Increased water-use efficiency during the 20th century did not translate into enhanced tree growth

Global Ecology and Biogeography

Volumn 20, Issue 4, 2011, Pages 597-608

  Peñuelas, Josep ^a   Canadell, Josep G ^b   Ogaya, Romà ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b CSIRO   (Australia)

Author keywords

13C; Climate change; CO2 fertilization; Drought; Forest; Geographical range; Tree growth; Water use efficiency

Indexed keywords

BIOME; CARBON DIOXIDE; CARBON ISOTOPE; CLIMATE CHANGE; CLIMATE MODELING; DROUGHT; GEOGRAPHICAL DISTRIBUTION; GLOBAL PERSPECTIVE; GROWTH RATE; GROWTH RESPONSE; TWENTIETH CENTURY; WATER USE EFFICIENCY;

EID: 79958136803     PISSN: 1466822X     EISSN: 14668238     Source Type: Journal    
DOI: 10.1111/j.1466-8238.2010.00608.x     Document Type: Article

References (109)

1. Allen, C.D., Macalady, A.K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D.D., Hogg, E.H., González, P., Fensham, R., Zhang, Z., Castro, J., Demidova, N., Lim, J.H., Allard, G., Running, S.W., Semerci, A. & Cobb, N. (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.
2. 13C in a Spanish pine forest network. Tellus, 60, 771-781.
3. Atkin, O.K., Bruhn, D., Hurry, V.M. & Tjoelker, M.G. (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology, 32, 87-105.
4. Barber, V.A., Juday, G.P. & Finney, B.P. (2000) Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress. Nature, 405, 668-673.
5. 13C and water-use efficiency of Abies alba (Mill.) during the last century. Ecology, 78, 1588-1596.
6. 2 degassing at Mammoth Mountain, California. Ecology, 80, 2420-2426.
7. 2-controlled mechanism of woody plant invasion in grasslands and savannas. Global Change Biology, 6, 865-869.
8. 2 and fire in promoting the spread of grasslands and savannas. Global Change Biology, 9, 973-982.
9. Boonstra, R., Desantis, L., Krebs, C.J. & Hik, D.S. (2008) Climate and nutrient influences on the growth of white spruce trees in the boreal forests of the Yukon. Climate Research, 36, 123-130.
10. Borgaonkar, H.P., Sikder, A.B., Ram, S. & Pant, G.B. (2010) El Niño and related monsoon drought signals in 523-year-long ring width records of teak (Tectona grandis L.F.) trees from south India. Palaeogeography, Palaeoclimatology, Palaeoecology, 285, 74-84.
11. Brookhouse, M., Lindesay, J. & Brack, C. (2008) The potential of tree rings in Eucalyptus pauciflora for climatological and hydrological reconstruction. Geophysical Research, 46, 421-434.
12. 2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences USA, 104, 18866-18870.
13. Canadell, J.G., Pataki, D., Gifford, R., Houghton, R.A., Luo, Y., Raupach, M.R., Smith, P. & Steffen, W. (2007b) Saturation of the terrestrial carbon sink. Terrestrial ecosystems in a changing world (ed. by J.G. Canadell, D. Pataki and L. Pitelka), pp. 59-78. Springer-Verlag, Berlin Heidelberg.
14. Cao, M. & Woodward, F.I. (1998) Dynamic responses of terrestrial ecosystem carbon cycling to global climate change. Nature, 393, 249-252.
15. Cook, E.R. & Kairiukstis, L.A. (1990) Methods of dendrochronology applications in the environmental sciences. Kluwer Academy Publishers, Dordrecht, The Netherlands.
16. Denman, K.L., Chidthaisong, G.B.A., Ciais, P. etal. (2007) Couplings between changes in the climate system and biogeochemistry. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (ed. by S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, H.L. Miller etal.), pp. 499-587. Cambridge University Press, Cambridge.
17. 2 enrichment) and N-fertilization. Plant Cell and Environment, 32, 1500-1512.
18. Duquesnay, A., Breda, N., Stievenard, M. & Dupouey, J.L. (1998) Changes of tree-ring delta C-13 and water use efficiency of beech (Fagus sylvatica L.) in north-eastern France during the past century. Plant Cell and Environment, 21, 565-572.
19. 4 grass community. Global Change Biology, 11, 1968-1981.
20. 2 concentrations in plants. Tree Physiology, 15, 105-111.
21. Farquhar, G.D. & Richards, R.A. (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology, 11, 539-552.
22. 2 assimilation in leaves of C3 species. Planta, 149, 78-90.
23. Farquhar, G.D., O'Leary, M.H. & Berry, J.A. (1982) On the relationship between carbon isotope discrimination and intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology, 9, 121-137.
24. 2 concentrations. Geochimica et Cosmochimica Acta, 63, 1891-1903.
25. 2 concentration. Geochimica et Cosmochimica Acta, 59, 2599-2608.
26. Fischlin, A., Midgley, G.F., Price, J.T., Leemans, R., Gopal, B., Turley, C., Rounsevell, M.D.A., Dube, O.P., Tarazona, J. & Velichko, A.A. (2007) Ecosystems, their properties, goods, and services. Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (ed. by M.L. Parry, O.F. Canziani, J.P. Palutikof, P.J. van der Linden and C.E. Hanson), pp. 211-272. Cambridge University Press, Cambridge.
27. Fowler, A.M., Palmer, J. & Fenwick, P. (2008) An assessment of the potential for centennial-scale reconstruction of atmospheric circulation from selected New Zealand tree-ring chronologies. Palaeogeography, Palaeoclimatology, Palaeoecology, 265, 238-254.
28. Friedlingstein, P., Cox, P., Betts, R. etal. (2006) Climate-carbon cycle feedback analysis. Results from the C4MIP model intercomparison. Journal of Climate, 19, 3337-3353.
29. 13C series from Pinus sylvestris in northern Fennoscandia contain long-term non-climatic trends? Chemical Geology, 252, 42-51.
30. Gebrekirstos, A., Mitlöhner, R., Teketay, D. & Worbes, M. (2008) Climate-growth relationships of the dominant tree species from semi-arid savanna woodland in Ethiopia. Trees, 22, 631-641.
31. Girardin, M.P., Raulier, F., Bernier, P.Y. & Tardif, J.C. (2008) Response of tree growth to a changing climate in boreal central Canada: a comparison of empirical, process-based, and hybrid modelling approaches. Ecological Modelling, 213, 209-228.
32. 2 - from simple regularities to biogeographic chaos. Ecological Modelling, 200, 433-451.
33. 2: a model for future forest responses? Global Change Biology, 3, 463-471.
34. Heinrich, I., Weidner, K., Helle, G., Vos, H., Lindesay, J. & Banks, J.C.G. (2009) Interdecadal modulation of the relationship between ENSO, IPO and precipitation: insights from tree rings in Australia. Climate Dynamics, 33, 63-73.
35. 13C and water-use efficiency of tropical Cedrela and Swietenia from Brazil. Tree Physiology, 25, 745-752.
36. Hughes, L. (2000) Biological consequences of global warming: is the signal already apparent? Trends in Ecology and Evolution, 15, 56-61.
37. 2 enrichment in a scrub oak woodland. Ecology, 87, 26-40.
38. IPCC (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, H.L. Miller etal. (eds) Cambridge University Press, Cambridge, UK.
39. Ivlev, A.A. & Voronin, V.I. (2007) The mechanism of carbon isotope fractionation in photosynthesis and carbon dioxide component of the greenhouse effect. Biology Bulletin, 34, 603-609.
40. Janssens, I.A., Dieleman, W., Luyssaert, S. etal. (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nature Geoscience, 3, 315 - 322.
41. Jump, A., Hunt, J. & Peñuelas, J. (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Global Change Biology, 12, 2163-2174.
42. Jump, A., Hunt, J. & Peñuelas, J. (2007) Climate relationships of growth and establishment across the altitudinal range of Fagus sylvatica in the Montseny Mountains, NE Spain. Ecoscience, 14, 507-518.
43. 2 on forest trees and forest ecosystems: knowledge gaps. Environmental International, 29, 161-169.
44. 13C from larches in eastern Siberia (Russia). Chemical Geology, 252, 31-41.
45. 2 on growth rates of western juniper. Global Change Biology, 7, 903-917.
46. 2 enrichment. Ecological Applications, 10, 1590-1619.
47. 2 responses: an issue of definition, time and resource supply. New Phytologist, 172, 393-411.
48. 2 fertilization: when, where, how much? Terrestrial ecosystems in a changing world, (ed. by J. Canadell, D. Pataki and L. Pitelka), pp. 9-21. Springer-Verlag, Berlin.
49. 2 fertilization effect? Dendrochronologia, 26, 13-19.
50. Le Quéré, C., Raupach, M.R., Canadell, J.G. etal. (2009) Trends in the sources and sinks of carbon dioxide. Nature Geoscience, 2, 831-836.
51. 2. Global Change Biology, 13, 2498-2508.
52. Linares, J.C., Delgado-Huertas, A., Camarero, J.J., Merino, J. & Carreira, J.A. (2009) Competition and drought limit the response of water-use efficiency to rising atmospheric carbon dioxide in the Mediterranean fir Abies pinsapo. Oecologia, 161, 611-624.
53. 2 concentration and to climate in semi-arid and arid areas of northwestern China. Plant Ecology, 193, 195-209.
54. 13C in tree rings to increasing drought on the northeastern Tibetan Plateau. Journal of Geophysical Research, 113, G03015, doi: 10.1029/2007JG000610.
55. Loader, N.J., Santillo, P.M., Woodman-Ralph, J.P., Rolfe, J.E., Hall, M.A., Gagen, M., Robertson, I., Wilson, R., Froyd, R. & McCarroll, D. (2008) Multiple stable isotopes from oak trees in southwestern Scotland and the potential for stable isotope dendroclimatology in maritime climatic regions. Chemical Geology, 252, 62-71.
56. Long, S.P., Ainsworth, E.A., Rogers, A. & Ort, D.R. (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology, 55, 591-628.
57. Luo, Y., Currie, W.S., Dukes, J.S., Finzi, A., Hartwig, U., Hungate, B., McMurtrie, R.E., Oren, R., Parton, W.J., Pataki, D.E., Shaw, M.R., Zak, D.R. & Field, C.B. (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience, 54, 731-739.
58. McCarroll, D. & Loader, N.J. (2004) Stable isotopes in tree rings. Quaternary Science Reviews, 23, 771-801.
59. McMahon, S.M., Parker, G.G. & Miller, D.R. (2010) Evidence for a recent increase in forest growth. Proceedings of the National Academy of Sciences USA, doi: 10.1073/pnas.0912376107.
60. Magnani, F., Mencuccini, M., Borghetti, M. etal. (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature, 447, 848-850.
61. Martínez-Vilalta, J., López, B.C., Adell, N., Badiella, L. & Ninyerola, M. (2008) Twentieth century increase of Scots pine radial growth in NE Spain shows strong climate interactions. Global Change Biology, 14, 2868-2881.
62. Melillo, J.M., Prentice, I.C., Farquhar, G.D., Schulze, E.D. & Sala, O.E. (1996) Terrestial biotic responses to environmental change and feedbacks to climate. Climate change 1995 (ed. by J.T. Houghton, L.G. Meira Filho, B.A. Callander, N. Harris, A. Kattengerg and K. Maskell), pp. 445-481. Cambridge University Press, Cambridge.
63. Morales, M.S., Villalba, R., Grau, H.R., Villagra, P.E., Boninsegna, J.A., Ripalta, A. & Paolini, L. (2001) Potencialidad de Prosopis ferox Griseb (Leguminosae, subfamilia: Mimosoidae) para estudios dendrocronológicos en desiertos subtropicales de alta montaña. Revista Chilena de Historia Natural, 74, 889.
64. 2. Oecologia, 140, 11-25.
65. Morgan, J.A., Milchunas, D.G., Lecain, D.R., West, M. & Mosier, A.R. (2007) Carbon dioxide enrichment alters plant community structure and accelerates shrub growth in the shortgrass steppe. Proceedings of the National Academy of Sciences USA, 104, 14724-14729.
66. 2 under water limited conditions. Vegetatio, 104, 193-209.
67. 2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences USA, 102, 18052-18056.
68. 2 enhancement of forest productivity constrained by limited nitrogen availability. Nature Precedings. Available at: (accessed 20 April 2010).
69. 2 - do photosynthetic and productivity data from FACE experiments support early predictions? New Phytologist, 162, 253-280.
70. O'Leary, M.H. (1981) Theoretical basis of carbon isotope fractionation in plants. Phytochemistry, 20, 553-567.
71. 2-enriched atmosphere. Nature, 411, 469-472.
72. Osmond, C.B., Björkman, O. & Anderson, D.J. (1980) Physiological processes in plant ecology. Toward a synthesis with Atriplex. Springer-Verlag, New York.
73. 2 enrichment. Tree Physiology, 14, 997-1003.
74. Pedersen, B.S. (1998) The role of stress in the mortality of midwestern oaks as indicated by growth prior to death. Ecology, 79, 79-93.
75. 2 increase. Plant Cell and Environment, 15, 485-489.
76. Peñuelas, J. & Boada, M. (2003) A global change-induced biome shift in the Montseny Mountains (NE Spain). Global Change Biology, 9, 131-140.
77. Peñuelas, J. & Filella, I. (2001) Phenology: responses to a warming world. Science, 294, 793-795.
78. 2 increase. Journal of Experimental Botany, 41, 1119-1124.
79. Peñuelas, J., Filella, I. & Comas, P. (2002) Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Global Change Biology, 8, 531-544.
80. Peñuelas, J., Ogaya, R., Boada, M. & Jump, A. (2007) Migration, invasion and decline: changes in recruitment and forest structure in a warming-linked biome shift in Catalonia (NE Spain). Ecography, 30, 830-838.
81. 13C at the southern range-edge of Fagus sylvatica: increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Global Change Biology, 14, 1076-1088.
82. Phipps, R.L. & Whiton, J.C. (1988) Decline in long-term growth trends of white oak. Canadian Journal of Forest Research, 18, 24-32.
83. 2 and drought. Annales des Sciences Forestières, 53, 431-446.
84. Piovesan, G., Di Filippo, A., Alessandrini, A., Biondi, F. & Schirone, B. (2005) Structure, dynamics and dendroecology of an old-growth Fagus forest in the Apennines. Journal of Vegetation Science, 16, 13-28.
85. Piovesan, G., Biondi, F., Di Filippo, A., Alessandrini, A. & Maugeri, M. (2008) Drought-driven growth reduction in old beech (Fagus sylvatica L.) forests of the central Apennines, Italy. Global Change Biology, 14, 1265-1281.
86. 2: on winners, losers and functional groups. New Phytologist, 157, 175-198.
87. 2 and temperature in a future climate. Forest Ecology and Management, 158, 179-188.
88. Rathgeber, C., Guiot, J., Roche, P. & Tessier, L. (1999) Augmentation de productivité du chêne pubescent en région méditerranéenne Française. Annals of Forest Science, 56, 211-219.
89. 2 increase using a statistical model. Global and Planetary Change, 26, 405-421.
90. 2. Nature, 440, 922-925.
91. Salzer, M.W., Hughes, M.K., Bunn, A.G. & Kipfmueller, K.F. (2009) Recent unprecedented tree-ring growth in bristlecone pine at the highest elevations and possible causes. Proceedings of the National Academy of Sciences USA, 106, 20348-20353.
92. Sano, M., Buckley, B.M. & Sweda, T. (2009) Tree-ring based hydroclimate reconstruction over northern Vietnam from Fokienia hodginsii: eighteenth century mega-drought and tropical Pacific influence. Climate Dynamics, 33, 331-340.
93. 2 spring into tree rings: an isotope approach. Tree Physiology, 23, 997-1004.
94. 2. Science, 298, 1987-1990.
95. 18O) in wood and cellulose of Siberian larch trees for early Medieval and recent periods. Journal of Geophysical Research, 113, G02019; doi: 10.1029/2007JG000473.
96. Silva, L.C.R., Anand, M., Oliveira, J.M. & Pillar, V. (2009) Past century changes in Araucaria angustifolia (Bertol.) Kuntze water use efficiency and growth in forest and grassland ecosystems of southern Brazil: implications for forest expansion. Global Change Biology, 15, 2387-2396.
97. Sitch, S., Huntingford, C., Gedney, N., Levy, P.E., Lomas, M., Piao, S.L., Betts, R., Ciais, P., Cox, P., Friedlingstein, P., Jones, C.D., Prentice, I.C. & Woodward, F.I. (2008) Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five dynamic global vegetation models (DGVMs). Global Change Biology, 14, 2015-2039.
98. 2 fertilization effect? New Phytologist, 171, 379-390.
99. 2 sobre el crecimiento de Nothofagus pumilio en la Patagonia. Revista Chilena de Historia Natural, 81, 239-256.
100. 2. Science, 316, 1732-1735.
101. 2 increase in Tianshan Mountains, Xinjiang Autonomous Region, China. Forest Ecology and Management, 246, 273-284.
102. Switsur, R. & Waterhouse, J. (1998) Stable isotopes in tree ring cellulose. Stable isotopes: integration of biological, ecological and geochemical processes (ed. by H. Griffiths), pp. 303-321. BIOS Scientific Publishers Ltd, Oxford.
103. 13C of tree rings in full-bark and strip-bark bristlecone pine trees in the White Mountains of California. Global Change Biology, 5, 33-40.
104. 2 concentrations. New Phytologist, 146, 59-74.
105. 2 growth enhancement declines with age in Quercus and Pinus. Ecological Monographs, 76, 549-564.
106. 13C discriminations of Pinus sylvestris vs. Pinus ponderosa at a dry site in Brandenburg (eastern Germany): 100-year growth comparison. Isotopes in Environmental and Health Studies, 43, 117-128.
107. 2 fertilization suggested by open-grown white spruce in a dry environment. Global Change Biology, 12, 601-610.
108. Waterhouse, J.S., Switsur, V.R., Barker, A.C., Carter, A.H.C., Hemming, D.L., Loader, N.J. & Robertson, I. (2004) Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations. Quaternary Science Reviews, 23, 803-810.
109. 2. Vegetatio, 104/105, 145-155.