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Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms

  • Physiological ecology - Original Paper
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Abstract

The ability of plants to maintain water flow through leaves under water stress-induced tension (assessed as the leaf hydraulic vulnerability; P50 leaf) is intimately linked with survival. We examined the significance of P50 leaf as an adaptive trait in influencing the dry-end distributional limits of cool temperate woody angiosperm species. We also examined differences in within-site variability in P50 leaf between two high-rainfall montane rainforest sites in Tasmania and Peru, respectively. A significant relationship between P50 leaf and the 5th percentile of mean annual rainfall across each species distribution was found in Tasmania, suggesting that P50 leaf influences species climatic limits. Furthermore, a strong correlation between P50 leaf and the minimum rainfall availability was found using five phylogenetically independent species pairs in wet and dry evergreen tree species, suggesting that rainfall is an important selective agent in the evolution of leaf hydraulic vulnerability. Greater within-site variability in P50 leaf was found among dominant montane rainforest species in Tasmania than in Peru and this result is discussed within the context of differences in spatial and temporal environmental heterogeneity and parochial historical ecology.

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References

  • Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184

    Article  Google Scholar 

  • Blackman CJ, Brodribb TJ (2011) Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Funct Plant Biol 38:118–126

    Article  Google Scholar 

  • Blackman CJ, Brodribb TJ, Jordan GJ (2009) Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant Cell Environ 32:1584–1595

    Article  PubMed  Google Scholar 

  • Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123

    Article  PubMed  Google Scholar 

  • Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol 149:575–584

    Article  PubMed  CAS  Google Scholar 

  • Brodribb T, Hill RS (1999) The importance of xylem constraints in the distribution of conifer species. New Phytol 143:365–372

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173

    Article  PubMed  CAS  Google Scholar 

  • Brodribb TJ, Holbrook NM (2004) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant Cell Environ 27:820–827

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiol 137:1139–1146

    Article  PubMed  CAS  Google Scholar 

  • Brodribb TJ, Holbrook NM (2007) Forced depression of leaf hydraulic conductance in situ: effects on the leaf gas exchange of forest trees. Funct Ecol 21:705–712

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450

    Article  Google Scholar 

  • Bush MB, Silman MR, Urrego DH (2004) 48,000 years of climate and forest change in a biodiversity hotspot. Science 303:827–829

    Article  PubMed  CAS  Google Scholar 

  • Cavender-Bares J, Kitajima K, Bazzaz FA (2004) Multiple trait associations in relation to habitat differentiation among 17 Floridian oak species. Ecol Monogr 74:635–662

    Article  Google Scholar 

  • Choat B, Sack L, Holbrook NM (2007) Diversity of hydraulic traits in nine Cordia species growing in tropical forests with contrasting precipitation. New Phytol 175:686–698

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cochard H, Barigah TS, Herbert E, Caupin F (2007) Cavitation in plants at low temperature: is sap transport limited by the tensile strength of water as expected from Briggs’ Z-tube experiment? New Phytol 173:571–575

    Article  PubMed  Google Scholar 

  • Crowden RK (1999) Alpine vegetation. In: Reid JB, Hill RS, Brown MJ, Hovenden MJ (eds) Vegetation of tasmania. Australian Biological Resources Study, Canberra, pp 333–356

    Google Scholar 

  • Feild TS, Chatelet DS, Brodribb TJ (2009) Ancestral xerophobia: a hypothesis of the whole plant ecophysiology of early angiosperms. Geobiology 7:237–264

    Article  PubMed  CAS  Google Scholar 

  • Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461

    Article  Google Scholar 

  • Hao GY et al (2008) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155:405–415

    Article  PubMed  Google Scholar 

  • Houlder D, Hutchinson M, Nix H, McMahon J (2003) Anuclim user’s guide. Australian National University, Canberra

    Google Scholar 

  • Hunt BG (2009) Multi-annual dry episodes in Australian climatic variability. Int J Climatol 29:1715–1730

    Article  Google Scholar 

  • Jacobsen AL, Pratt RB, Ewers FW, Davis SD (2007) Cavitation resistance among 26 chaparral species of southern California. Ecol Monogr 77:99–115

    Article  Google Scholar 

  • Johnson DM, Meinzer FC, Woodruff DR, McCulloh KA (2009a) Leaf xylem embolism, detected acoustically and by cryo-SEM, corresponds to decreases in leaf hydraulic conductance in four evergreen species. Plant Cell Environ 32:828–836

    Article  PubMed  Google Scholar 

  • Johnson DM, Woodruff DR, McCulloh KA, Meinzer FC (2009b) Leaf hydraulic conductance, measured in situ, declines and recovers daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species. Tree Physiol 29:879–887

    Article  PubMed  CAS  Google Scholar 

  • Jordan GJ (1997) Evidence of Pleistocene plant extinction and diversity from Regatta Point, western Tasmania, Australia. Bot J Linn Soc 123:45–71

    Article  Google Scholar 

  • Jordan GJ, Dillon RA, Weston PH (2005) Solar radiation as a factor in the evolution of scleromorphic leaf anatomy in Proteaceae. Am J Bot 92:789–796

    Article  PubMed  Google Scholar 

  • Jordan GJ, Weston PH, Carpenter RJ, Dillon RA, Brodribb TJ (2008) The evolutionary relations of sunken covered, and encrypted stomata to dry habitats in Proteaceae. Am J Bot 95:521–530

    Article  PubMed  Google Scholar 

  • Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199

    Article  Google Scholar 

  • Markesteijn L, Poorter L, Paz H, Sack L, Bongers F (2011) Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits. Plant Cell Environ 31:137–148

    Article  Google Scholar 

  • McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185

    Article  PubMed  Google Scholar 

  • Meinzer FC, Clearwater MJ, Goldstein G (2001) Water transport in trees: current perspectives, new insights and some controversies. Environ Exp Bot 45:239–262

    Article  PubMed  Google Scholar 

  • Meinzer FC, McCulloh KA, Lachenbruch B, Woodruff DR, Johnson DM (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

    Article  PubMed  Google Scholar 

  • Nunez M, Colhoun EA (1986) A note on air temperature lapse rates on Mount Wellington. Pap Proc R Soc Tasman 120:11–15

    Google Scholar 

  • Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299

    Article  PubMed  CAS  Google Scholar 

  • Poorter L, Markesteijn L (2008) Seedling traits determine drought tolerance of tropical tree species. Biotropica 40:321–331

    Article  Google Scholar 

  • Poorter L, McDonald I, Alarcon A, Fichtler E, Licona JC, Pena-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492

    Article  PubMed  Google Scholar 

  • Reich PB, Borchert R (1984) Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. J Ecol 72:61–74

    Article  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: A test across six biomes. Ecology 80:1955–1969

    Article  Google Scholar 

  • Ricklefs RE (2008) Disintegration of the ecological community. Am Nat 172:741–750

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26:1343–1356

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, San Francisco

    Google Scholar 

  • Steane DA, McKinnon GE, Vaillancourt RE, Potts BM (1999) ITS sequence data resolve higher level relationships among the eucalypts. Mol Phylogenet Evol 12:215–223

    Article  PubMed  CAS  Google Scholar 

  • Turner IM (1994) Sclerophylly: primarily protective? Funct Ecol 8:669–675

    Article  Google Scholar 

  • Tyree MT, Hammel HT (1972) Measurement of turgor pressure and water relations of plants by pressure-bomb technique. J Exp Bot 23:267–282

    Article  Google Scholar 

  • Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Plant Mol Biol 40:19–38

    Article  Google Scholar 

  • Vasquez R, Rojas R, Monteagudo A, Meza K, van der Werf H, Ortiz-Gentry R, Catchpole D (2005) Flora vascular de la selva central del peru: una aproximacion de la composicion floristica de tres areas naturales protegidas. Arnaldoa 12:112–125

    Google Scholar 

  • Woodruff DR, Meinzer FC, Lachenbruch B (2008) Height-related trends in leaf xylem anatomy and shoot hydraulic characteristics in a tall conifer: safety versus efficiency in water transport. New Phytol 180:90–99

    Article  PubMed  CAS  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We wish to thank Damien Catchpole for his logistical support during field work in Peru and provision of meteorological data. We acknowledge the Peruvian authorities for approving the research within the national park (Authorisation No. 025-C/C-2006-INRENA-INAP and Authorisation No. 033-C/C-2008-INRENA-INAP) and the exportation of plant material (Permit NO. 000497-AG-DGFFS). We also thank Carlos Llerena, Guido Casimira and Yoshie Yoshioka for administrative and technical assistance in Peru. We are also grateful to Prof. Taylor Feild for constructive comments on the manuscript. The Australian Research Council provided support in the form of a fellowship to T.J.B. and a post-graduate grant to C.J.B.

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Correspondence to Chris J. Blackman.

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Communicated by Frederick Meinzer.

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442_2011_2064_MOESM1_ESM.doc

Online Resource 1. Ancestral habitat affinity for the Tasmanian species and the 5th and 95th percentile of mean annual rainfall across each Tasmanian species’ distribution (DOC 141 kb)

Online Resource 2. Phylogeny of the plant species sampled from Tasmania and Peru (DOC 61 kb)

Online Resource 3. Remaining vulnerability curves for the Peruvian montane rainforest species (DOC 764 kb)

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Blackman, C.J., Brodribb, T.J. & Jordan, G.J. Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms. Oecologia 168, 1–10 (2012). https://doi.org/10.1007/s00442-011-2064-3

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