, Volume 28, Issue 4, pp 1035–1051 | Cite as

Unthinned slow-growing ponderosa pine (Pinus ponderosa) trees contain muted isotopic signals in tree rings as compared to thinned trees

  • Julia A. Sohn
  • J. Renée Brooks
  • Jürgen Bauhus
  • Martin Kohler
  • Thomas E. Kolb
  • Nathan G. McDowell
Original Paper


Key message

The muted wood isotopic signal in slow-growing trees of unthinned stands indicates lower responsiveness to changing environmental conditions compared to fast-growing trees in thinned stands.


To examine the physiological processes associated with higher growth rates after thinning, we analyzed the oxygen isotopic values in wood (δ18Ow) of 12 ponderosa pine (Pinus ponderosa) trees from control, moderately, and heavily thinned stands and compared them with wood-based estimates of carbon isotope discrimination (∆13C), basal area increment (BAI), and gas exchange. We found that (heavy) thinning led to shifts and increased inter-annual variability of both stable carbon and oxygen isotope ratios relative to the control throughout the first post-thinning decade. Results of a sensitivity analysis suggested that both an increase in stomatal conductance (g s) and differences in source water among treatments are equally probable causes of the δ18Ow shift in heavily thinned stands. We modeled inter-annual changes in δ18Ow of trees from all treatments using environmental and physiological data and found that the significant increase in δ18Ow inter-annual variance was related to greater δ18Ow responsiveness to changing environmental conditions for trees in thinned stands when compared to control stands. Based on model results, the more muted climatic response of wood isotopes in slow-growing control trees is likely to be the consequence of reduced carbon sink strength causing a higher degree of mixing of previously stored and fresh assimilates when compared to faster-growing trees in thinned stands. Alternatively, the muted response of δ18Ow to climatic variation of trees in the control stand may result from little variation in the control stand in physiological processes (photosynthesis, transpiration) that are known to affect δ18Ow.


Oxygen isotopes Thinning Pinus ponderosa (ponderosa pine) Gas exchange Sensitivity analysis 



We would like to thank the Deutsche Forschungsgemeinschaft (BA 2821/11-1), the Landesgraduiertenförderung Baden-Württemberg, the graduate school “Environment, Society and Global Change” at Freiburg University, and the Wissenschaftliche Gesellschaft Freiburg for their financial support. Many thanks also to Dr. Bernd Kammerer and Erika Fischer of the Center for Biological Systems Analysis (ZBSA) in Freiburg for their help with stable isotope analysis. This manuscript has been subjected to the Environmental Protection Agency’s peer and administrative review, and it has been approved for publication as an EPA document. Mention of trade names or commercial products does not constitute endorsement or recommendation for use. This project was also supported by the Department of Energy, Office of Biological and Environmental Research. We thank Lucy Kerhoulas from NAU who assembled and kindly provided the climatic data used in this study.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Adams HD, Luce CH, Breshears DD, Allen CD, Weiler M, Hale VC, Smith AMS, Huxman TE (2012) Ecohydrological consequences of drought- and infestation- triggered tree die-off: insights and hypotheses. Ecohydrology 5:145–159Google Scholar
  2. Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Pro Natl Acad Sci USA 95:14839–14842Google Scholar
  3. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684Google Scholar
  4. Aussenac G, Granier A (1988) Effects of thinning on water stress and growth in Douglas-fir. Can J For Res 18:100–105. doi: 10.1139/x88-015 Google Scholar
  5. Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytol 190:1003–1018PubMedGoogle Scholar
  6. Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34:83–94. doi: 10.1071/fp06228 Google Scholar
  7. Barbour MM, Farquhar GD (2000) Relative humidity- and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant Cell Environ 23:473–485Google Scholar
  8. Barbour MM, Schurr U, Henry BK et al (2000) Variation in the oxygen isotope ratio of phloem sap sucrose from castor bean. Evidence in support of the Peclet effect. Plant Physiol 123:671–679PubMedCentralPubMedGoogle Scholar
  9. Barbour MM, Andrews TJ, Farquhar GD (2001) Correlations between oxygen isotope ratios of wood constituents of Quercus and Pinus samples from around the world. Funct Plant Biol 28:335–348Google Scholar
  10. Barbour MM, Walcroft AS, Farquhar GD (2002) Seasonal variation in delta C-13 and delta O-18 of cellulose from growth rings of Pinus radiata. Plant Cell Environ 25:1483–1499Google Scholar
  11. Barnard HR, Brooks JR, Bond BJ (2012) Applying the dual-isotope conceptual model to interpret physiological trends under uncontrolled conditions. Tree Physiol 32:1183–1198. doi: 10.1093/treephys/tps078 PubMedGoogle Scholar
  12. Biondi F (1996) Decadal-scale dynamics at the Gus Pearson Natural Areas: evidence for inverse (a)symmetric competition? Can J For Res 26:1397–1406. doi: 10.1139/x26-156 Google Scholar
  13. Brandes E, Kodama N, Whittaker K et al (2006) Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation. Glob Change Biol 12:1922–1939. doi: 10.1111/j.1365-2486.2006.01205.x Google Scholar
  14. Breda N, Granier A, Aussenac G (1995) Effects of thinning on soil and tree water relations, transpiration and growth in an oak forest (Quercus-Petraea (Matt) Liebl). Tree Physiol 15:295–306PubMedGoogle Scholar
  15. Breshears DD, Allen CD (2002) The importance of rapid, disturbance-induced losses in carbon management and sequestration: rapid, disturbance-induced C losses. Glob Ecol Biogeogr 11:1–5. doi: 10.1046/j.1466-822X.2002.00274.x Google Scholar
  16. Breshears DD, Cobb NS, Rich PM et al (2005) Regional vegetation die-off in response to global-change-type drought. Proc Natl Acad Sci 102:15144–15148. doi: 10.1073/pnas.0505734102 PubMedCentralPubMedGoogle Scholar
  17. Brooks JR, Coulombe R (2009) Physiological responses to fertilization recorded in tree rings: isotopic lessons from a long-term fertilization trial. Ecol Appl 19:1044–1060PubMedGoogle Scholar
  18. Brooks JR, Mitchell AK (2011) Interpreting tree responses to thinning and fertilization using tree-ring stable isotopes. New Phytol 190:770–782. doi: 10.1111/j.1469-8137.2010.03627.x PubMedGoogle Scholar
  19. Burke EJ, Brown SJ, Christidis N (2006) Modeling the recent evolution of global drought and projections for the twenty-first century with the Hadley centre climate model. J Hydrometeorol 7:1113–1125. doi: 10.1175/JHM544.1 Google Scholar
  20. Cannell MG, Dewar RC (1994) Carbon allocation in trees: a review of concepts for modelling. Adv Ecol Res 25:59–104Google Scholar
  21. Cescatti A, Piutti E (1998) Silvicultural alternatives, competition regime and sensitivity to climate in a European beech forest. For Ecol Manag 102:213–223Google Scholar
  22. Ciais P, Reichstein M, Viovy N et al (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533. doi: 10.1038/nature03972 PubMedGoogle Scholar
  23. Covington WW, Fule PZ, Moore MM et al (1997) Restoring ecosystem health in ponderosa pine forests of the southwest. J Forest 95:23–29Google Scholar
  24. Craig H, Gordon LI (1965) Deuterium and oxygen 18 variations in the ocean and the marine atmosphere. In: Tongiorgi E (ed) Proceedings of a Conference on Stable Isotopes in Oceanographic Studies and Palaeotemperatures. Lischi and Figli, Pisa, Italy, pp 9–130Google Scholar
  25. DeNiro MJ, Epstein S (1981) Isotopic composition of cellulose from aquatic organisms. Geochim Cosmochim Acta 45:1885–1894. doi: 10.1016/0016-7037(81)90018-1 Google Scholar
  26. Dore S, Montes-Helu M, Hart SC et al (2012) Recovery of ponderosa pine ecosystem carbon and water fluxes from thinning and stand-replacing fire. Glob Change Biol 18:3171–3185. doi: 10.1111/j.1365-2486.2012.02775.x Google Scholar
  27. English NB, McDowell NG, Allen CD, Mora C (2011) The effects of α-cellulose extraction and blue-stain fungus on retrospective studies of carbon and oxygen isotope variation in live and dead trees: stable isotopes in tree-ring wood and cellulose of live and dead trees. Rapid Commun Mass Spectrom 25:3083–3090. doi: 10.1002/rcm.5192 PubMedGoogle Scholar
  28. Farquhar GD, Lloyd J (1993) Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Stable Isot. Plant Carbon-Water Relat. Elsevier, Amsterdam, pp 47–70Google Scholar
  29. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537Google Scholar
  30. Farquhar GD, Barbour MM, Henry BK (1998) Interpretation of oxygen isotope composition of leaf material. In: Griffiths H (ed) Stable isotopes: integration of biological, ecological and geochemical processes. BIOS Scientific Publishers, Oxford, pp 27–61Google Scholar
  31. Feeney SR, Kolb TE, Covington WW, Wagner MR (1998) Influence of thinning and burning restoration treatments on presettlement ponderosa pines at the Gus Pearson Natural Area. Can J For Res Rev Can Rech For 28:1295–1306Google Scholar
  32. Fettig CJ, Klepzig KD, Billings RF et al (2007) The effectiveness of vegetation management practices for prevention and control of bark beetle infestations in coniferous forests of the western and southern United States. For Ecol Manag 238:24–53. doi: 10.1016/j.foreco.2006.10.011 Google Scholar
  33. Fiedler CE, Arno SF, Harrington MG (1996) Flexible silvicultural and prescribed burning approaches for improving health of ponderosa pine forests. US For Serv Gen Tec. Rep RMRS-278, pp 69–74Google Scholar
  34. Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water use. Funct Ecol 5:270–277Google Scholar
  35. Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31. doi: 10.1038/297028a0 Google Scholar
  36. Fritts HC (1976) Tree rings and climate. Academic Press, London, New York, San FranciscoGoogle Scholar
  37. Galvez DA, Landhausser SM, Tyree MT (2011) Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol 31:250–257. doi: 10.1093/treephys/tpr012 PubMedGoogle Scholar
  38. Gaylord ML, Kolb TE, Wallin KF, Wagner MR (2007) Seasonal dynamics of tree growth, physiology, and resin defenses in a northern Arizona ponderosa pine forest. Can J For Res 37:1173–1183. doi: 10.1139/X06-309 Google Scholar
  39. Gessler A, Brandes E, Buchmann N et al (2009) Tracing carbon and oxygen isotope signals from newly assimilated sugars in the leaves to the tree-ring archive. Plant Cell Environ 32:780–795. doi: 10.1111/j.1365-3040.2009.01957.x PubMedGoogle Scholar
  40. Gessler A, Brandes E, Keitel C et al (2013) The oxygen isotope enrichment of leaf-exported assimilates—does it always reflect lamina leaf water enrichment? New Phytol 200:144–157. doi: 10.1111/nph.12359 PubMedCentralPubMedGoogle Scholar
  41. Gleixner G, Scrimgeour C, Schmidt H-L, Viola R (1998) Stable isotope distribution in the major metabolites of source and sink organs of Solanum tuberosum L.: a powerful tool in the study of metabolic partitioning in intact plants. Planta 207:241–245. doi: 10.1007/s004250050479 Google Scholar
  42. Helle G, Schleser GH (2004) Beyond CO2-fixation by Rubisco—an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27:367–380Google Scholar
  43. Hill SA, Waterhouse JS, Field EM et al (1995) Rapid recycling of triose phosphates in oak stem tissue. Plant Cell Environ 18:931–936Google Scholar
  44. Hogg EH, Brandt JP, Michaelian M (2008) Impacts of a regional drought on the productivity, dieback, and biomass of western Canadian aspen forests. Can J For Res 38:1373–1384. doi: 10.1139/X08-001 Google Scholar
  45. Hsiao TC, Acevedo E (1974) Plant responses to water deficits, water-use efficiency, and drought resistance. Agric Meteorol 14:59–84Google Scholar
  46. Huntington TG (2006) Evidence for intensification of the global water cycle: review and synthesis. J Hydrol 319:83–95. doi: 10.1016/j.jhydrol.2005.07.003 Google Scholar
  47. IPCC (2007) Climate change 2007: synthesis report. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate changeGoogle Scholar
  48. Kagawa A, Sugimoto A, Maximov TC (2006) Seasonal course of translocation, storage and remobilization of 13C pulse-labeled photoassimilate in naturally growing Larix gmelinii saplings. New Phytol 171:793–804. doi: 10.1111/j.1469-8137.2006.01780.x PubMedGoogle Scholar
  49. Kahmen A, Simonin K, Tu K et al (2009) The influence of species and growing conditions on the 18-O enrichment of leaf water and its impact on “effective path length”. New Phytol 184:619–630. doi: 10.1111/j.1469-8137.2009.03008.x PubMedGoogle Scholar
  50. Kahmen A, Sachse D, Arndt SK et al (2011) Cellulose 18O is an index of leaf-to-air vapor pressure difference (VPD) in tropical plants. Proc Natl Acad Sci 108:1981–1986. doi: 10.1073/pnas.1018906108 PubMedCentralPubMedGoogle Scholar
  51. Keel SG, Siegwolf RTW, Körner C (2006) Canopy CO2 enrichment permits tracing the fate of recently assimilated carbon in a mature deciduous forest. New Phytol 172:319–329. doi: 10.1111/j.1469-8137.2006.01831.x PubMedGoogle Scholar
  52. Kerhoulas LP, Kolb TE, Koch GW (2013) Tree size, stand density, and the source of water used across seasons by ponderosa pine in northern Arizona. For Ecol Manag 289:425–433. doi: 10.1016/j.foreco.2012.10.036 Google Scholar
  53. Koepke DF, Kolb TE (2013) Species variation in water relations and xylem vulnerability to cavitation at a forest-woodland ecotone. Forensic Sci 59:524–535. doi: 10.5849/forsci.12-053 Google Scholar
  54. Koepke DF, Kolb TE, Adams HD (2010) Variation in woody plant mortality and dieback from severe drought among soils, plant groups, and species within a northern Arizona ecotone. Oecologia 163:1079–1090. doi: 10.1007/s00442-010-1671-8 PubMedGoogle Scholar
  55. Kolb TE, Stone JE (2000) Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine-oak forest. Tree Physiol 20:1–12PubMedGoogle Scholar
  56. Kolb TE, Holmberg KM, Wagner MR, Stone JE (1998) Regulation of ponderosa pine foliar physiology and insect resistance mechanisms by basal area treatments. Tree Physiol 18:375–381PubMedGoogle Scholar
  57. Kolb TE, Agee JK, Fule PZ, McDowell NG, Pearson K, Sala A, Waring RH (2007) Perpetuating old ponderosa pine. For Ecol Manag 249:141–157Google Scholar
  58. Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17Google Scholar
  59. Kriedemann PE (1986) Stomatal and photosynthetic limitations to leaf growth. Funct Plant Biol 13:15–31Google Scholar
  60. Kuptz D, Fleischmann F, Matyssek R, Grams TEE (2011) Seasonal patterns of carbon allocation to respiratory pools in 60-yr-old deciduous (Fagus sylvatica) and evergreen (Picea abies) trees assessed via whole-tree stable carbon isotope labeling. New Phytol 191:160–172. doi: 10.1111/j.1469-8137.2011.03676.x PubMedGoogle Scholar
  61. Kurz WA, Dymond CC, Stinson G et al (2008) Mountain pine beetle and forest carbon feedback to climate change. Nature 452:987–990. doi: 10.1038/nature06777 PubMedGoogle Scholar
  62. Latham P, Tappeiner J (2002) Response of old-growth conifers to reduction in stand density in western Oregon forests. Tree Physiol 22:137–146PubMedGoogle Scholar
  63. Laurent M, Antoine N, Joel G (2003) Effects of different thinning intensities on drought response in Norway spruce (Picea abies (L.) Karst.). For Ecol Manag 183:47–60. doi: 10.1016/s0378-1127(03)00098-7 Google Scholar
  64. Leavitt SW (1993) Seasonal 13 C/12 C changes in tree rings: species and site coherence, and a possible drought influence. Can J For Res 23:210–218. doi: 10.1139/x93-028 Google Scholar
  65. Legoff N, Ottorini JM (1993) Thinning and climate effects on growth of beech (Fagus-sylvatica L) in experimental stands. For Ecol Manag 62:1–14Google Scholar
  66. Ma S, Concilio A, Oakley B et al (2010) Spatial variability in microclimate in a mixed-conifer forest before and after thinning and burning treatments. For Ecol Manag 259:904–915. doi: 10.1016/j.foreco.2009.11.030 Google Scholar
  67. Marshall JD, Monserud RA (1996) Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105:13–21. doi: 10.1007/BF00328786 Google Scholar
  68. Martin-Benito D, Del Rio M, Heinrich I et al (2010) Response of climate-growth relationships and water use efficiency to thinning in a Pinus nigra afforestation. For Ecol Manag 259:967–975. doi: 10.1016/j.foreco.2009.12.001 Google Scholar
  69. Martinez-Vilalta J, Sala A, Pinol J (2004) The hydraulic architecture of Pinaceae—a review. Plant Ecol 171:3–13Google Scholar
  70. McDowell N, Brooks JR, Fitzgerald SA, Bond BJ (2003) Carbon isotope discrimination and growth response of old Pinus ponderosa trees to stand density reductions. Plant Cell Environ 26:631–644Google Scholar
  71. McDowell NG, Adams HD, Bailey JD et al (2006) Homeostatic maintenance of ponderosa pine gas exchange in response to stand density changes. Ecol Appl 16:1164–1182PubMedGoogle Scholar
  72. McDowell NG, Adams HD, Bailey JD, Kolb TE (2007) The role of stand density on growth efficiency, leaf area index, and resin flow in southwestern ponderosa pine forests. Can J For Res Rev Can Rech For 37:343–355. doi: 10.1139/x06-233 Google Scholar
  73. McDowell NG, White S, Pockman WT (2008) Transpiration and stomatal conductance across a steep climate gradient in the southern Rocky Mountains. Ecohydrology 1:193–204. doi: 10.1002/eco.20 Google Scholar
  74. McDowell NG, Allen CD, Marshall L (2010) Growth, carbon-isotope discrimination, and drought-associated mortality across a Pinus ponderosa elevational transect. Glob Change Biol 16:399–415. doi: 10.1111/j.1365-2486.2009.01994.x Google Scholar
  75. McDowell NG, Bond BJ, Dickman LT et al (2011) Relationships between tree height and carbon isotope discrimination. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- Age-Relat. Chang. Tree Struct. Funct. Springer, Dordrecht, pp 255–286Google Scholar
  76. Michaelian M, Hogg EH, Hall RJ, Arsenault E (2011) Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest: aspen mortality following severe drought. Glob Change Biol 17:2084–2094. doi: 10.1111/j.1365-2486.2010.02357.x Google Scholar
  77. Mitchell PJ, O’Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA (2013) Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol 197:862–872PubMedGoogle Scholar
  78. Moore MM, Casey CA, Bakker JD et al (2006) Herbaceous vegetation responses (1992–2004) to restoration treatments in a ponderosa pine forest. Rangel Ecol Manag 59:135–144. doi: 10.2111/05-051R2.1 Google Scholar
  79. Moreno-Gutiérrez C, Barberá GG, NicoláS E et al (2011) Leaf δ18O of remaining trees is affected by thinning intensity in a semiarid pine forest: thinning intensity influences tree water status. Plant Cell Environ 34:1009–1019. doi: 10.1111/j.1365-3040.2011.02300.x PubMedGoogle Scholar
  80. Negron JF, McMillin JD, Anhold JA, Coulson D (2009) Bark beetle-caused mortality in a drought-affected ponderosa pine landscape in Arizona, USA. For Ecol Manag 257:1353–1362Google Scholar
  81. Offermann C, Ferrio JP, Holst J et al (2011) The long way down—are carbon and oxygen isotope signals in the tree ring uncoupled from canopy physiological processes? Tree Physiol 31:1088–1102. doi: 10.1093/treephys/tpr093 PubMedGoogle Scholar
  82. Parsons DJ, DeBenedetti SH (1979) Impact of fire suppression on a mixed-conifer forest. For Ecol Manag 2:21–33. doi: 10.1016/0378-1127(79)90034-3 Google Scholar
  83. Peterson DL, Johnson MC, Agee JK, Jain TB, McKenzie D, Reinhardt ED (2005) Forest structure and fire hazard in the western United States. USDA For Serv Gen Tech Re. PNW-GTR-628Google Scholar
  84. Phillips OL, Aragao LEOC, Lewis SL et al (2009) Drought sensitivity of the Amazon rainforest. Science 323:1344–1347. doi: 10.1126/science.1164033 PubMedGoogle Scholar
  85. Pinol J, Sala A (2000) Ecological implications of xylem cavitation for several Pinaceae in the Pacific Northern USA. Funct Ecol 14:538–545. doi: 10.1046/j.1365-2435.2000.00451.x Google Scholar
  86. Powers MD, Pregitzer KS, Palik BJ, Webster CR (2009) Wood delta C-13, delta O-18 and radial growth responses of residual red pine to variable retention harvesting. Tree Physiol 30:326–334. doi: 10.1093/treephys/tpp119 PubMedGoogle Scholar
  87. Rambo TR, North MP (2009) Canopy microclimate response to pattern and density of thinning in a Sierra Nevada forest. For Ecol Manag 257:435–442. doi: 10.1016/j.foreco.2008.09.029 Google Scholar
  88. Richardson AD, Carbone MS, Keenan TF et al (2013) Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol 197:850–861. doi: 10.1111/nph.12042 PubMedGoogle Scholar
  89. Roden JS, Ehleringer JR (2000) Hydrogen and oxygen isotope ratios of tree ring cellulose for field-grown riparian trees. Oecologia 123:481–489Google Scholar
  90. Roden JS, Farquhar GD (2012) A controlled test of the dual-isotope approach for the interpretation of stable carbon and oxygen isotope ratio variation in tree rings. Tree Physiol 32:490–503. doi: 10.1093/treephys/tps019 PubMedGoogle Scholar
  91. Roden J, Siegwolf R (2012) Is the dual-isotope conceptual model fully operational? Tree Physiol 32:1179–1182. doi: 10.1093/treephys/tps099 PubMedGoogle Scholar
  92. Roden JS, Lin G, Ehleringer JR (2000) A mechanistic model for interpretation of hydrogen and oxygen isotope ratios in tree-ring cellulose. Geochim Cosmochim Acta 64:21–35. doi: 10.1016/S0016-7037(99)00195-7 Google Scholar
  93. Ronco F, Edmister CB, Trujillo DB (1985) Growth of ponderosa pine thinned to different stocking levels in northern Arizona. USDA For Serv Res Pap RM-262, p 15Google Scholar
  94. Sala A, Hoch G (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ 32:22–30. doi: 10.1111/j.1365-3040.2008.01896.x PubMedGoogle Scholar
  95. Saurer M, Aellen K, Siegwolf R (1997) Correlating delta C-13 and delta O-18 in cellulose of trees. Plant Cell Environ 20:1543–1550Google Scholar
  96. Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350–357Google Scholar
  97. Schwalm CR, Williams CA, Schaefer K et al (2012) Reduction in carbon uptake during turn of the century drought in western North America. Nat Geosci 5:551–556. doi: 10.1038/ngeo1529 Google Scholar
  98. Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454. doi: 10.1007/s00442-007-0932-7 PubMedGoogle Scholar
  99. Skov KR, Kolb TE, Wallin KF (2004) Tree size and drought affect ponderosa pine physiological response to thinning and burning treatments. For Sci 50:81–91Google Scholar
  100. Skov KR, Kolb TE, Wallin KF (2005) Difference in radial growth response to restoration thinning and burning treatments between young and old ponderosa pine in Arizona. Western J Appl For 20:36–43Google Scholar
  101. Sohn JA, Kohler M, Gessler A, Bauhus J (2012) Interactions of thinning and stem height on the drought response of radial stem growth and isotopic composition of Norway spruce (Picea abies). Tree Physiol 32:1199–1213Google Scholar
  102. Sohn JA, Gebhardt T, Ammer C et al (2013) Mitigation of drought by thinning: short-term and long-term effects on growth and physiological performance of Norway spruce (Picea abies). For Ecol Manag 308:188–197. doi: 10.1016/j.foreco.2013.07.048 Google Scholar
  103. Song X, Barbour MM, Farquhar GD et al (2013) Transpiration rate relates to within- and across-species variations in effective path length in a leaf water model of oxygen isotope enrichment: transpiration-related variation in Péclet path length. Plant Cell Environ 36:1338–1351. doi: 10.1111/pce.12063 Google Scholar
  104. Sternberg L, DeNiro M (1983) Biogeochemical implications of the isotopic equilibrium fractionation factor between oxygen atoms of acetone and water. Geochim et Cosmochim Acta 47:2271–2274Google Scholar
  105. Sternberg LDSL, Deniro MJ, Savidge RA (1986) Oxygen isotope exchange between metabolites and water during biochemical reactions leading to cellulose synthesis. Plant Physiol 82:423–427. doi: 10.1104/pp.82.2.423 PubMedCentralGoogle Scholar
  106. Tissue DT, Wright SJ (1995) Effect of seasonal water availability on phenology and the annual shoot carbohydrate cycle of tropical forest shrubs. Funct Ecol 9:518–527Google Scholar
  107. Van Mantgem PJ, Stephenson NL, Byrne JC et al (2009) Widespread increase of tree mortality rates in the Western United States. Science 323:521–524. doi: 10.1126/science.1165000 PubMedGoogle Scholar
  108. Walcroft AS, Silvester WB, Whitehead D, Kelliher FM (1997) Seasonal changes in stable carbon isotope ratios within annual rings of Pinus radiata reflect environmental regulation of growth processes. Aust J Plant Physiol 24:57–68Google Scholar
  109. Williams MA, Baker WL (2012) Comparison of the higher-severity fire regime in historical (A.D. 1800s) and modern (A.D. 1984–2009) Montane forests across 624,156 ha of the Colorado front range. Ecosystems 15:832–847. doi: 10.1007/s10021-012-9549-8 Google Scholar
  110. Wollum AG, Schubert GH (1975) Effect of thinning on the foliage and forest floor properties of ponderosa pine stands. Soil Sci Soc Am Proc 39:968–972Google Scholar
  111. Woodruff DR, Meinzer FC (2011) Size-dependent changes in biophysical control of tree growth: the role of turgor. In: Size-and age-related changes in tree structure and function. Springer, Netherlands, pp 363–384Google Scholar
  112. Würth MKR, Pelez-Riedl S, Wright SJ, Körner C (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia 143:11–24. doi: 10.1007/s00442-004-1773-2 PubMedGoogle Scholar
  113. Zausen GL, Kolb TE, Bailey JD, Wagner MR (2005) Long-term impacts of stand management on ponderosa pine physiology and bark beetle abundance in northern Arizona: a replicated landscape study. For Ecol Manag 218:291–305. doi: 10.1016/j.foreco.2005.08.023 Google Scholar
  114. Zhang JW, Feng Z, Cregg BM, Schumann CM (1997) Carbon isotopic composition, gas exchange, and growth of three populations of ponderosa pine differing in drought tolerance. Tree Physiol 17:461–466PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Julia A. Sohn
    • 1
  • J. Renée Brooks
    • 2
  • Jürgen Bauhus
    • 1
  • Martin Kohler
    • 1
  • Thomas E. Kolb
    • 3
  • Nathan G. McDowell
    • 4
  1. 1.Chair of Silviculture, Faculty of Environment and Natural ResourcesUniversity of FreiburgFreiburgGermany
  2. 2.U.S. Environmental Protection AgencyNational Health and Environmental Effects Research LaboratoryCorvallisUSA
  3. 3.School of ForestryNorthern Arizona UniversityFlagstaffUSA
  4. 4.Earth and Environmental Sciences DivisionLos Alamos National LaboratoryLos AlamosUSA

Personalised recommendations