen E. & Hammel H. (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148, 339-346.
62. Scoffoni C. & Sack L. (2014) Are leaves 'freewheelin'? Testing for a Wheeler-type effect in leaf xylem hydraulic decline. Plant, Cell and Environment 38, 534-543.
63. Scoffoni C., McKown A.D., Rawls M. & Sack L. (2012) Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state. Journal of Experimental Botany 63, 643-658.
64. Scoffoni C., Vuong C., Diep S., Cochard H. & Sack L. (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiology 164, 1772-1788.
65. Sperry J.S. (2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13-23.
66. Sperry J.S. & Pockman W.T. (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant, Cell and Environment 16, 279-287.
67. Sperry J.S., Donnelly J.R. & Tyree M.T. (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell and Environment 11, 35-40.
68. Tyree M.T. & Dixon M.A. (1983) Cavitation events in Thuja occidentalis L. Plant Physiology 72, 1094-1099.
69. Tyree M.T. & Ewers F.W. (1991) The hydraulic architecture of trees and other woody plants. New Phytologist 119, 345-360.
70. Tyree M.T. & Hammel H.T. (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23, 267-282.
71. Tyree M.T. & Zimmermann M.H. (2002) Xylem Structure and the Ascent of Sap, 2nd edn, Springer, Berlin, Germany.
72. Wheeler J.K., Huggett B.A., Tofte A.N., Rockwell F.E. & Holbrook N.M. (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell and Environment 36, 1938-1949.
73. White E., Tucker N., Meyers N. & Wilson J. (2004) Seed dispersal to revegetated isolated rainforest patches in North Queensland. Forest Ecology and Management 192, 409-426.
74. Wolkerstorfer S.V., Rosner S. & Hietz P. (2012) An improved method and data analysis for ultrasound acoustic emissions and xylem vulnerability in conifer wood. Physiologia Plantarum 146, 184-191.
75. Zhang Y.J., Meinzer F.C., Hao G.Y., Scholz F.G., Bucci S.J., Takahashi F.S.C., ... Goldstein G. (2009) Size-dependent mortality in a Neotropical savanna tree: the role of height-related adjustments in hydraulic architecture and carbon allocation. Plant, Cell and Environment 32, 1456-1466.
76. Zimmermann M.H. (1983) Xylem Structure and the Ascent of Sap, 1st edn, Springer, Berlin, Germany.
77. Zimmermann M.H. & Brown C.L. (1971) Trees: Structure and Function, Springer, New York, USA.