Reduced transpiration response to precipitation pulses precedes mortality in a piñon-juniper woodland subject to prolonged drought

New Phytologist

Volumn 200, Issue 2, 2013, Pages 375-387

  Plaut, Jennifer A ^a   Wadsworth, W Duncan ^b   Pangle, Robert ^a   Yepez, Enrico A ^c   Mcdowell, Nate G ^d   Pockman, William T ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b Rice University   (United States)

^c INSTITUTO TECNOLÓGICO DE SONORA   (Mexico)

^d LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

Carbon starvation; Die off; Hydraulic conductance; Hydraulic failure; Mixed effects model; Semi arid

Indexed keywords

ANTECEDENT CONDITIONS; CARBON; CLIMATE CHANGE; DROUGHT; GLOBAL CLIMATE; IRRIGATION; MORTALITY; ROOT; SOIL MOISTURE; STARVATION; SURVIVAL; TRANSPIRATION; VEGETATION; WOODLAND;

JUNIPERUS; JUNIPERUS MONOSPERMA; PINUS EDULIS; TILLANDSIA LINEATISPICA;

CARBON; RAIN;

ARTICLE; CARBON STARVATION; DIE-OFF; DROUGHT; ECOSYSTEM; EVAPOTRANSPIRATION; HYDRAULIC CONDUCTIVITY; HYDRAULIC FAILURE; IRRIGATION (AGRICULTURE); JUNIPERUS; METABOLISM; MIXED EFFECTS MODEL; PHYSIOLOGY; PINE; SEMI-ARID; SOIL; THEORETICAL MODEL; TREE; UNITED STATES; VAPOR PRESSURE;

CARBON STARVATION; DIE-OFF; HYDRAULIC CONDUCTANCE; HYDRAULIC FAILURE; MIXED EFFECTS MODEL; SEMI-ARID;

AGRICULTURAL IRRIGATION; CARBON; DROUGHTS; ECOSYSTEM; JUNIPERUS; MODELS, THEORETICAL; NEW MEXICO; PINUS; PLANT TRANSPIRATION; RAIN; SOIL; TREES; VAPOR PRESSURE;

EID: 84884415307     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12392     Document Type: Article

References (78)

1. 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, USA 106: 7063-7066.
2. Adams HD, Macalady AK, Breshears DD, Allen CD, Stephenson NL, Saleska SR, Huxman TE, McDowell NG. 2010. Climate induced tree mortality: earth system consequences. EOS Transactions, AGU 91: 153-154.
3. Allen CD, Macalady A, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Gonzales P, Hogg T, Rigling A, Breshears D et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259: 660-684.
4. Allison I, Bindoff NL, Bindschadler RA, Cox PM, de Noblet N, England MH, Francis JE, Gruber N, Haywood AM, Karoly DJ et al. 2009. The Copenhagen Diagnosis, 2009: updating the World on the latest climate science. Sydney, NSW, Australia: The University of New South Wales Climate Change Research Centre.
5. Anderegg WRL, Plavcová L, Anderegg LDL, Hacke UG, Berry JA, Field CB. 2013. Drought's legacy: multi-year hydraulic deterioration underlies widespread aspen die-off and portends increased future risk. Global Change Biology 91: 1188-1196.
6. Balling RC Jr, Goodrich GB. 2010. Increasing drought in the American Southwest? A continental perspective using a spatial analytical evaluation of recent trends. Physical Geography 31: 293-306.
7. Bates D, Maechler M, Bolker B. 2012. lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0. http://CRAN.R-project.org/package=lme4
8. Blackman CJ, Brodribb TJ, Jordan GJ. 2009. Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant, Cell & Environment 32: 1584-1595.
9. Bonan GB. 2008. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320: 1444-1449.
10. Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT. 2009. Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Frontiers in Ecology and the Environment 7: 185-189.
11. 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 Phytologist 188: 533-542.
12. Brodribb TJ, Cochard H. 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149: 575-584.
13. Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDSL. 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 & Environment 26: 1633-1645.
14. Burgess SSO. 2006. Measuring transpiration responses to summer precipitation in a Mediterranean climate: a simple screening tool for identifying plant water-use strategies. Physiologia Plantarum 127: 404-412.
15. Bush SE, Hultine KR, Sperry JS, Ehleringer JR. 2010. Calibration of thermal dissipation sap flow probes for ring- and diffuse-porous trees. Tree Physiology 30: 1545-1554.
16. Clearwater MJ, Meinzer FC, Andrade JL, Goldstein G, Holbrook NM. 1999. Potential errors in measurement of nonuniform sap flow using heat dissipation probes. Tree Physiology 19: 681-687.
17. Cohen Y, Cohen S, Cantuarias-Aviles T, Schiller G. 2008. Variations in the radial gradient of sap velocity in trunks of forest and fruit trees. Plant and Soil 305: 49-59.
18. Cook BI, Seager R. 2013. The response of the North American Monsoon to increased greenhouse gas forcing. Journal of Geophysical Research: Atmospheres 118: 1690-1699.
19. Dai A. 2013. Increasing drought under global warming in observations and models. Nature Climate Change 3: 52-58.
20. 2 concentration. Tree Physiology 30: 1001-1015.
21. 2 uptake in grass and shrub plant communities on Walnut Gulch Experimental Watershed. Water Resources Research, 44: W05S16.
22. Fisher R, McDowell NG, Purves D, Moorcroft P, Sitch S, Cox P, Huntingford C, Meir P, Woodward FI. 2010. Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. New Phytologist 187: 666-681.
23. Galiano L, Martínez-Vilalta J, Sabaté S, Lloret F. 2012. Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean holm oak forest. Tree Physiology 32: 478-489.
24. Gallé A, Haldimann P, Feller U. 2007. Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytologist 174: 799-810.
25. Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, Pangle RE, McDowell NG. 2013. Drought causes predisposition to insect attacks and mortality of piñon-juniper woodlands. New Phytologist 198: 567-578.
26. Gelman A, Hill J. 2007. Data analysis using regression and multilevel/hierarchical models. New York, NY, USA: Cambridge University Press.
27. Goulden ML, Field CB. 1994. Three methods for monitoring the gas exchange of individual tree canopies - ventilated- chamber, sap-flow and Penman-Monteith measurements on evergreen oaks. Functional Ecology 8: 125-135.
28. Granier A. 1987. Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. Tree Physiology 3: 309-319.
29. Heisler-White JL, Blair JM, Kelly EF, Harmoney K, Knapp AK. 2009. Contingent productivity responses to more extreme rainfall regimes across a grassland biome. Global Change Biology 15: 2894-2904.
30. Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Snadquist DR, Potts DL, Schwinning S. 2004. Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141: 254-268.
31. Jackson RB, Randerson JT, Canadell JG, Anderson RG, Avissar R, Baldocchi DD, Bonan GB, Caldeira K, Diffenbaugh NS, Field CB et al. 2008. Protecting climate with forests. Environmental Research Letters 3: article number 044006.
32. Knapp AK, Beier C, Briske DD, Classen AT, Luo Y, Reichstein M, Smith MD, Smith SD, Bell JE, Fay PA et al. 2008. Consequences of more extreme precipitation regimes for terrestrial ecosystems. BioScience 58: 811-821.
33. Leuzinger S, Bigler C, Wolf A, Körner C. 2009. Poor methodology for predicting large-scale tree die-off. Proceedings of the National Academy of Sciences, USA 106: E106; author reply E107.
34. Limousin J-M, Bickford CP, Dickman LT, Pangle RE, Hudson PJ, Boutz AL, Gehres N, Osuna JL, Pockman WT, McDowell NG. 2013. Regulation and acclimation of leaf gas exchange in a piñon-juniper woodland exposed to three different precipitation regimes. Plant, Cell & Environment. doi: 10.1111/pce.12089.
35. Limousin J-M, Rambal S, Ourcival JM, Rocheteau A, Joffre R, Rodriguez-Cortina R. 2009. Long-term transpiration change with rainfall decline in a Mediterranean Quercus ilex forest. Global Change Biology 15: 2163-2175.
36. Linton MJ, Sperry JS, Williams DG. 1998. Limits to water transport in Juniperus osteosperma and Pinus edulis: implications for drought tolerance and regulation of transpiration. Functional Ecology 12: 906-911.
37. Lo Gullo MA, Nardini A, Trifilò P, Salleo S. 2003. Changes in leaf hydraulics and stomatal conductance following drought stress and irrigation in Ceratonia siliqua (Carob tree). Physiologia Plantarum 117: 186-194.
38. Loik ME, Breshears DD, Lauenroth WK, Belnap J. 2004. A multi-scale perspective of water pulses in dryland ecosystems: climatology and ecohydrology of the western USA. Oecologia 141: 269-281.
39. McDowell NG. 2011. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155: 1051-1059.
40. McDowell NG, Beerling D, Breshears D, Fisher R, Raffa K, Stitt M. 2011. Interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology and Evolution 26: 523-532.
41. McDowell NG, Sevanto S. 2010. The mechanisms of carbon starvation: how, when, or does it even occur at all? New Phytologist 186: 264-266.
42. 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. Functional Ecology 23: 922-930.
43. Mildrexler DJ, Zhao M, Running SW. 2011. A global comparison between station air temperatures and MODIS land surface temperatures reveals the cooling role of forests. Journal of Geophysical Research 116: G03025.
44. Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SSO. 2008. Using multiple trait associations to define hydraulic functional types in plant communities of south-western Australia. Oecologia 158: 385-397.
45. Notaro M, Gutzler D. 2012. Simulated impact of vegetation on climate across the North American monsoon region in CCSM3.5. Climate Dynamics 38: 795-814.
46. Notaro M, Mauss A, Williams J. 2012. Projected vegetation changes for the American Southwest: combined dynamic modeling and bioclimatic-envelope approach. Ecological Applications 22: 1365-1388.
47. Noy-Meir I. 1973. Desert ecosystems: environment and producers. Annual Review of Ecology and Systematics 4: 25-51.
48. Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG et al. 2011. A large and persistent carbon sink in the World's forests. Science 333: 988-993.
49. Pangle RE, Hill JP, Plaut JA, Yepez EA, Elliot JR, Gehres N, McDowell NG, Pockman WT. 2012. Methodology and performance of a rainfall manipulation experiment in a piñon-juniper woodland. Ecosphere 3: 28.
50. Pinheiro JC, Bates DM. 2000. Mixed-effects models in S and S-PLUS. New York, NY, USA: Springer.
51. Plaut JA, Yepez EA, Hill J, Pangle R, Sperry JS, Pockman WT, McDowell NG. 2012. Hydraulic limits preceding mortality in a piñon-juniper woodland under experimental drought. Plant, Cell & Environment 35: 1601-1617.
52. R Core Team. 2012. R: a language and environment for statistical computing. Vienna, Austria. R Foundation for Statistical Computing.
53. 3 woody legume, Prosopis velutina. New Phytologist 181: 672-682.
54. Reynolds JF, Kemp PR, Ogle K, Fernández RJ. 2004. Modifying the 'pulse-reserve' paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141: 194-210.
55. Ross I, Misson L, Rambal S, Arneth A, Scott RL, Carrara A, Cescatti A, Genesio L. 2012. How do variations in the temporal distribution of rainfall events affect ecosystem fluxes in seasonall water-limited Northern Hemisphere shrublands and forests? Biogeosciences 9: 1007-1024.
56. Royer PD, Cobb NS, Clifford MJ, Huang C-Y, Breshears DD, Adams HD, Villegas JC. 2011. Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. Journal of Ecology 99: 714-723.
57. Ruff TW, Kushnir Y, Seager R. 2012. Comparing twentieth- and twenty-first-century patterns of interannual precipitation variability over the western United States and northern Mexico. Journal of Hydrometeorology 13: 366-378.
58. Sala A. 2009. Lack of direct evidence for the carbon-starvation hypothesis to explain drought-induced mortality in trees. Proceedings of the National Academy of Sciences, USA 106: E68; author reply E69.
59. Sala A, Piper F, Hoch G. 2010. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist 186: 274-281.
60. Sala A, Woodruff DR, Meinzer FC. 2012. Carbon dynamics in trees: feast or famine? Tree Physiology 32: 764-775.
61. Salleo S, Trifilo P, Esposito S, Nardini A, LoGullo M. 2009. Starch-to- sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Functional Plant Biology 36: 815-825.
62. Schuldt B, Leuschner C, Horna V, Moser G, Köhler M, van Straaten O, Barus H. 2011. Change in hydraulic properties and leaf traits in a tall rainforest tree species subjected to long-term throughfall exclusion in the perhumid tropics. Biogeosciences 8: 2179-2194.
63. Seager R, Ting M, Li C, Naik N, Cook B, Nakamura J, Liu H. 2012. Projections of declining surface-water availability for the southwestern United States. Nature Climate Change 3: 482-486.
64. st century hydroclimate of southwestern North America. Proceedings of the National Academy of Sciences, USA 107: 21277-21282.
65. Sheffield J, Wood E, Roderick M. 2012. Little change in global drought over the past 60 years. Nature 491: 435-438.
66. Taylor CM, de Jeu RAM, Guichard F, Harris P, Dorigo W. 2012. Afternoon rain more likely over drier soils. Nature 489: 423-426.
67. Thomey ML, Collins SL, Vargas R, Johnson JE, Brown RF, Natvig DO, Friggens MT. 2011. Effect of precipitation variability on net primary production and soil respiration in a Chihuahuan Desert grassland. Global Change Biology 17: 1505-1515.
68. Trifilò P, Raimondo F, Nardini A, Lo Gullo MA, Salleo S. 2004. Drought resistance of Ailanthus altissima: root hydraulics and water relations. Tree Physiology 24: 107-114.
69. 2 emissions from forests. Nature Geoscience 2: 737-738.
70. West AG, Hultine KR, Burtch KG, Ehleringer JR. 2007a. Seasonal variations in moisture use in a piñon-juniper woodland. Oecologia 153: 787-798.
71. West AG, Hultine KR, Jackson TL, Ehleringer JR. 2007b. Differential summer water use by Pinus edulis and Juniperus osteosperma reflects contrasting hydraulic characteristics. Tree Physiology 27: 1711-1720.
72. West AG, Hultine KR, Sperry JS, Bush SE, Ehleringer JR. 2008. Transpiration and hydraulic strategies in a piñon-juniper woodland. Ecological Applications 18: 911-927.
73. Williams AP, Allen CD, Macalady AK, Griffin D, Woodhouse CA, Meko DM, Swetnam TW, Rauscher SA, Seager R, Grissino-Mayer HD et al. 2012. Temperature as a potent driver of regional forest drought stress and tree mortality. Nature Climate Change 3: 292-297.
74. Williams DG, Ehleringer JR. 2000. Intra- and interspecific variation for summer precipitation use in pinyon-juniper woodlands. Ecological Monographs 70: 517-537.
75. Yan S, Wan C, Sosebee RE, Wester DB, Fish EB, Zartman RE. 2000. Responses of photosynthesis and water relations to rainfall in the desert shrub creosote bush (Larrea tridentata) as influenced by municipal biosolids. Journal of Arid Environments 46: 397-412.
76. Yaseef NR, Yakir D, Rotenberg E, Schiller G, Cohen S. 2010. Ecohydrology of a semi-arid forest: partitioning among water balance components and its implications for predicted precipitation changes. Ecohydrology 3: 143-154.
77. Zeppel M, Macinnis-Ng CMO, Ford C, Eamus D. 2008. The response of sap flow to pulses of rain in a temperate Australian woodland. Plant and Soil 305: 121-130.
78. Zwieniecki MA, Holbrook NM. 2009. Confronting Maxwell's demon: biophysics of xylem embolism repair. Trends in Plant Science 14: 530-534.