Plant and Soil

, Volume 363, Issue 1–2, pp 257–271 | Cite as

Respiratory C fluxes and root exudation differ in two full-sib clones of Pinus taeda (L.) under contrasting fertilizer regimes in a greenhouse

  • Jeremy P. Stovall
  • John R. Seiler
  • Thomas R. Fox
Regular Article



We investigated whether changes in respiratory C fluxes, soil CO2 efflux, or root exudate quantity or quality explained differences in growth rates between closely related clones of Pinus taeda (L.).


A factorial design with two clones, fertilized and control treatments, and four sequential harvests was installed in a greenhouse for 121 days.


The two clones did show significant differences in respiratory C fluxes, soil CO2 efflux, and root exudation quantity and quality. While the clones also differed in growth rates, the C fluxes assessed in this paper did not explain how seedlings were able to allocate more C to stem growth in the months following fertilizer application. Changes in root exudation were not consistent with reduced heterotrophic soil CO2 efflux, which does not appear to be a plant-mediated process.


These results indicate that if single genotypes are deployed over large land areas in plantations, dramatic differences between clonal plant-soil interactions may require consideration in ecosystem C budgets. Further, the range of belowground fluxes observed implies that genotype-specific C allocation may make some clones better able to exploit a given resource environment than others.


Soil CO2 efflux Carbon allocation Intensive silviculture Varietal forestry 



Kelly Merkl, Matthew Seiler, Bonnie Stovall, and John Peterson helped out with sample processing. Chris Maier, Mike Aust, and Amy Brunner provided useful criticism and advice. Jeff Wright and Phil Dougherty at ArborGen provided the seedlings, and Kurt Johnsen and Pete Anderson of the USDA Forest Service helped us obtain the soil used in this study. Funding was provided by the NSF Center for Advanced Forestry Systems and the Forest Nutrition Cooperative.


  1. Adams DM, Haynes RW, Daigneault AJ (2006) Estimated timber harvest by U.S. region and ownership, 1950-2002. USDA Forest Service General Technical Report PNW-GTR-659. Pacific Northwest Research Station, Portland, p 64Google Scholar
  2. Albaugh TJ, Allen HL, Dougherty PM, Kress LW, King JS (1998) Leaf area and above- and belowground growth responses of loblolly pine to nutrient and water additions. Forest Sci 44:317–328Google Scholar
  3. Albaugh TJ, Allen HL, Fox TR (2007) Historical patterns of forest fertilization in the southeastern United States from 1969 to 2004. South J Appl Forest 31:129–137Google Scholar
  4. Bettinger P, Clutter M, Siry J, Kane M, Pait J (2009) Broad implications of southern United States pine clonal forestry on planning and management of forests. Int Forest Rev 11:331–345CrossRefGoogle Scholar
  5. Bitoki O (2008) Comparing early survival and growth of varietal and open-pollinated loblolly pine seedlings. VDOF Forest Research Review. p 4-5Google Scholar
  6. Bol R, Moering J, Kuzyakov Y, Amelung W (2003) Quantification of priming and CO2 respiration sources following slurry-C incorporation into two grassland soils with different C content. Rapid Commun Mass Spectrom 17:2585–2590PubMedCrossRefGoogle Scholar
  7. Bown HE, Watt MS, Clinton PW, Mason EG, Whitehead D (2009) The influence of N and P supply and genotype on carbon flux and partitioning in potted Pinus radiata plants. Tree Physiol 29:857–868PubMedCrossRefGoogle Scholar
  8. Butnor JR, Johnsen KH, Oren R, Katul GG (2003) Reduction of forest floor respiration by fertilization on both carbon dioxide-enriched and reference 17-year-old loblolly pine stands. Glob Chang Biol 9:849–861CrossRefGoogle Scholar
  9. Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–240CrossRefGoogle Scholar
  10. Conner RG, Hartsell AJ (2002) Forest area and condition. In: Weir DN, Greiss JG (eds) Southern forest resources assessment. USDA Forest Service, Southern Research Station, AshevilleGoogle Scholar
  11. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47CrossRefGoogle Scholar
  12. Egle K, Romer W, Keller H (2003) Exudation of low molecular weight organic acids by Lupinus albus L., Lupinus angustifolius L. and Lupinus luteus L. as affected by phosphorus supply. Agronomie 23:511–518CrossRefGoogle Scholar
  13. Fox TR, Comerford NB (1992) Influence of oxalate loading on phosphorus and aluminum solubility in spodosols. Soil Sci Soc Am J 56:290–294CrossRefGoogle Scholar
  14. Fox TR, Comerford NB, Mcfee WW (1990) Kinetics of phosphorus release from spodosols—effects of oxalate and formate. Soil Sci Soc Am J 54:1441–1447CrossRefGoogle Scholar
  15. Fox TR, Allen HL, Albaugh TJ, Rubilar R, Carlson CA (2007) Tree nutrition and forest fertilization of pine plantations in the southern United States. South J Appl Forest 31:5–11Google Scholar
  16. Giardina CP, Binkley D, Ryan MG, Fownes JH, Senock RS (2004) Belowground carbon cycling in a humid tropical forest decreases with fertilization. Oecologia 139:545–550PubMedCrossRefGoogle Scholar
  17. Gough CM, Seiler JR (2004) Belowground carbon dynamics in loblolly pine (Pinus taeda) immediately following diammonium phosphate fertilization. Tree Physiol 24:845–851PubMedCrossRefGoogle Scholar
  18. Grayston SJ, Vaughan D, Jones D (1997) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56CrossRefGoogle Scholar
  19. Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48:115–146CrossRefGoogle Scholar
  20. Henry F, Nguyen C, Paterson E, Sim A, Robin C (2005) How does nitrogen availability alter rhizodeposition in Lolium multiflorum Lam. during vegetative growth? Plant Soil 269:181–191CrossRefGoogle Scholar
  21. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  22. King NT, Seiler JR, Fox TR, Johnsen KH (2008) Post-fertilization physiology and growth performance of loblolly pine clones. Tree Physiol 28:703–711PubMedCrossRefGoogle Scholar
  23. Kuzyakov Y (2002) Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 165:382–396CrossRefGoogle Scholar
  24. Kuzyakov Y, Bol R (2006) Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biol Biochem 38:747–758CrossRefGoogle Scholar
  25. Lagomarsino A, Moscatelli MC, De Angelis P, Grego S (2006) Labile substrates quality as the main driving force of microbial mineralization activity in a poplar plantation soil under elevated CO2 and nitrogen fertilization. Sci Total Environ 372:256–265PubMedCrossRefGoogle Scholar
  26. Landi L, Valori F, Ascher J, Renella G, Falchini L, Nannipieri P (2006) Root exudate effects on the bacterial communities, CO2 evolution, nitrogen transformations and ATP content of rhizosphere and bulk soils. Soil Biol Biochem 38:509–516CrossRefGoogle Scholar
  27. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute Inc., CaryGoogle Scholar
  28. Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Chang Biol 13:2089–2109CrossRefGoogle Scholar
  29. Maier CA, Kress LW (2000) Soil CO2 evolution and root respiration in 11 year-old loblolly pine (Pinus taeda) plantations as affected by moisture and nutrient availability. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 30:347–359Google Scholar
  30. Maier CA, Albaugh TJ, Allen HL, Dougherty PM (2004) Respiratory carbon use and carbon storage in mid-rotation loblolly pine (Pinus taeda L.) plantations: the effect of site resources on the stand carbon balance. Glob Chang Biol 10:1335–1350CrossRefGoogle Scholar
  31. Mullins GL, Heckendorn SE (2009) Laboratory procedures: Virginia Tech soil testing laboratory. Publication 452-881, Virginia Cooperative Extension, BlacksburgGoogle Scholar
  32. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agronomie 23:375–396CrossRefGoogle Scholar
  33. Nguyen NT, Nakabayashi K, Thompson J, Fujita K (2003) Role of exudation of organic acids and phosphate in aluminum tolerance of four tropical woody species. Tree Physiol 23:1041–1050PubMedCrossRefGoogle Scholar
  34. Norman JM, Kucharik CJ, Gower ST, Baldocchi DD, Crill PM, Rayment M, Savage K, Striegl RG (1997) A comparison of six methods for measuring soil-surface carbon dioxide fluxes. J Geophys Res Atmos 102:28771–28777CrossRefGoogle Scholar
  35. Olsson P, Linder S, Giesler R, Hogberg P (2005) Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Glob Chang Biol 11:1745–1753CrossRefGoogle Scholar
  36. Paul AD, Foster GS, Caldwell T, McRae J (1997) Trends in genetic and environmental parameters for height, diameter, and volume in a multilocation clonal study with loblolly pine. Forest Science 43:87–98Google Scholar
  37. Pellet DM, Grunes DL, Kochian LV (1995) Organic-acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L). Planta 196:788–795CrossRefGoogle Scholar
  38. Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum-resistance mechanisms in wheat—roles of root apical phosphate and malate exudation. Plant Physiol 112:591–597PubMedGoogle Scholar
  39. Phillips RP, Fahey TJ (2007) Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol 176:655–664PubMedCrossRefGoogle Scholar
  40. Qin RJ, Hirano Y, Brunner I (2007) Exudation of organic acid anions from poplar roots after exposure to Al, Cu and Zn. Tree Physiol 27:313–320PubMedCrossRefGoogle Scholar
  41. Raich JW, Schlesinger WH (1992) The global carbon-dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B Chem Phys Meteorol 44:81–99CrossRefGoogle Scholar
  42. Ratnayake M, Leonard RT, Menge JA (1978) Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal formation. New Phytol 81:543–552CrossRefGoogle Scholar
  43. Ryan MG (1991) Effects of climate change on plant respiration. Ecol Appl 1:157–167CrossRefGoogle Scholar
  44. Ryan MG, Hubbard RM, Pongracic S, Raison RJ, McMurtrie RE (1996) Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status. Tree Physiol 16:333–343PubMedCrossRefGoogle Scholar
  45. Samuelson LJ (2000) Effects of nitrogen on leaf physiology and growth of different families of loblolly and slash pine. New Forests 19:95–107CrossRefGoogle Scholar
  46. Samuelson LJ, Johnsen K, Stokes T, Lu WL (2004) Intensive management modifies soil CO2 efflux in 6-year-old Pinus taeda L. stands. For Ecol Manage 200:335–345CrossRefGoogle Scholar
  47. Smith RL (1991) EPA Region 3 guidance on handling chemical concentration data near the detection limit in risk assessments. In US EPA Region 3 HSCD: Risk Assessment, Technical Guidance Manual. United States Environmental Protection Agency, PhiladelphiaGoogle Scholar
  48. Stovall JP, Fox TR, Seiler JR (2012) Short-term changes in biomass partitioning of two full-sib clones of Pinus taeda L. under differing fertilizer regimes over 4 months. Trees—Structure and FunctionGoogle Scholar
  49. Thirukkumaran CM, Parkinson D (2000) Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest floor amended with nitrogen and phosphorous fertilizers. Soil Biol Biochem 32:59–66CrossRefGoogle Scholar
  50. Tyree MC, Seiler JR, Aust WM, Sampson DA, Fox TR (2006) Long-term effects of site preparation and fertilization on total soil CO2 efflux and heterotrophic respiration in a 33-year-old Pinus taeda L. plantation on the wet flats of the Virginia Lower Coastal Plain. For Ecol Manage 234:363–369CrossRefGoogle Scholar
  51. Tyree MC, Seiler JR, Fox TR (2008) The effects of fertilization on soil respiration in 2-year-old Pinus taeda L. clones. Forest Science 54:21–30Google Scholar
  52. Valentini R, Matteucci G, Dolman AJ, Schulze ED, Rebmann C, Moors EJ, Granier A, Gross P, Jensen NO, Pilegaard K, Lindroth A, Grelle A, Bernhofer C, Grunwald T, Aubinet M, Ceulemans R, Kowalski AS, Vesala T, Rannik U, Berbigier P, Loustau D, Guomundsson J, Thorgeirsson H, Ibrom A, Morgenstern K, Clement R, Moncrieff J, Montagnani L, Minerbi S, Jarvis PG (2000) Respiration as the main determinant of carbon balance in European forests. Nature 404:861–865PubMedCrossRefGoogle Scholar
  53. Vose JM, Allen HL (1988) Leaf-area, stemwood growth, and nutrition relationships in loblolly-pine. Forest Science 34:547–563Google Scholar
  54. Vose JM, Ryan MG (2002) Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis. Glob Chang Biol 8:182–193CrossRefGoogle Scholar
  55. Werth M, Kuzyakov Y (2008) Root-derived carbon in soil respiration and microbial biomass determined by C-14 and C-13. Soil Biol Biochem 40:625–637CrossRefGoogle Scholar
  56. Wertin TM, Teskey RO (2008) Close coupling of whole-plant respiration to net photosynthesis and carbohydrates. Tree Physiol 28:1831–1840PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Jeremy P. Stovall
    • 1
    • 2
  • John R. Seiler
    • 1
  • Thomas R. Fox
    • 1
  1. 1.Department of Forest Resources and Environmental ConservationVirginia TechBlacksburgUSA
  2. 2.NacogdochesUSA

Personalised recommendations