The Response of Belowground Carbon Allocation in Forests to Global Change

Belowground carbon allocation (BCA) in forests regulates soil organic matter formation and influences biotic and abiotic properties of soil such as bulk density, cation exchange capacity, and water holding capacity. On a global scale, the total quantity of carbon allocated belowground by terrestrial plants is enormous, exceeding by an order of magnitude the quantity of carbon emitted to the atmosphere through combustion of fossil fuels. Despite the importance of BCA to the functioning of plant and soil communities, as well as the global carbon budget, controls on BCA are relatively poorly understood. Consequently, our ability to predict how BCA will respond to changes in atmospheric greenhouse gases, climate, nutrient deposition, and plant community composition remains rudimentary. In this synthesis, we examine BCA from three perspectives: coarse-root standing stock, belowground net primary production (BNPP), and total belowground carbon allocation (TBCA). For each, we examine methodologies and methodological constraints, as well as constraints of terminology. We then examine available data for any predictable variation in BCA due to changes in species composition, mean annual temperature, or elevated CO2 in existing Free Air CO2 Exposure (FACE) experiments. Finally, we discuss what we feel are important future directions for belowground carbon allocation research, with a focus on global change issues.

[1]  F. Smith,et al.  Age-related changes in production and below-ground carbon allocation in Pinus contorta forests , 1999 .

[2]  C. Giardina,et al.  Clear cutting and burning affect nitrogen supply, phosphorus fractions and seedling growth in soils from a Wyoming lodgepole pine forest , 2001 .

[3]  M. G. Ryan,et al.  Annual carbon cost of autotrophic respiration in boreal forest ecosystems in relation to species and climate , 1997 .

[4]  M. G. Ryan,et al.  Belowground and aboveground biomass in young postfire lodgepole pine forests of contrasting tree density , 2003 .

[5]  K. Vogt,et al.  A comparison of methods for estimating forest fine root production with respect to sources of error , 1993 .

[6]  J. Devereux Joslin,et al.  Disturbances During Minirhizotron Installation Can Affect Root Observation Data , 1999 .

[7]  M. G. Ryan,et al.  Dark respiration of pines , 1994 .

[8]  M. Lukac,et al.  Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE). , 2003 .

[9]  R. Ruess,et al.  Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska , 2003 .

[10]  P. Reich Effects of low concentrations of o(3) on net photosynthesis, dark respiration, and chlorophyll contents in aging hybrid poplar leaves. , 1983, Plant physiology.

[11]  S. Long,et al.  Free-air Carbon Dioxide Enrichment (FACE) in Global Change Research: A Review , 1999 .

[12]  John Grace,et al.  Respiration in the balance , 2000, Nature.

[13]  K. Pregitzer Fine roots of trees - a new perspective. , 2002, The New phytologist.

[14]  Jeffrey Q. Chambers,et al.  TROPICAL FORESTS : AN EVALUATION AND SYNTHESIS OF EXISTING FIELD DATA , 2022 .

[15]  N. E. Miller,et al.  Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Christina E. Wells,et al.  MARKED DIFFERENCES IN SURVIVORSHIP AMONG APPLE ROOTS OF DIFFERENT DIAMETERS , 2001 .

[17]  R. E. Dickson,et al.  Contrasting fine-root production, survival and soil CO2 efflux in pine and poplar plantations , 2000, Plant and Soil.

[18]  M. G. Ryan,et al.  Belowground carbon cycling in a humid tropical forest decreases with fertilization , 2004, Oecologia.

[19]  H. Mooney,et al.  Plant Physiological Ecology-Field Methods and Instrumentation. , 1990 .

[20]  J. Reynolds,et al.  Allometric relations and growth in Pinus taeda: the effect of elevated CO2, and changing N availability , 1996 .

[21]  E. Bååth,et al.  Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. , 2001, The New phytologist.

[22]  A. Bolte,et al.  Relationships between tree dimension and coarse root biomass in mixed stands of European beech (Fagus sylvatica L.) and Norway spruce (Picea abies[L.] Karst.) , 2004, Plant and Soil.

[23]  T. Hinckley,et al.  Influence of temperature and water potential on root growth of white oak , 1981 .

[24]  W. Schlesinger,et al.  Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem , 2000 .

[25]  E. Holland,et al.  Uncertainties in the temperature sensitivity of decomposition in tropical and subtropical ecosystems: Implications for models , 2000 .

[26]  H. Gholz Applications of Physiological Ecology to Forest Management , 1997 .

[27]  L. Ganio,et al.  Lifetime and temporal occurrence of ectomycorrhizae on ponderosa pine (Pinus ponderosa Laws.) seedlings grown under varied atmospheric CO2 and nitrogen levels , 1997, Plant and Soil.

[28]  P. Curtis,et al.  Atmospheric CO2, soil nitrogen and turnover of fine roots , 1995 .

[29]  Christina E. Wells,et al.  Building roots in a changing environment: implications for root longevity , 2000 .

[30]  K. Pregitzer,et al.  Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis , 2000 .

[31]  Christina E. Wells,et al.  Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae). , 2002, American journal of botany.

[32]  R. Norby,et al.  CO2 enrichment and warming of the atmosphere enhance both productivity and mortality of maple tree fine roots , 2004 .

[33]  J. Groenwold,et al.  The Relation between Root Growth along Observation Tubes and in Bulk Soil , 2015 .

[34]  Michael G. Ryan,et al.  Seasonal and annual respiration of a ponderosa pine ecosystem , 1999 .

[35]  L. Larsson,et al.  Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. , 2003, The New phytologist.

[36]  W. Kurz,et al.  Belowground biomass dynamics in the Carbon Budget Model of the Canadian Forest Sector: recent improvements and implications for the estimation of NPP and NEP , 2003 .

[37]  P. Hanson,et al.  Factors controlling the timing of root elongation intensity in a mature upland oak stand , 2004, Plant and Soil.

[38]  M. Coleman,et al.  Carbon allocation and nitrogen acquisition in a developing Populus deltoides plantation. , 2004, Tree physiology.

[39]  K. Pregitzer Woody plants, carbon allocation and fine roots. , 2003, The New phytologist.

[40]  L. Finér,et al.  Root dynamics at drained peatland sites of different fertility in southern Finland , 1998, Plant and Soil.

[41]  E. Davidson,et al.  Belowground carbon allocation in forests estimated from litterfall and IRGA-based soil respiration measurements , 2002 .

[42]  M. G. Messina,et al.  Southern Forested Wetlands: Ecology and Management , 1998 .

[43]  M. Coleman,et al.  Forest production responses to irrigation and fertilization are not explained by shifts in allocation , 2005 .

[44]  M. Sancholle,et al.  Sterol distribution in arbuscular mycorrhizal fungi , 1999 .

[45]  M. G. Ryan,et al.  Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status. , 1996, Tree physiology.

[46]  C. Giardina,et al.  Primary production and carbon allocation in relation to nutrient supply in a tropical experimental forest , 2003 .

[47]  H. L. Allen,et al.  Leaf Area and Above- and Belowground Growth Responses of Loblolly Pine to Nutrient and Water Additions , 1998, Forest Science.

[48]  W. Horwath,et al.  14C Allocation in tree-soil systems. , 1994, Tree physiology.

[49]  S. M. Atkinson That sinking feeling. , 2005, Annals of emergency medicine.

[50]  Carl C. Trettin,et al.  Carbon Cycling in Wetland Forest Soils , 2003 .

[51]  K. Nadelhoffer,et al.  Fine Root Production Estimates and Belowground Carbon Allocation in Forest Ecosystems , 1992 .

[52]  W. Schlesinger,et al.  The influence of elevated atmospheric CO2 on fine root dynamics in an intact temperate forest , 2001 .

[53]  Christian P. Giardina,et al.  Reduction of soil carbon formation by tropospheric ozone under increased carbon dioxide levels , 2003, Nature.

[54]  J. L. Chambers,et al.  Root dynamics in bottomland hardwood forests of the Southeastern United States Coastal Plain , 2003, Plant and Soil.

[55]  P. Mucha,et al.  Fluid dynamics: That sinking feeling , 2001, Nature.

[56]  Knute J. Nadelhoffer,et al.  Belowground Carbon Allocation in Forest Ecosystems: Global Trends , 1989 .

[57]  Yiqi Luo Uncertainties in interpretation of isotope signals for estimation of fine root longevity: theoretical considerations , 2003 .

[58]  M. G. Ryan,et al.  Eucalyptus production and the supply, use and efficiency of use of water, light and nitrogen across a geographic gradient in Brazil , 2004 .

[59]  R. Fogel,et al.  Contribution of mycorrhizae and soil fungi to nutrient cycling in a Douglas-fir ecosystem , 1983 .

[60]  P. Curtis,et al.  ATMOSPHERIC CO2 AND THE COMPOSITION AND FUNCTION OF SOIL MICROBIAL COMMUNITIES , 2000 .

[61]  Thomas H. Painter,et al.  Climatic, edaphic, and biotic controls over storage and turnover of carbon in soils , 1994 .

[62]  H. Lyr,et al.  Growth Rates and Growth Periodicity of Tree Roots , 1967 .

[63]  Kurt S. Pregitzer,et al.  THE DEMOGRAPHY OF FINE ROOTS IN A NORTHERN HARDWOOD FOREST , 1992 .

[64]  S. Gower,et al.  Belowground carbon allocation in unfertilized and fertilized red pine plantations in northern Wisconsin. , 1995, Tree physiology.

[65]  M. G. Ryan,et al.  Total Belowground Carbon Allocation in a Fast-growing Eucalyptus Plantation Estimated Using a Carbon Balance Approach , 2002, Ecosystems.

[66]  D. Phillips,et al.  Advancing fine root research with minirhizotrons. , 2001, Environmental and experimental botany.

[67]  R. Mitchell,et al.  Rapid fine root disappearance in a pine woodland: a substantial carbon flux , 2002 .

[68]  G. Taylor,et al.  Elevated CO2 and tree root growth: contrasting responses in Fraxinus excelsior, Quercus petraea and Pinus sylvestris. , 1998, The New phytologist.

[69]  G. Berntson,et al.  Growth and mycorrhizal colonization of three North American tree species under elevated atmospheric CO2. , 1997, The New phytologist.

[70]  R. B. Jackson,et al.  Ecosystem carbon loss with woody plant invasion of grasslands , 2002, Nature.

[71]  G. Berntson,et al.  The allometry of root production and loss in seedlings of Acer rubrum (Aceraceae) and Betula papyrifera (Betulaceae): implications for root dynamics in elevated CO2 , 1996 .

[72]  G. Shaver,et al.  Productivity of Arctic Ecosystems , 2001 .

[73]  K. Minkkinen,et al.  Long-term effect of forest drainage on the peat carbon stores of pine mires in Finland , 1998 .

[74]  K. Pregitzer,et al.  Patterns of fine root mortality in two sugar maple forests , 1993, Nature.

[75]  H. M. Taylor Minirhizotron observation tubes : methods and applications for measuring rhizosphere dynamics , 1987 .

[76]  K. Pregitzer,et al.  Temporal and depth-related patterns of fine root dynamics in northern hardwood forests , 1996 .

[77]  J. Sarmiento That sinking feeling , 2000, Nature.

[78]  P. Reich,et al.  Ambient Levels of Ozone Reduce Net Photosynthesis in Tree and Crop Species , 1985, Science.

[79]  Michael G. Ryan,et al.  Below-ground process responses to elevated CO2 and temperature: a discussion of observations, measurement methods, and models , 2004 .

[80]  J. D. Ovington,et al.  Dry-matter Production by Pinus sylvestris L. , 1957 .

[81]  Paul D. Allison,et al.  Survival analysis using sas®: a practical guide , 1995 .

[82]  K. Pregitzer,et al.  Responses of tree fine roots to temperature , 2000 .

[83]  J. Coleman,et al.  BIOMASS ALLOCATION IN PLANTS: ONTOGENY OR OPTIMALITY? A TEST ALONG THREE RESOURCE GRADIENTS , 1999 .

[84]  R. B. Jackson,et al.  Global patterns of root turnover for terrestrial ecosystems , 2000 .

[85]  Ü. Rannik,et al.  Productivity overshadows temperature in determining soil and ecosystem respiration across European forests , 2001 .

[86]  N. McDowell,et al.  Belowground carbon allocation of Rocky Mountain Douglas-fir , 2001 .

[87]  John M. Norman,et al.  Root mass, net primary production and turnover in aspen, jack pine and black spruce forests in Saskatchewan and Manitoba, Canada. , 1997, Tree physiology.

[88]  Harold A. Mooney,et al.  Terrestrial Global Productivity , 2001 .

[89]  S. T. Gower,et al.  A global relationship between the heterotrophic and autotrophic components of soil respiration? , 2004 .

[90]  Jean-Francois Lamarque,et al.  Variations in the predicted spatial distribution of atmospheric nitrogen deposition and their impact on carbon uptake by terrestrial ecosystems , 1997 .

[91]  R. Yanai,et al.  The Ecology of Root Lifespan , 1997 .

[92]  D. Binkley,et al.  Soil Functional Responses to Excess Nitrogen Inputs at Global Scale , 2004, Ambio.

[93]  K. Paustian,et al.  Measuring and understanding carbon storage in afforested soils by physical fractionation , 2002 .

[94]  R. B. Jackson,et al.  Variation in Xylem Structure and Function in Stems and Roots of Trees to 20 M Depth , 2004 .

[95]  Christina E. Wells,et al.  Soil insects alter fine root demography in peach (Prunus persica) , 2002 .

[96]  N. Buchmann,et al.  Large-scale forest girdling shows that current photosynthesis drives soil respiration , 2001, Nature.

[97]  R. B. Jackson,et al.  Root dynamics and global change : seeking an ecosystem perspective , 2000 .

[98]  D. Binkley,et al.  CHANGES IN SOIL CARBON FOLLOWING AFFORESTATION IN HAWAII , 1998 .

[99]  P. Groffman,et al.  Environmental control of fine root dynamics in a northern hardwood forest , 2003 .

[100]  G. Lovett,et al.  Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska , 2002 .

[101]  Julie D. Jastrow,et al.  Impacts of Fine Root Turnover on Forest NPP and Soil C Sequestration Potential , 2003, Science.

[102]  R. J. Olson,et al.  NET PRIMARY PRODUCTION AND CARBON ALLOCATION PATTERNS OF BOREAL FOREST ECOSYSTEMS , 2001 .

[103]  D. Binkley,et al.  Rapid changes in soils following eucalyptus afforestation in Hawaii , 1999 .

[104]  Jane M. F. Johnson,et al.  Fine root dynamics in a developing Populus deltoides plantation. , 2004, Tree physiology.

[105]  Karl J Niklas,et al.  Global Allocation Rules for Patterns of Biomass Partitioning in Seed Plants , 2002, Science.

[106]  Stan D. Wullschleger,et al.  Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage , 2002 .

[107]  K. Pregitzer,et al.  Clonal variation in above- and below-ground growth responses of Populus tremuloides Michaux: Influence of soil warming and nutrient availability , 1999, Plant and Soil.

[108]  P. Reich,et al.  Productivity of Evergreen and Deciduous Temperate Forests , 2001 .

[109]  Keryn I. Paul,et al.  Change in soil carbon following afforestation , 2002 .

[110]  J. Aber,et al.  Soil warming and carbon-cycle feedbacks to the climate system. , 2002, Science.

[111]  E. Paul,et al.  Soil microbiology and biochemistry. , 1998 .

[112]  Stan D. Wullschleger,et al.  Productivity and compensatory responses of yellow-poplar trees in elevated C02 , 1992, Nature.

[113]  Vemap Participants Vegetation/ecosystem modeling and analysis project: Comparing biogeography and biogeochemistry models in a continental-scale study of terrestrial ecosystem responses to climate change and CO2 doubling , 1995 .

[114]  R. K. Hermann,et al.  Standing crop, production, and turnover of fine roots on dry, moderate, and wet sites of mature Douglas-fir in western Oregon , 1985 .

[115]  G. Lovett,et al.  ECTOMYCORRHIZAL FUNGAL ABOVEGROUND COMMUNITY CHANGE OVER AN ATMOSPHERIC NITROGEN DEPOSITION GRADIENT , 2001 .

[116]  P. Curtis,et al.  INTERACTIVE EFFECTS OF ATMOSPHERIC CO2 AND SOIL‐N AVAILABILITY ON FINE ROOTS OF POPULUS TREMULOIDES , 2000 .

[117]  K. Pregitzer,et al.  The relationship between fine root demography and the soil environment in northern hardwood forests , 1997 .

[118]  R. Birdsey,et al.  The Potential of U.S. Forest Soils to Sequester Carbon and Mitigate the Greenhouse Effect , 2002 .

[119]  R. Norby,et al.  Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi‐factor world , 2004 .

[120]  Roderick C. Dewar,et al.  Carbon Allocation in Trees: a Review of Concepts for Modelling , 1994 .

[121]  E. Davidson,et al.  The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures , 1994, Nature.

[122]  Peter B Reich,et al.  The impact of material used for minirhizotron tubes for root research. , 2003, The New phytologist.

[123]  R. Ruess,et al.  Root respiration in North American forests: effects of nitrogen concentration and temperature across biomes , 2002, Oecologia.

[124]  K. Treseder A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. , 2004, The New phytologist.

[125]  J. King,et al.  Growth and carbon accumulation in root systems of Pinus taeda and Pinus ponderosa seedlings as affected by varying CO(2), temperature and nitrogen. , 1996, Tree physiology.

[126]  Allen,et al.  Stand-level allometry in Pinus taeda as affected by irrigation and fertilization. , 1999, Tree physiology.

[127]  K. Pregitzer,et al.  Field measurements of root respiration indicate little to no seasonal temperature acclimation for sugar maple and red pine. , 2003, Tree physiology.

[128]  A. Fitter,et al.  Root production and turnover in an upland grassland subjected to artificial soil warming respond to radiation flux and nutrients, not temperature , 1999, Oecologia.

[129]  D. Livingstone Some Interstadial and Postglacial Pollen Diagrams from Eastern Canada , 1968 .

[130]  Michael G. Ryan,et al.  EFFECTS OF TREE DENSITY AND STAND AGE ON CARBON ALLOCATION PATTERNS IN POSTFIRE LODGEPOLE PINE , 2004 .

[131]  R. E. Dickson,et al.  Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project , 2003 .

[132]  K. Vogt,et al.  Biomass distribution and above- and below-ground production in young and mature Abiesamabilis zone ecosystems of the Washington Cascades , 1981 .

[133]  Michael G. Ryan,et al.  Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature , 2000, Nature.

[134]  R. Qualls,et al.  Effects of increased atmospheric CO2, temperature, and soil N availability on root exudation of dissolved organic carbon by a N-fixing tree (Robinia pseudoacacia L.) , 2000, Plant and Soil.

[135]  Joyce E. Penner,et al.  Spatial and Temporal Patterns in Terrestrial Carbon Storage Due to Deposition of Fossil Fuel Nitrogen , 1996 .

[136]  C. C. Grier,et al.  Above- and below-ground net production in 40-year-old Douglas-fir stands on low and high productivity sites , 1981 .

[137]  J. Burke,et al.  Soil Temperature and Root Growth , 1998 .

[138]  B. Enquist Universal scaling in tree and vascular plant allometry: toward a general quantitative theory linking plant form and function from cells to ecosystems. , 2002, Tree physiology.

[139]  J. Aber,et al.  The Role of Fine Roots in the Organic Matter and Nitrogen Budgets of Two Forested Ecosystems , 1982 .