Skip to main content
Log in

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

Trees Aims and scope Submit manuscript

Abstract

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.

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • 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 5:145–159

    Google Scholar 

  • Allen CD, Breshears DD (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Pro Natl Acad Sci USA 95:14839–14842

    CAS  Google Scholar 

  • 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 259:660–684

    Google Scholar 

  • 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 

  • 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 190:1003–1018

    PubMed  Google Scholar 

  • Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34:83–94. doi:10.1071/fp06228

    CAS  Google Scholar 

  • Barbour MM, Farquhar GD (2000) Relative humidity- and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant Cell Environ 23:473–485

    CAS  Google Scholar 

  • 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 123:671–679

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 28:335–348

    CAS  Google Scholar 

  • 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 25:1483–1499

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 15:295–306

    PubMed  Google Scholar 

  • 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 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brooks JR, Coulombe R (2009) Physiological responses to fertilization recorded in tree rings: isotopic lessons from a long-term fertilization trial. Ecol Appl 19:1044–1060

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • Cannell MG, Dewar RC (1994) Carbon allocation in trees: a review of concepts for modelling. Adv Ecol Res 25:59–104

    Google Scholar 

  • Cescatti A, Piutti E (1998) Silvicultural alternatives, competition regime and sensitivity to climate in a European beech forest. For Ecol Manag 102:213–223

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Covington WW, Fule PZ, Moore MM et al (1997) Restoring ecosystem health in ponderosa pine forests of the southwest. J Forest 95:23–29

    Google Scholar 

  • 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 9–130

  • 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

    CAS  Google Scholar 

  • 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 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 47–70

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537

    CAS  Google Scholar 

  • 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 27–61

  • 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 28:1295–1306

    Google Scholar 

  • 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 

  • 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 69–74

  • Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water use. Funct Ecol 5:270–277

  • Francey RJ, Farquhar GD (1982) An explanation of 13C/12C variations in tree rings. Nature 297:28–31. doi:10.1038/297028a0

    CAS  Google Scholar 

  • Fritts HC (1976) Tree rings and climate. Academic Press, London, New York, San Francisco

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 27:367–380

    CAS  Google Scholar 

  • Hill SA, Waterhouse JS, Field EM et al (1995) Rapid recycling of triose phosphates in oak stem tissue. Plant Cell Environ 18:931–936

    CAS  Google Scholar 

  • 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 

  • Hsiao TC, Acevedo E (1974) Plant responses to water deficits, water-use efficiency, and drought resistance. Agric Meteorol 14:59–84

    Google Scholar 

  • 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 

  • 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 change

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • 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

    PubMed  Google Scholar 

  • 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 20:1–12

    PubMed  Google Scholar 

  • 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 18:375–381

    PubMed  Google Scholar 

  • Kolb TE, Agee JK, Fule PZ, McDowell NG, Pearson K, Sala A, Waring RH (2007) Perpetuating old ponderosa pine. For Ecol Manag 249:141–157

    Google Scholar 

  • Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17

    Google Scholar 

  • Kriedemann PE (1986) Stomatal and photosynthetic limitations to leaf growth. Funct Plant Biol 13:15–31

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Latham P, Tappeiner J (2002) Response of old-growth conifers to reduction in stand density in western Oregon forests. Tree Physiol 22:137–146

    CAS  PubMed  Google Scholar 

  • 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 

  • 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

    CAS  Google Scholar 

  • Legoff N, Ottorini JM (1993) Thinning and climate effects on growth of beech (Fagus-sylvatica L) in experimental stands. For Ecol Manag 62:1–14

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Martinez-Vilalta J, Sala A, Pinol J (2004) The hydraulic architecture of Pinaceae—a review. Plant Ecol 171:3–13

    Google Scholar 

  • 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 26:631–644

    Google Scholar 

  • McDowell NG, Adams HD, Bailey JD et al (2006) Homeostatic maintenance of ponderosa pine gas exchange in response to stand density changes. Ecol Appl 16:1164–1182

    PubMed  Google Scholar 

  • 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 

  • 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

    CAS  Google Scholar 

  • 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 

  • 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 255–286

    Google Scholar 

  • 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 

  • 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 197:862–872

    CAS  PubMed  Google Scholar 

  • 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 

  • 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

    PubMed  Google Scholar 

  • 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 257:1353–1362

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 

  • 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-628

  • Phillips OL, Aragao LEOC, Lewis SL et al (2009) Drought sensitivity of the Amazon rainforest. Science 323:1344–1347. doi:10.1126/science.1164033

    CAS  PubMed  Google Scholar 

  • 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 

  • 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

    PubMed  Google Scholar 

  • 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 

  • 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

    CAS  PubMed  Google Scholar 

  • Roden JS, Ehleringer JR (2000) Hydrogen and oxygen isotope ratios of tree ring cellulose for field-grown riparian trees. Oecologia 123:481–489

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Roden J, Siegwolf R (2012) Is the dual-isotope conceptual model fully operational? Tree Physiol 32:1179–1182. doi:10.1093/treephys/tps099

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 15

  • 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

    PubMed  Google Scholar 

  • Saurer M, Aellen K, Siegwolf R (1997) Correlating delta C-13 and delta O-18 in cellulose of trees. Plant Cell Environ 20:1543–1550

    Google Scholar 

  • 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 125:350–357

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Skov KR, Kolb TE, Wallin KF (2004) Tree size and drought affect ponderosa pine physiological response to thinning and burning treatments. For Sci 50:81–91

    Google Scholar 

  • 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 20:36–43

    Google Scholar 

  • 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 32:1199–1213

  • 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 

  • 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

    CAS  Google Scholar 

  • Sternberg L, DeNiro M (1983) Biogeochemical implications of the isotopic equilibrium fractionation factor between oxygen atoms of acetone and water. Geochim et Cosmochim Acta 47:2271–2274

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  Google Scholar 

  • Tissue DT, Wright SJ (1995) Effect of seasonal water availability on phenology and the annual shoot carbohydrate cycle of tropical forest shrubs. Funct Ecol 9:518–527

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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 24:57–68

    Google Scholar 

  • 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 

  • Wollum AG, Schubert GH (1975) Effect of thinning on the foliage and forest floor properties of ponderosa pine stands. Soil Sci Soc Am Proc 39:968–972

    CAS  Google Scholar 

  • 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 363–384

  • 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

    PubMed  Google Scholar 

  • 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 

  • 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 17:461–466

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia A. Sohn.

Additional information

Communicated by A. Geßler.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sohn, J.A., Brooks, J.R., Bauhus, J. et al. Unthinned slow-growing ponderosa pine (Pinus ponderosa) trees contain muted isotopic signals in tree rings as compared to thinned trees. Trees 28, 1035–1051 (2014). https://doi.org/10.1007/s00468-014-1016-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-014-1016-z

Keywords

Navigation