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Strong hydraulic segmentation and leaf senescence due to dehydration may trigger die-back in Nothofagus dombeyi under severe droughts: a comparison with the co-occurring Austrocedrus chilensis

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Total leaf hydraulic dysfunction during severe drought could lead to die-back in N. dombeyi , while hydraulic traits of A. chilensis allow it to operate far from the threshold of total hydraulic failure.

Abstract

Die-back was observed in South America temperate forests during one of the most severe droughts of the 20th century (1998–1999). During this drought Austrocedrus chilensis trees survived, whereas trees of the co-occurring species (Nothofagus dombeyi) experienced symptoms of water stress, such as leaf wilting and abscission, before tree die-back occurred. We compared hydraulic traits of these two species (a conifer and an angiosperm species, respectively) in a forest stand located close to the region with records of N. dombeyi mass mortality. We asked whether different hydraulic traits exhibited by the two species could help explain their contrasting survivorship rates. Austrocedrus chilensis had wide leaf safety margins, which appear to be the consequence of relatively high leaf-and-stem capacitance, large stored water use, strong stomatal control and ability to recover from embolism-induced loss of leaf hydraulic capacity. On the other hand, N. dombeyi even though had a stem hydraulic threshold of −6.7 MPa before reaching substantial hydraulic failure (P88), leaf P88 occurred at leaf water potentials of only −2 MPa, which probably are reached during anomalous droughts. Massive mortality in N. dombeyi appears to be the result of the total loss of leaf hydraulic conductance leading to leaf dehydration and leaf drop. Drought occurs during the summer and it is highly likely that N. dombeyi cannot recover its photosynthetic surface to produce carbohydrates required to avoid tissue injury in the winter season with subfreezing temperatures. Strong hydraulic segmentation in N. dombeyi does not seem to have an adaptive value to survive severe droughts.

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References

  • Adams HD, Germino MJ, Breshears DD, Barron-Gafford GA, Guardiola-Claramonte M, Zou CB, Huxman TE (2013) Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol 197(1142):1151. doi:10.1111/nph.12102

    Google Scholar 

  • Alberdi M (1987) Ecofisiología de especies chilenas del género. Nothofagus Bosque 8:77–84

    Google Scholar 

  • Allen C, Alison K, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears D, Hogg E, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J, Allard G, Running S, Semerci A, Cobb B (2010) A global overview of drought and heat-induced tree mortality reveals emerging change risks for forests. Forest Ecol Manage 259:660–684

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109:233–237

    Article  Google Scholar 

  • Barigah ST, Charrier O, Douris M, Bonhomme M, Herbette S, Ameglio T, Fichot R, Brignolas F, Cochard H (2013) Water stress-induced xylem hydraulic failure is a causal factor of tree mortality in beech and poplar. Ann Bot 112:1431–1437

    Article  PubMed  Google Scholar 

  • Barnard DM, Meinzer FC, Lachenbruch B, McCulloh KA, Johnson DM, Woodruff DR (2011) Climate-related trends in sapwood biophysical properties in two conifers: avoidance of hydraulic dysfunction through coordinated adjustments in xylem efficiency, safety and capacitance. Plant Cell Environ 34:643–654

    Article  PubMed  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 

  • Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JH, Floyd ML, Belnap J et al (2005) Regional vegetation die-off in response to global-change-type drought. Proc Natl Acad Sci USA 102:15144–15148

    Article  PubMed  CAS  PubMed Central  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  PubMed Central  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  PubMed Central  Google Scholar 

  • Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846

    Article  PubMed  Google Scholar 

  • Brodribb TJ, Bowman DJMS, Nichols S, Delzon S, Burlett R (2010) Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol 188:533–542

    Article  PubMed  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg SL (2003) Dynamic changes in hydraulic conductivity in petioles of two savannas tree species: factors and mechanisms contributing to the refilling to embolized vessels. Plant Cell Environ 26:1633–1645

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Zhang Y, Hao G-Y (2008) Water relations and hydraulic architecture in Cerrado trees: adjustments to seasonal changes in water availability and evaporative demand. Braz J Plant Physiol 20:233–245

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Campanello PI, Montti L, Jimenez M, La Manna L, Rockwell A, Guerra P, Lopez-Bernal P, Troncoso O, Holbrook MN, Goldsein G (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiol 32:880–892

    Article  PubMed  Google Scholar 

  • Bucci SJ, Scholz FG, Peschiutta ML, Arias N, Meinzer FC, 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 Environ 36:2163–2174

    Article  PubMed  CAS  Google Scholar 

  • Carnicer J, Barbeta A, Sperlich D, Coll M, Peñuelas J (2013) Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale. Front Plant Sci 4:409. doi:10.3389/fpls.2013.00409

    Article  PubMed  PubMed Central  Google Scholar 

  • Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Jacobsen AL, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne A (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–756

    PubMed  CAS  Google Scholar 

  • Coll M, Peñuelas J, Ninyerola M, Pons X, Carnicer J (2013) Multivariate effect gradients driving forest demographic responses in the Iberian Peninsula. For Ecol Manage 303:195–209

    Article  Google Scholar 

  • Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis, Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on climate change. Cambridge University Press, New York

    Google Scholar 

  • Do F, Rocheteau A (2002) Influence of natural temperature gradients on measurements of xylem sap flow with thermal dissipation probes. 2. Advantages and calibration of a noncontinuous heating system. Tree Physiol 22:649–654

    Article  PubMed  CAS  Google Scholar 

  • Domec J-C, Gartner BL (2001) Cavitation and water storage capacity in bole xylem segments of mature and young Douglas-®r trees. Trees 15:204–214

    Article  Google Scholar 

  • Fajardo A, Piper FI, Hoch G (2013) Similar variation in carbon storage between deciduous and evergreen treeline species across elevational gradients. Ann Bot 112:623–631

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson P, Celis A (1998) Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant, Cell Environ 21:397–406

    Article  Google Scholar 

  • Gómez-Aparicio L, Garcia Valdes R, Ruiz-Benito P, Zavala MA (2011) Disentangling the relative importance of climate, size and competition on tree growth in Iberian forests: implications for forest management under global change. Glob Change Biol 17:2400–2414

    Article  Google Scholar 

  • Granier A (1985) Une nouvelle méthode pour la mesure du flux de séve brute dans le tronc des arbres. Ann Sci For 42:193–200

    Article  Google Scholar 

  • Granier A (1987) Evaluation of transpiration in a Douglas fir stand by means of sap flow measurement. Tree Physiol 3:309–320

    Article  PubMed  Google Scholar 

  • Greslebin AG, Hansen EM, Winton L, Rajchenberg M (2005) Phytophthora species from declining Austrocedrus chilensis forests in Patagonia, Argentina. Mycologia 97:218–228

    Article  PubMed  Google Scholar 

  • Gyenge JE, Fernández ME, Schlichter T (2007) Influence of radiation and drought on gas exchange of Austrocedrus chilensis seedlings. BOSQUE 28:220–225

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh K (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 G-W, Hoffmann WA, Scholz FG, Bucci SJ, Meinzer FC, Franco AC, Cao K-F, Goldstein G (2008) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155:405–415

    Article  PubMed  Google Scholar 

  • Hartmann H, Ziegler W, Kolle O, Trumbore S (2013) Thirst beats hunger declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200:340–349

    Article  PubMed  CAS  Google Scholar 

  • Jiménez-Castillo M, Lobos-Catalán P, Aguilera-Betti I, Rivera R (2011) Tasas diarias de transpiración y relaciones hídricas en especies arbóreas con distinto nivel de sombra tolerancia en un bosque templado chileno. Gayana Botánica 68:155–162

    Article  Google Scholar 

  • Johnson DM, Woodruff DR, McCulloh KA, Meinzer FC (2009) 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 

  • Johnson DM, McCulloh KA, Meinzer FC, Woodruff DR (2011) Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species. Tree Physiol 31:659–668

    Article  PubMed  CAS  Google Scholar 

  • La Manna L, Rajchenberg M (2004) The decline of Austrocedrus chilensis forests in Patagonia, Argentina: soil features as predisposing factors. For Ecol Manage 190:345–357

    Article  Google Scholar 

  • Larjavaara M, Muller-Landau HC (2010) Rethinking the value of high wood density. Funct Ecol 24:701–705

    Article  Google Scholar 

  • Martínez-Ferri E, Balaguer L, Valladares F, Chico JM, Manrique E (2000) Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer. Tree Physiol 20:131–138

    Article  PubMed  Google Scholar 

  • McCulloh KA, Johnson D, Meinzer FC, Woodruff DR (2013) The dynamic pipeline: hydraulic capacitance and xylem hydraulic safety in four tall conifer species Plant Cell Environ doi: 10.1111/pce.12225

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532

    Article  PubMed  Google Scholar 

  • Meinzer FC, James SA, Goldstein G, Woodruff DR (2003) Whole-tree water transport scales with sapwood capacitance in tropical forest canopy trees. Plant Cell Environ 26:1147–1155

    Article  Google Scholar 

  • Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23:922–930

    Article  Google Scholar 

  • Mundo IA, El Mujtar VA, Perdomo MH, Gallo LA, Villalba R, Barrera MD (2010) Austrocedrus chilensis growth decline in relation to drought events in Northern Patagonia, Argentina. Trees 24:561–570

    Article  Google Scholar 

  • Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Sci 180:604–611

    Article  PubMed  CAS  Google Scholar 

  • Pfautsch S, Peri PL, Macfarlane C, van Ogtrop F, Adams MA (2014) Relating water use to morphology and environment of Nothofagus from the world’s most southern forests. Trees 28:125–136

    Article  Google Scholar 

  • Plaut JA, Wadsworth WD, Pangle R, Yepez EA, McDowell NG, Pockman WT (2013) Reduced transpiration response to precipitation pulses precedes mortality in a pinon–juniper woodland subject to prolonged drought. New Phytol 200:375–387

    Article  PubMed  Google Scholar 

  • Poyatos R, Aguade D, Galiano L, Mencuccini M, Martınez-Vilalta J (2013) Drought-induced defoliation and long periods of near-zero gas exchange play a key role in accentuating metabolic decline of Scots pine. New Phytol 200:388–401

    Article  PubMed  CAS  Google Scholar 

  • Pratt RB, Jacobsen A, Ewers FW, Davis SD (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

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Díaz M, Alberdi M, Piper F, Bravo LA, Corcuera LJ (2005) Low temperature responses of Nothofagus dombeyi and Nothofagus nitida, two evergreen species from south central Chile. Tree Physiol 25:1389–1398

    Article  PubMed  Google Scholar 

  • Richards AE, Wright IJ, Lenz TI, Zanne AE (2013) Sapwood capacitance is greater in evergreen sclerophyll species growing in high compared to low-rainfall environments. Funct Ecol doi: 10.1111/1365-2435.12193

  • Riveros M, Perez M, Baez P, Baez A (2003) Resource allocation dynamics preceding flowering in species of the genus Nothofagus. Bosque 24:85–95

    Article  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 

  • Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281

    Article  PubMed  Google Scholar 

  • Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775

    Article  PubMed  CAS  Google Scholar 

  • Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2007) Biophysical properties and functional significance of stem water storage tissues in neo-tropical savanna trees. Plant Cell Environ 30:236–248

    Article  PubMed  Google Scholar 

  • Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Salazar A (2008) Plant-and Stand level variation in biophysical and physiological traits along tree density gradients in the Cerrado. Braz J Plant Physiol 20:217–232

    Article  Google Scholar 

  • Scholz FG, Phillips NG, Bucci SJ, Meinzer FC, Goldstein G (2011) Hydraulic capacitance. In: Meinzer FC et al. (eds) Biophysics and functional significance of internal water sources in relation to tree size in size- and age-related changes in tree structure and function Vol. 4 Springer 341–361

  • Suarez ML, Kitzberger T (2008) Recruitment patterns following a severe drought: long-term compositional shifts in Patagonian forests. Can J For Res 38:3002–3010

    Article  Google Scholar 

  • Suarez ML, Kitzberger T (2010) Differential effects of climate variability on forest dynamics along a precipitation gradient in northern Patagonia. J Ecol 98:1023–1034

    Article  Google Scholar 

  • Suarez ML, Ghermandi L, Kitzberger T (2004) Factors predisposing episodic drought-induced tree mortality in Nothofagus: site, climatic sensitivity and growth trends. J Ecol 92:954–966

    Article  Google Scholar 

  • Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Urli M, Porte AJ, Cochard H, Guengant Y, Burlett R, Delzon S (2013) Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiol 33:672–683

    Article  PubMed  CAS  Google Scholar 

  • Velez ML, Silva PV, Troncoso OA, Greslebin AG (2012) Alteration of physiological parameters of Austrocedrus chilensis by the pathogen Phytophthora austrocedrae. Plant Physiol 61:877–888

    Google Scholar 

  • Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ 36:1938–1949

    PubMed  CAS  Google Scholar 

  • Zúñiga R, Alberdi M, Reyes-Díaz M, Olivares O, Hess S, Bravo LA, Corcuera LJ (2006) Seasonal changes in the photosynthetic performance of two evergreen Nothofagus species in south central Chile. Revista Chilena de Historia Natural 79:489–504

    Article  Google Scholar 

  • Zwieniecki MA, Holbrook NM (1998) Short term changes in xylem water conductivity in white ash, red maple and Sitka spruce. Plant Cell Environ 21:1173–1180

    Article  Google Scholar 

  • Zwieniecki MA, Holbrook MN (2009) Confronting Maxwell’s demon: biophysics of xylem embolism repair. Trends Plant Sci 14:530–534

    Article  PubMed  CAS  Google Scholar 

  • Zwieniecki MA, Brodribb TJ, Holbrook MN (2007) Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environ 30:910–921

    Article  PubMed  Google Scholar 

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Author contribution statement

FG Scholz, SJ Bucci and G Goldstein designed the study, collected and analyzed the data and wrote the manuscript.

Acknowledgments

This study was supported by CONICET grant (PIP 112-200801-01703) and Anpcyt grants (PICT 2008-1202, PICT 2010-960, PICT 2012-2344). We thank to Oyarzo family for permission to access the study area and for logistic support, and we are grateful to Sean Gleason and other anonymous reviewers for their comments to improve the manuscript. This work complies with Argentinean Law.

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Authors have not conflict of interest

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Authors and Affiliations

  1. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Fabián G. Scholz, Sandra J. Bucci & Guillermo Goldstein

  2. Grupo de Estudios Biofísicos y Eco-fisiológicos (GEBEF), Departamento de Biología, Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, Comodoro Rivadavia, Argentina

    Fabián G. Scholz & Sandra J. Bucci

  3. Laboratorio de Ecología Funcional (LEF), Departamento de Ecología, Genética y Evolución, FCEyN, Universidad de Buenos Aires, Buenos Aires, Argentina

    Guillermo Goldstein

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  1. Fabián G. Scholz
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  3. Guillermo Goldstein
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Correspondence to Fabián G. Scholz.

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Communicated by A. C. Franco.

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Scholz, F.G., Bucci, S.J. & Goldstein, G. Strong hydraulic segmentation and leaf senescence due to dehydration may trigger die-back in Nothofagus dombeyi under severe droughts: a comparison with the co-occurring Austrocedrus chilensis . Trees 28, 1475–1487 (2014). https://doi.org/10.1007/s00468-014-1050-x

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