Intraspecific variation in drought susceptibility in Eucalyptus globulus is linked to differences in leaf vulnerability
Christopher J. Lucani
A , Timothy J. Brodribb A C , Greg Jordan A and Patrick J. Mitchell B
+ Author Affiliations
- Author Affiliations
A School of Natural Sciences, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.
B CSIRO Land and Water, 15 College Road, Sandy Bay, Tas. 7005, Australia.
C Corresponding author. Email: timothy.brodribb@utas.edu.au
Functional Plant Biology 46(3) 286-293 https://doi.org/10.1071/FP18077
Submitted: 28 March 2018 Accepted: 19 October 2018 Published: 23 November 2018
Abstract
Understanding intraspecific variation in the vulnerability of the xylem to hydraulic failure during drought is critical in predicting the response of forest tree species to climate change. However, few studies have assessed intraspecific variation in this trait, and a likely limitation is the large number of measurements required to generate the standard ‘vulnerability curve’ used to assess hydraulic failure. Here we explore an alternative approach that requires fewer measurements, and assess within species variation in leaf xylem vulnerability in Eucalyptus globulus Labill., an ecologically and economically important species with known genetic variation in drought tolerance. Using this approach we demonstrate significant phenotypic differences and evidence of plasticity among two provenances with contrasting drought tolerance.
Additional keywords: eucalypt, leaf xylem vulnerability.
References
Aasamaa K, Sõber A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Functional Plant Biology 28, 765–774.| Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees.Crossref | GoogleScholarGoogle Scholar |
Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proceedings of the National Academy of Sciences of the United States of America 106, 7063–7066.
| Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought.Crossref | GoogleScholarGoogle Scholar |
Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6, art129
| On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene.Crossref | GoogleScholarGoogle Scholar |
Anderegg WRL (2015) Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation. New Phytologist 205, 1008–1014.
| Spatial and temporal variation in plant hydraulic traits and their relevance for climate change impacts on vegetation.Crossref | GoogleScholarGoogle Scholar |
Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B (2016) Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proceedings of the National Academy of Sciences of the United States of America 113, 5024–5029.
| Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe.Crossref | GoogleScholarGoogle Scholar |
Blackman CJ, Brodribb TJ, Jordan GJ (2012) Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms. Oecologia 168, 1–10.
| Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms.Crossref | GoogleScholarGoogle Scholar |
Blackman CJ, Aspinwall MJ, Resco de Dios V, Smith RA, Tissue DT (2016) Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2. Functional Ecology 30, 1491–1500.
| Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2.Crossref | GoogleScholarGoogle Scholar |
Blackman CJ, Aspinwall MJ, Tissue DT, Rymer PD (2017) Genetic adaptation and phenotypic plasticity contribute to greater leaf hydraulic tolerance in response to drought in warmer climates. Tree Physiology 37, 583–592.
| Genetic adaptation and phenotypic plasticity contribute to greater leaf hydraulic tolerance in response to drought in warmer climates.Crossref | GoogleScholarGoogle Scholar |
Booth TH, Broadhurst LM, Pinkard E, Prober SM, Dillon SK, Bush D, Pinyopusarerk K, Doran JC, Ivkovich M, Young AG (2015) Native forests and climate change: lessons from eucalypts. Forest Ecology and Management 347, 18–29.
| Native forests and climate change: lessons from eucalypts.Crossref | GoogleScholarGoogle Scholar |
Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JH, Floyd ML, Belnap J, Anderson JJ, Myers OB, Meyer CW (2005) Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences of the United States of America 102, 15144–15148.
| Regional vegetation die-off in response to global-change-type drought.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Science 177, 245–251.
| Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Cochard H (2009) Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149, 575–584.
| Hydraulic failure defines the recovery and point of death in water-stressed conifers.Crossref | GoogleScholarGoogle Scholar |
Brodribb T, Hill R (1999) The importance of xylem constraints in the distribution of conifer species. New Phytologist 143, 365–372.
| The importance of xylem constraints in the distribution of conifer species.Crossref | GoogleScholarGoogle Scholar |
Brodribb T, Holbrook N (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist 165, 839–846.
| Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (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.
| Conifer species adapt to low-rainfall climates by following one of two divergent pathways.Crossref | GoogleScholarGoogle Scholar |
Brodribb TJ, Skelton RP, Mcadam SAMM, Bienaimé D, Lucani CJ, Marmottant P (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209, 1403–1409.
| Visual quantification of embolism reveals leaf vulnerability to hydraulic failure.Crossref | GoogleScholarGoogle Scholar |
Butt N, Pollock LJ, Mcalpine CA (2013) Eucalypts face increasing climate stress. Ecology and Evolution 3, 5011–5022.
| Eucalypts face increasing climate stress.Crossref | GoogleScholarGoogle Scholar |
Carter JL, White DA (2009) Plasticity in the Huber value contributes to homeostasis in leaf water relations of a mallee eucalypt with variation to groundwater depth. Tree Physiology 29, 1407–1418.
| Plasticity in the Huber value contributes to homeostasis in leaf water relations of a mallee eucalypt with variation to groundwater depth.Crossref | GoogleScholarGoogle Scholar |
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752–755.
| Global convergence in the vulnerability of forests to drought.Crossref | GoogleScholarGoogle Scholar |
Cochard H, Delzon S (2013) Hydraulic failure and repair are not routine in trees. Annals of Forest Science 70, 659–661.
| Hydraulic failure and repair are not routine in trees.Crossref | GoogleScholarGoogle Scholar |
Delzon S, Cochard H (2014) Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytologist 203, 355–358.
| Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin.Crossref | GoogleScholarGoogle Scholar |
Dutkowski G, Potts B (1999) Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification. Australian Journal of Botany 47, 237–263.
| Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification.Crossref | GoogleScholarGoogle Scholar |
Dutkowski GW, Potts BM (2012) Genetic variation in the susceptibility of Eucalyptus globulus to drought damage. Tree Genetics & Genomes 8, 757–773.
| Genetic variation in the susceptibility of Eucalyptus globulus to drought damage.Crossref | GoogleScholarGoogle Scholar |
Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37, 4302–4315.
| WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
Freeman JS, Jackson HD, Steane DA, McKinnon GE, Dutkowski GW, Potts BM, Vaillancourt RE (2001) Chloroplast DNA phylogeography of Eucalyptus globulus. Australian Journal of Botany 49, 585–596.
| Chloroplast DNA phylogeography of Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Givnish TJ, Wong SC, Stuart-Williams H, Holloway-Phillips M, Farquhar GD (2014) Determinants of maximum tree height in Eucalyptus species along a rainfall gradient in Victoria, Australia. Ecology 95, 2991–3007.
| Determinants of maximum tree height in Eucalyptus species along a rainfall gradient in Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao K, et al (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytologist 209, 123–136.
| Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species.Crossref | GoogleScholarGoogle Scholar |
Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, et al (2011) TRY – a global database of plant traits. Global Change Biology 17, 2905–2935.
| TRY – a global database of plant traits.Crossref | GoogleScholarGoogle Scholar |
López R, López de Heredia U, Collada C, Cano FJ, Emerson BC, Cochard H, Gil L, Lo U, Heredia D, Collada C, Cano FJ, Emerson BC, Gil L, López R, López de Heredia U, Collada C, Cano FJ, Emerson BC, Cochard H, Gil L (2013) Vulnerability to cavitation, hydraulic efficiency, growth and survival in an insular pine (Pinus canariensis). Annals of Botany 111, 1167–1179.
| Vulnerability to cavitation, hydraulic efficiency, growth and survival in an insular pine (Pinus canariensis).Crossref | GoogleScholarGoogle Scholar |
Maherali H, DeLucia EH (2000) Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates. Tree Physiology 20, 859–867.
| Xylem conductivity and vulnerability to cavitation of ponderosa pine growing in contrasting climates.Crossref | GoogleScholarGoogle Scholar |
Maherali H, Pockman W, Jackson R (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85, 2184–2199.
| Adaptive variation in the vulnerability of woody plants to xylem cavitation.Crossref | GoogleScholarGoogle Scholar |
Martínez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JF, Llorens P, Nikinmaa E, Nolè A, Poyatos R, Ripullone F, Sass-Klaassen U, Zweifel R (2009) Hydraulic adjustment of Scots pine across Europe. New Phytologist 184, 353–364.
| Hydraulic adjustment of Scots pine across Europe.Crossref | GoogleScholarGoogle Scholar |
Matusick G (2012) Drought and heat triggers sudden and severe dieback in a dominant Mediterranean-type woodland species. Open Journal of Forestry 02, 183–186.
| Drought and heat triggers sudden and severe dieback in a dominant Mediterranean-type woodland species.Crossref | GoogleScholarGoogle Scholar |
McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution 26, 523–532.
| The interdependence of mechanisms underlying climate-driven vegetation mortality.Crossref | GoogleScholarGoogle Scholar |
McKinnon GE, Jordan GJ, Vaillancourt RE, Steane DA, Potts BM (2004) Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philosophical Transactions of the Royal Society of London 359, 275–284, discussion 284.
| Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts.Crossref | GoogleScholarGoogle Scholar |
McLean EH, Prober SM, Stock WD, Steane DA, Potts BM, Vaillancourt RE, Byrne M (2014) Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa. Plant, Cell & Environment 37, 1440–1451.
| Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa.Crossref | GoogleScholarGoogle Scholar |
Mitchell PJ, O’Grady AP, Hayes KR, Pinkard EA (2014) Exposure of trees to drought-induced die-off is defined by a common climatic threshold across different vegetation types. Ecology and Evolution 4, 1088–1101.
| Exposure of trees to drought-induced die-off is defined by a common climatic threshold across different vegetation types.Crossref | GoogleScholarGoogle Scholar |
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.
| Leaf hydraulic capacity and drought vulnerability: possible trade-offs and correlations with climate across three major biomes.Crossref | GoogleScholarGoogle Scholar |
Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees 15, 14–24.
| Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation?Crossref | GoogleScholarGoogle Scholar |
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15, 684–692.
| Plant phenotypic plasticity in a changing climate.Crossref | GoogleScholarGoogle Scholar |
Pfautsch S, Harbusch M, Wesolowski A, Smith R, Macfarlane C, Tjoelker MG, Reich PB, Adams MA (2016) Climate determines vascular traits in the ecologically diverse genus Eucalyptus. Ecology Letters 19, 240–248.
| Climate determines vascular traits in the ecologically diverse genus Eucalyptus.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2011) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 24 October 2018]
Sack L, Holbrook N (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
| Leaf hydraulics.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C, Albuquerque C, Brodersen CR, Townes S V., John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiology
| Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration.Crossref | GoogleScholarGoogle Scholar |
Soudzilovskaia NA, Elumeeva TG, Onipchenko VG, Shidakov II, Salpagarova FS, Khubiev AB, Tekeev DK, Cornelissen JHC (2013) Functional traits predict relationship between plant abundance dynamic and long-term climate warming. Proceedings of the National Academy of Sciences of the United States of America 110, 18180–18184.
| Functional traits predict relationship between plant abundance dynamic and long-term climate warming.Crossref | GoogleScholarGoogle Scholar |
Sperry J, Tyree M (1988) Mechanism of water stress-induced xylem embolism. Plant Physiology 88, 581–587.
| Mechanism of water stress-induced xylem embolism.Crossref | GoogleScholarGoogle Scholar |
Thuiller W, Albert C, Araújo MB, Berry PM, Cabeza M, Guisan A, Hickler T, Midgley GF, Paterson J, Schurr FM, Sykes MT, Zimmermann NE (2008) Predicting global change impacts on plant species’ distributions: future challenges. Perspectives in Plant Ecology, Evolution and Systematics 9, 137–152.
| Predicting global change impacts on plant species’ distributions: future challenges.Crossref | GoogleScholarGoogle Scholar |
Toro MA, Silió L, Rodriguez MC, Soria F, Toval G (1998) Genetic analysis of survival to drought in Eucalyptus globulus in Spain. In ‘Sixth world congress on genetics application to livestock production. Vol. 27’. pp. 499–502. (University of New England: Armidale, NSW)
Tyree MT, Zimmermann MH (2002) ‘Xylem structure and the ascent of sap.’ (Springer: Berlin)
Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: Is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15, 335–360.
| Biophysical perspectives of xylem evolution: Is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction?Crossref | GoogleScholarGoogle Scholar |
Will RE, Wilson SM, Zou CB, Hennessey TC (2013) Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone. New Phytologist 200, 366–374.
| Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone.Crossref | GoogleScholarGoogle Scholar |
Yang Y, Zhu Q, Peng C, Wang H, Chen H (2015) From plant functional types to plant functional traits: a new paradigm in modelling global vegetation dynamics. Progress in Physical Geography 39, 514–535.
| From plant functional types to plant functional traits: a new paradigm in modelling global vegetation dynamics.Crossref | GoogleScholarGoogle Scholar |
Zolfaghar S, Villalobos-Vega R, Cleverly J, Eamus D (2015) Co-ordination among leaf water relations and xylem vulnerability to embolism of Eucalyptus trees growing along a depth-to-groundwater gradient. Tree Physiology 35, 732–743.
| Co-ordination among leaf water relations and xylem vulnerability to embolism of Eucalyptus trees growing along a depth-to-groundwater gradient.Crossref | GoogleScholarGoogle Scholar |
