, Volume 29, Issue 6, pp 1735–1747 | Cite as

Effects of long-term elevated CO2 treatment on the inner and outer bark chemistry of sweetgum (Liquidambar styraciflua L.) trees

  • Thomas L. Eberhardt
  • Nicole Labbé
  • Chi-Leung So
  • Keonhee Kim
  • Karen G. Reed
  • Daniel J. Leduc
  • Jeffrey M. Warren
Original Article


Key message

Long-term exposure of sweetgum trees to elevated atmospheric CO 2 concentrations significantly shifted inner bark (phloem) and outer bark (rhytidome) chemical compositions, having implications for both defense and nutrient cycling.


Changes in plant tissue chemistry due to increasing atmospheric carbon dioxide (CO2) concentrations have direct implications for tissue resistance to abiotic and biotic stress while living, and soil nutrient cycling when senesced as litter. Although the effects of elevated CO2 concentrations on tree foliar chemistry are well documented, the effects on tree bark chemistry are largely unknown. The objective of this study was to determine the effects of a long-term elevated CO2 treatment on the contents of individual elements, extractives, ash, lignin, and polysaccharide sugars of sweetgum (Liquidambar styraciflua L.) bark. Trees were harvested from sweetgum plots equipped with the Free-Air CO2 Enrichment (FACE) apparatus, receiving either elevated or ambient CO2 treatments over a 12-year period. Whole bark sections were partitioned into inner bark (phloem) and outer bark (rhytidome) samples before analysis. Principal component analysis, coupled with either Fourier transform infrared spectroscopy or pyrolysis–gas chromatography–mass spectrometry data, was also used to screen for differences. Elevated CO2 reduced the N content (0.42 vs. 0.35 %) and increased the C:N ratio (109 vs. 136 %) of the outer bark. For the inner bark, elevated CO2 increased the Mn content (470 vs. 815 mg kg−1), total extractives (13.0 vs. 15.6 %), and residual ash content (8.1 vs. 10.8 %) as compared to ambient CO2; differences were also observed for some hemicellulosic sugars, but not lignin. Shifts in bark chemistry can affect the success of herbivores and pathogens in living trees, and as litter, bark can affect the biogeochemical cycling of nutrients within the forest floor. Results demonstrate that increasing atmospheric CO2 concentrations have the potential to impact the chemistry of temperate, deciduous tree bark such as sweetgum.


Ash Climate change Extractives Lignin Phloem Rhytidome 



This material is based upon work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research, under contract DE-AC05-00OR22725. The authors are grateful to Fred J. Matt, USDA Forest Service, Forest Products Laboratory, for the lignin and sugar analyses; Joanne Childs and Holly Vander Stel at ORNL carried out the total phenolic content analysis.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877CrossRefPubMedGoogle Scholar
  2. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment FACE? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372CrossRefPubMedGoogle Scholar
  3. Anttonen S, Manninen A-M, Saranpää P, Kainulainen P, Linder S, Vapaavuori E (2002) Effects of long-term nutrient optimization on stem wood chemistry in Picea abies. Trees 16:386–394CrossRefGoogle Scholar
  4. Boltersdorf SH, Pesch R, Werner W (2014) Comparative use of lichens, mosses and tree bark to evaluate nitrogen deposition in Germany. Environ Pollut 189:43–53CrossRefPubMedGoogle Scholar
  5. Calfapietra C, Angelis PD, Gielen B, Lukac M, Moscatelli MC, Avino G, Lagomarsino A, Polle A, Ceulemans R, Scarascia Mugnozza G, Hoosbeek M, Cotrufo MF (2007) Increased nitrogen-use efficiency of a short-rotation poplar plantation in elevated CO2 concentration. Tree Physiol 27:1153–1163CrossRefPubMedGoogle Scholar
  6. Chen H, Ferrari C, Angiuli M, Yao J, Raspi C, Bramanti E (2010) Qualitative and quantitative analysis of wood samples by Fourier transform infrared spectroscopy and multivariate analysis. Carbohydr Polym 82:772–778CrossRefGoogle Scholar
  7. Choong ET, Fogg PJ (1976) Extractives content and cell-wall specific gravity in sweetgum. LSU Wood Utilization Note #30, p 4Google Scholar
  8. Davis MW (1998) A rapid modified method for compositional carbohydrate analysis of lignocellulosics by high pH anion-exchange chromatography with pulsed amperometric detection (HPAEC/PAD). J Wood Technol 18(2):235–252CrossRefGoogle Scholar
  9. Duca D, Riva G, Pedretti EF, Toscano G (2014) Wood pellet quality with respect to EN 14961-2 standard and certifications. Fuel 135:9–14CrossRefGoogle Scholar
  10. Eberhardt TL (2012) Impact of industrial source on the chemical composition of loblolly pine bark. For Prod J 62:516–519Google Scholar
  11. Eberhardt TL (2013) Longleaf pine inner bark and outer bark thicknesses: measurement and relevance. South J Appl For 37:177–180CrossRefGoogle Scholar
  12. Eberhardt TL, Catallo WJ, Shupe TF (2010) Hydrothermal transformation of Chinese privet seed biomass to gas-phase and semi-volatile products. Bioresour Technol 101:4198–4204CrossRefPubMedGoogle Scholar
  13. Effland MJ (1977) Modified procedure to determine the acid-insoluble lignin in wood and pulp. Tappi J 60(10):143–144Google Scholar
  14. Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376CrossRefPubMedGoogle Scholar
  15. Gall R, Landolt W, Schleppi P, Michellod V, Bucher JB (2002) Water content and bark thickness of Norway spruce (Picea abies) stems: phloem water capacitance and sap flow. Tree Physiol 22:613–623CrossRefPubMedGoogle Scholar
  16. Garten CT, Iversen CM, Norby RJ (2011) Litterfall 15N abundance indicates declining soil nitrogen availability in a free air CO2-enrichment experiment. Ecology 92:133–139CrossRefPubMedGoogle Scholar
  17. Gielen B, Ceulemans R (2001) The likely impact of rising atmospheric CO2 on natural and managed Populus: a literature review. Environ Pollut 115:335–358CrossRefPubMedGoogle Scholar
  18. Gilman EF, Watson DG (1993) Liquidambar styraciflua—sweetgum. Fact Sheet ST-358, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, p 4Google Scholar
  19. Hatfield R, Fukushima RS (2005) Can lignin be accurately measured? Crop Sci 45:832–839CrossRefGoogle Scholar
  20. Hillis WE (1962) Wood extractives and their significance to the pulp and paper industries. Academic Press, New YorkGoogle Scholar
  21. IPCC (2007) Summary for policy makers. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: The physical science basis. Contribution of Working Group I to the Fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK, pp 1–18Google Scholar
  22. Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytol 186:346–357CrossRefPubMedGoogle Scholar
  23. Johnson DW, Cheng W, Joslin JD, Norby RJ, Edwards NT, Todd DE Jr (2004) Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochemistry 69:379–403CrossRefGoogle Scholar
  24. Kaakinen S, Kostiainen K, Ek F, Saranpää P, Kubiske ME, Sober J, Karnosky DF, Vapaavuori E (2004) Stem wood properties of Populus tremuloides, Betula papyrifera and Acer saccharum saplings after 3 years of treatments to elevated carbon dioxide and ozone. Glob Chang Biol 10:1513–1525CrossRefGoogle Scholar
  25. Kilpeläinen A, Gerendiain AZ, Luostarinen K, Peltola H, Kellomäki S (2007) Elevated temperature and CO2 concentration effects on xylem anatomy of Scots pine. Tree Physiol 27:1329–1338CrossRefPubMedGoogle Scholar
  26. Kim K, Labbé N, Warren JM, Elder T, Rials TG (2015) Chemical and anatomical changes in Liquidambar styraciflua L. xylem after long term exposure to elevated CO2. Environ Pollut 198:179–185CrossRefPubMedGoogle Scholar
  27. Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411CrossRefPubMedGoogle Scholar
  28. Kostiainen K, Kaakinen S, Warsta E, Kubiske ME, Nelson ND, Sober J, Karnosky DF, Saranpää P, Vapaavuori E (2008) Wood properties of trembling aspen and paper birch after 5 years of exposure to elevated concentrations of CO2 and O3. Tree Physiol 28:805–813CrossRefPubMedGoogle Scholar
  29. Kostiainen K, Kaakinen S, Saranpää P, Sigurdsson BD, Lundqvist S-O, Linder S, Vapaavuori E (2009) Stem wood properties of mature Norway spruce after 3 years of continuous exposure to elevated [CO2] and temperature. Glob Chang Biol 15:368–379CrossRefGoogle Scholar
  30. Labosky P Jr (1979) Chemical constituents of four southern pine barks. Wood Sci 12(2):80–85Google Scholar
  31. Lestander TA, Lundström A, Finell M (2012) Assessment of biomass functions for calculating bark proportions and ash contents of refined biomass fuels derived from major boreal tree species. Can J For Res 42:59–66CrossRefGoogle Scholar
  32. Lindsey K, Johnson A, Kim P, Jackson S, Labbé N (2013) Monitoring switchgrass composition to optimize harvesting periods for bioenergy and value-added products. Biomass Bioenergy 56:29–37CrossRefGoogle Scholar
  33. Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry. Trends Ecol Evol 17(10):457–461CrossRefGoogle Scholar
  34. López-González D, Fernandez-Lopez M, Valverde JL, Sanchez-Silva L (2014) Gasification of lignocellulosic biomass char obtained from pyrolysis: kinetic and evolved gas analyses. Energy 71:456–467CrossRefGoogle Scholar
  35. Luo Z-B, Calfapietra C, Liberloo M, Scarascia-Mugnozza G, Polle A (2006) Carbon partitioning to mobile and structural fractions in poplar wood under elevated CO2 (EUROFACE) and N fertilization. Glob Chang Biol 12:272–283CrossRefGoogle Scholar
  36. Luo Z-B, Calfapietra C, Liberloo M, Scarascia-Mugnozza G, Polle A (2008) Carbon-based secondary metabolites and internal nitrogen pools in Populus nigra under Free Air CO2 Enrichment (FACE) and nitrogen fertilisation. Plant Soil 304:45–57CrossRefGoogle Scholar
  37. Matthews S, Mila I, Scalbert A, Donnelly DMX (1997) Extractable and non-extractable proanthocyanidins in barks. Phytochemistry 45(2):405–410CrossRefGoogle Scholar
  38. Mattson WJ, Julkunen-Tiitto R, Herms DA (2005) CO2 enrichment and carbon partitioning to phenolics: do plant responses accord better with the protein competition or the growth-differentiation balance models? Oikos 111:337–347CrossRefGoogle Scholar
  39. McGinnis GD, Parikh S (1975) The chemical constituents of loblolly pine bark. Wood Sci 7(4):295–297Google Scholar
  40. Meier D, Fortmann I, Odermatt J, Faix O (2005) Discrimination of genetically modified poplar clones by analytical pyrolysis-gas chromatography and principal component analysis. J Appl Pyrolysis 74:129–137CrossRefGoogle Scholar
  41. Mencuccini M, Hölttä T, Sevanto S, Nikinmaa E (2013) Concurrent measurements of change in the bark and xylem diameters of trees reveal a phloem-generated turgor signal. New Phytol 198:1143–1154CrossRefPubMedGoogle Scholar
  42. Natali SM, Sañudo-Wilhelmy SA, Lerdau MT (2009) Plant and soil mediation of elevated CO2 impacts on trace metals. Ecosystems 12:715–727CrossRefGoogle Scholar
  43. Norby RJ, Todd DE, Fults J, Johnson DW (2001) Allometric determination of tree growth in a CO2-enriched sweetgum stand. New Phytol 150:477–487CrossRefGoogle Scholar
  44. Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of deciduous forest to atmospheric CO2 enrichment. Proc Natl Acad Sci 101:9689–9693PubMedCentralCrossRefPubMedGoogle Scholar
  45. Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulemans R, De Angelis P, Finzi AC, Karnosky DF, Kubiske ME, Lukac M, Pregitzer KS, Scarascia-Mugnozza GE, Schlesinger WH, Oren R (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc Natl Acad Sci 102:18052–18056PubMedCentralCrossRefPubMedGoogle Scholar
  46. Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proc Natl Acad Sci 107:19368–19373PubMedCentralCrossRefPubMedGoogle Scholar
  47. Overdieck D, Ziche D, Böttcher-Jungclaus K (2007) Temperature responses of growth and wood anatomy in European beech saplings grown in different carbon dioxide concentrations. Tree Physiol 27:261–268CrossRefPubMedGoogle Scholar
  48. Peterson AG, Ball JT, Luo Y, Field CB, Reich PB, Curtis PS, Griffin KL, Gunderson CA, Norby RJ, Tissue DT, Forstreuter M, Rey A, Vogel CS, Participants CMEAL (1999) The photosynthesis—leaf nitrogen relationship at ambient and elevated atmospheric carbon dioxide: a meta-analysis. Glob Chang Biol 5:331–346CrossRefGoogle Scholar
  49. Porankiewicz B, Iskra P, Sandak J, Tanaka C, Jóźwiak K (2006) High-speed steel tool wear during wood cutting in the presence of high-temperature corrosion and mineral contamination. Wood Sci Technol 40:673–682CrossRefGoogle Scholar
  50. Qiao Y-Z, Zhang Y-B, Wang K-Y, Wang Q, Tian Q-Z (2008) Growth and wood/bark properties of Abies faxoniana seedlings as affected by elevated CO2. J Integr Plant Biol 50:265–270CrossRefPubMedGoogle Scholar
  51. Raessler M, Wissuwa B, Breul A, Unger W, Grimm T (2010) Chromatographic analysis of major non-structural carbohydrates in several wood species—an analytical approach for higher accuracy of data. Anal Method 2:532–538CrossRefGoogle Scholar
  52. Rana R, Müller G, Naumann A, Polle A (2008) FTIR spectroscopy in combination with principal component analysis or cluster analysis as a tool to distinguish beech (Fagus sylvatica L.) trees grown at different sites. Holzforschung 62:530–538CrossRefGoogle Scholar
  53. Saxe H, Ellsworth DS, Heath J (1998) Tansley Review No 98 Tree and forest functioning in an enriched CO2 atmosphere. New Phytol 139:395–436CrossRefGoogle Scholar
  54. So CL, Eberhardt TL (2006) Rapid analysis of inner and outer bark composition of southern yellow pine bark from industrial sources. Holz Roh Werkst 64:463–467CrossRefGoogle Scholar
  55. Spencer R, Choong ET (1977) Isolation and characterization of several extractives in the bark and wood of sweetgum. Holzforschung 31(1):25–31CrossRefGoogle Scholar
  56. Talbot JM, Treseder KK (2012) Interactions among lignin, cellulose, and nitrogen drive litter chemistry-decay relationships. Ecology 93(2):345–354CrossRefPubMedGoogle Scholar
  57. Toscano G, Riva G, Pedretti EF, Corinaldesi F, Mengarelli C, Duca D (2013) Investigation on wood pellet quality and relationship between ash content and the most important chemical elements. Biomass Bioenergy 56:317–322CrossRefGoogle Scholar
  58. van Heerden PS, Towers GHN, Lewis NG (1996) Nitrogen metabolism in lignifying Pinus taeda cell cultures. J Biol Chem 271(21):12350–12355CrossRefPubMedGoogle Scholar
  59. Van Nevel L, Mertens J, Demey A, De Schrijver A, De Neve S, Tack FMG, Verheyen K (2014) Metal and nutrient dynamics in decomposing tree litter on a metal contaminated site. Environ Pollut 189:54–62CrossRefPubMedGoogle Scholar
  60. Warren JM, Pötzelsberger E, Wullschleger SD, Thornton PE, Hasenauer H, Norby RJ (2011) Ecohydrologic impact of reduced stomatal conductance in forest exposed to elevated CO2. Ecohydrology 4:196–210CrossRefGoogle Scholar
  61. Warren JM, Jensen AM, Medlyn BE, Norby RJ, Tissue DT (2015) CO2 stimulation of photosynthesis in Liquidambar styraciflua is not sustained during a 12-year field experiment. AoB Plants 7: plu074. doi: 10.1093/aobpla/plu074
  62. Watanabe Y, Satomura T, Sasa K, Funada R, Koike T (2010) Differential anatomical responses to elevated CO2 in saplings of four hardwood species. Plant Cell Environ 33:1101–1111PubMedGoogle Scholar
  63. Yazaki K, Maruyama Y, Mori S, Koike T, Funada R (2005) Effects of elevated carbon dioxide concentration on wood structure and formation in trees. In: Omasa K, Nouchi I, De Kok LJ (eds) Plant responses to air pollution and global change. Springer, Tokyo, pp 89–97CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2015

Authors and Affiliations

  • Thomas L. Eberhardt
    • 1
    • 5
  • Nicole Labbé
    • 2
  • Chi-Leung So
    • 3
  • Keonhee Kim
    • 2
  • Karen G. Reed
    • 1
  • Daniel J. Leduc
    • 1
  • Jeffrey M. Warren
    • 4
  1. 1.USDA Forest Service, Southern Research StationPinevilleUSA
  2. 2.Center for Renewable CarbonUniversity of TennesseeKnoxvilleUSA
  3. 3.School of Renewable Natural ResourcesLouisiana State University Agricultural CenterBaton RougeUSA
  4. 4.Climate Change Science Institute and Environmental Sciences DivisionOak Ridge National LaboratoryOak RidgeUSA
  5. 5.USDA Forest Service, Forest Products LaboratoryMadisonUSA

Personalised recommendations