[an error occurred while processing this directive] [an error occurred while processing this directive] [an error occurred while processing this directive]
[an error occurred while processing this directive]

Advances in the carbon use efficiency of forest

Expand
  • Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu 610041, China

Received date: 2013-05-27

  Accepted date: 2013-10-05

  Online published: 2013-11-06

Abstract

Carbon use efficiency (CUE), which is defined as the ratio of net carbon gain to gross carbon assimilation, can be used to assess not only the capacity of forests to transfer carbon from the atmosphere to the terrestrial biomass but also to determine the impact of respiration on productivity in forests. CUE is an important parameter for comparing carbon cycle variability among ecosystems. Understanding such controls on CUE can be helpful in determining whether the terrestrial ecosystem is a carbon source or sink. Forest CUE under different environmental regimes and global change scenarios has recently received increasing attention. This paper introduces the calculation methods of plant CUE and the corresponding measurement techniques, and reviews the research progress in the effects of important factors on forest CUE. The main findings are as follows: (1) Some studies proposed that CUE is constant among forests with a possible appropriate universal value of 0.50. However, it is doubtful whether this conservative CUE assumption regardless of ecosystem types is globally applicable. CUE can vary with ecosystems, forest types, species, and ontogeny of plant development. Forest ecosystems have a lower CUE than shrub and herbaceous ecosystems. CUE is significantly higher in deciduous than in mixed and evergreen forests. Tropical forests often have lower CUE than temperate forests. CUE is known to depend on successional stage and stand age. (2) Forest CUE is related to temperature, precipitation, and geographical factors. A parabolic relationship between CUE and annual mean temperature is founded at a global scale. Acclimation of the respiration to temperature contributes to high carbon-use efficiency in seasonally dry vegetation. The CUE decreases with enhanced precipitation and remains unchanged in areas where water availability is in surplus. CUE of plants grown at low light level is low. (3) The elevated CO2 may increase whole-plant respiration, causing CUE to decline. The potential for elevated CO2 to affect CUE may depend on tree age or genotype. (4) Plants grown on the barren soil, and under low temperature and drought conditions, may have larger changes in CUE than plants grown under near-optimal conditions. Forest managements such as irrigation, fertilization, and selective logging can affect ecosystem CUE. (5) CUE varies widely with the changing seasons within a year. The maximum of CUE in temperate forests usually occurs in spring. The future research should be focused on: (1) exploring the spatial variations in forest CUE and their driving mechanism from tissues, individual plant, community, to ecosystem scales; (2) analyzing the processes and mechanism in CUE of different vegetation types at temporal scales by combining the plant eco-physiology and biology with eddy covariance technique and modeling approaches; and (3) evaluating the response and adaption of forest CUE to climate change by synergistic experiments of multi-factors.

Cite this article

ZHU Wan-Ze . Advances in the carbon use efficiency of forest[J]. Chinese Journal of Plant Ecology, 2013 , 37(11) : 1043 -1058 . DOI: 10.3724/SP.J.1258.2013.00108

[an error occurred while processing this directive]

References

[1] Albrizio R, Steduto P (2003). Photosynthesis, respiration and conservative carbon use efficiency of four field grown crops. Agricultural and Forest Meteorology, 116, 19-36.
[2] Allison SD, Wallenstein MD, Bradford MA (2010). Soil-carbon response to warming dependent on microbial physiology. Nature Geoscience, 3, 336-340.
[3] Amthor JS (1989). Respiration and Crop Productivity. Springer-Verlag, New York.
[4] Amthor JS (1994). Plant respiratory responses to the environment and their effects on the carbon balance. In: Wilkinson RE ed. Plant-Environment Interactions. Marcel Dekker, New York. 501-554.
[5] Amthor JS (2000). The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later. Annals of Botany, 86, 1-20.
[6] Arag?o LEOC, Malhi Y, Metcalfe DB, Silva-Espejo JE, Jiménez E, Navarrete D, Almeida S, Costa ACL, Salinas N, Phillips OL, Anderson LO, Alvarez E, Baker TR, Goncalvez PH, Huamán-Ovalle J, Mamani-Solórzano M, Meir1 P, Monteagudo A, Pati?o S, Pe?uela MC, Prieto A, Quesada CA, Rozas-Dávila A, Rudas A, Silva JA Jr, Vásquez R (2009). Above- and below-ground net primary productivity across ten Amazonian forests on contrasting soils. Biogeosciences, 6, 2759-2778.
[7] Arneth A, Kelliher FM, McSeveny TM, Byers JN (1998). Net ecosystem productivity, net primary productivity and ecosystem carbon sequestration in a Pinus radiata plantation subject to soil water deficit. Tree Physiology, 18, 785-793.
[8] Arnone JA, K?rner C (1997). Temperature adaptation and acclimation potential of leaf dark respiration in two species of Ranunculus from warm and cold habitats. Arctic and Alpine Research, 29, 122-125.
[9] Atkin OK, Atkinson LJ, Fisher RA, Campbell CD, Castells JZ, Pitchford JW, Woodward FI, Hurry V (2008). Using temperature-dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate-vegetation model. Global Change Biology, 14, 2709-2726.
[10] Atkin OK, Bruhn D, Hurry VW, Tjoelker MG (2005). The hot and the cold: unravelling the variable response of plant respiration to temperature. Functional Plant Biology, 32, 87-105.
[11] Atkin OK, Evans JR, Ball MC, Lumbers H, Pons TL (2000). Leaf respiration of snow gum in the light and dark: interactions between temperature and irradiance. Plant Physiology, 122, 915-923.
[12] Atkin OK, Scheurwater I, Pons TL (2006). High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Global Change Biology, 12, 500-515.
[13] Azcón-Bieto J, Osmond CB (1983). Relationship between photosynthesis and respiration: the effect of carbohydrate status on the rate of CO2 production by respiration in darkened and illuminated wheat leaves. Plant Physiology, 71, 574-581.
[14] Baldocchi D, Falge E, Gu LH, Olson R, Hollinger D, Running S, Anthoni P, Bernhofer C, Davis KJ, Evans R, Fuentes J, Goldstein A, Katul G, Law BE, Lee Z, Malhi Y, Meyers T, Munger WJ, Oechel W, Paw UKT, Pilegaard K, Schmid HP, Valentini R, Verma S, Vesala T, Wilson KB, Wofsy S (2001). FLUXNET: a new tool to study the temporal and spatial variability of ecosystem-scale carbon dioxide, water vapor, and energy flux densities. Bulletin of the American Meteorological Society, 82, 2415-2434.
[15] Baldocchi DD, Hincks BB, Meyers TP (1988). Measuring biosphere-atmosphere exchanges of biologically related gases with micrometeorological methods. Ecology, 69, 1331-1340.
[16] Bolstad PV, Davis KJ, Martin J, Cook BD, Wang W (2004). Component and whole-system respiration fluxes in northern deciduous forests. Tree Physiology, 24, 493-504.
[17] Bolstad PV, Reich P, Lee T (2003). Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra. Tree Physiology, 23, 969-976.
[18] Bown HE (2007). Representing Nutrition of Pinus radiata in Physiological Hybrid Productivity Models. PhD dissertation, University of Canterbury, Christchurch, New Zealand.
[19] Bradford MA, Crowther TW (2013). Carbon use efficiency and storage in terrestrial ecosystems. New Phytologist, 199, 7-9.
[20] Campioli M, Gielen B, G?ckede M, Papale D, Bouriaud O, Granier A (2011). Temporal variability of the NPP:GPP ratio at seasonal and interannual time scales in a temperate beech forest. Biogeosciences, 8, 2481-2492.
[21] Canadell JG, Mooney HA, Baldocchi DD, Berry JA, Ehleringer JR, Field CB, Gower ST, Hollinger DY, Hunt JE, Jackson RB, Running SW, Shaver GR, Steffen W, Trumbore SE, Valentini R, Bond BY (2000). Carbon metabolism of the terrestrial biosphere: a multi-technique approach for improved understanding. Ecosystems, 3, 115-130.
[22] Cannell MGR (1989). Physiological basis of wood production: a review. Scandinavian Journal of Forest Research, 4, 459-490.
[23] Cannell MGR, Thornley JHM (2000). Modelling the components of plant respiration: some guiding principles. Annals of Botany, 85, 45-54.
[24] Cavaleri MA, Oberbauer SF, Ryan MG (2008). Foliar and ecosystem respiration in an old-growth tropical rain forest. Plant, Cell & Environment, 31, 473-483.
[25] Chambers JQ, Tribuzy ES, Toledo LC, Crispim BF, Higuchi N, dos Santos J, Araújo AC, Kruijt B, Nobre AD, Trumbore SE (2004). Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency. Ecological Applications, 14, 72-88.
[26] Chapin FS III, Matson PA, Vitousek P, Chapin MC (2002). Principles of Terrestrial Ecosystem Ecology. Springer- Verlag, New York.
[27] Chen GS, Yang YS, Gao R, Xie JS, Yang ZJ, Mao YL (2008). Changes in belowground carbon allocation in a Chinese fir chronosequence in Fujian Province, China. Journal of Plant Ecology (Chinese Version), 32, 1285-1293.
[27] [ 陈光水, 杨玉盛, 高人, 谢锦升, 杨智杰, 毛艳玲 (2008). 杉木林年龄序列地下碳分配变化. 植物生态学报, 32, 1285-1293.]
[28] Chen GS, Yang YS, Guo JF, Xie JS, Yang ZJ (2011). Relationships between carbon allocation and partitioning of soil respiration across world mature forests. Plant Ecology, 212, 195-206.
[29] Cheng WX, Sims DA, Luo YQ, Coleman JS, Johnson DW (2000). Photosynthesis, respiration, and net primary production of sunflower stands in ambient and elevated atmospheric CO2 concentrations: an invariant NPP:GPP ratio? Global Change Biology, 6, 931-941.
[30] Choudhury BJ (2000). Carbon use efficiency, and net primary productivity of terrestrial vegetation. Advances in Space Research, 26, 1105-1108.
[31] Clark DB, Mercado LM, Sitch S, Jones CD, Gedney N, Best MJ, Pryor M, Rooney GG, Essery RLH, Blyth E, Boucher O, Harding RJ, Huntingford C, Cox PM (2011). The Joint UK Land Environment Simulator (JULES), model description―Part 2: carbon fluxes and vegetation dynamics. Geoscientific Model Development, 4, 701-722.
[32] Cox PM (2001). Description of the “TRIFFID” dynamic global vegetation model. Hadley Centre Technical Note, 24, 1-16.
[33] Crowther TW, Bradford MA (2013). Thermal acclimation in widespread heterotrophic soil microbes. Ecology Letters, 16, 469-477.
[34] Curtis PS, Vogel CS, Gough CM, Schmid HP, Su HB, Bovard BD (2005). Respiratory carbon losses and the carbon use efficiency of a northern hardwood forest, 1999-2003. New Phytologist, 167, 437-456.
[35] DeLucia EH, Drake JE, Thomas RB, Gonzalez-Meler M (2007). Forest carbon use efficiency: Is respiration a constant fraction of gross primary production? Global Change Biology, 13, 1157-1167.
[36] DeLucia EH, George K, Hamilton JG (2002). Radiation-use efficiency of a forest exposed to elevated concentrations of atmospheric carbon dioxide. Tree Physiology, 22, 1003-1010.
[37] DeLucia EH, Moore DJ, Norby RJ (2005). Contrasting responses of forest ecosystems to rising atmospheric CO2: implications for the global C cycle. Global Biogeo- chemical Cycles, 19, GB3006. doi: 10.1029/2004GB-002346.
[38] Dewar RC, Medlyn BE, McMurtrie RE (1998). A mechanistic analysis of light and carbon use efficiencies. Plant, Cell & Environment, 21, 573-588.
[39] Dewar RC, Medlyn BE, McMurtrie RE (1999). Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model. Global Change Biology, 5, 615-622.
[40] Dillaway DN, Kruger EL (2011). Leaf respiratory acclimation to climate: comparisons among boreal and temperate tree species along a latitudinal transect. Tree Physiology, 31, 1114-1127.
[41] Enquist BJ, Kerkhoff AJ, Stark SC, Swenson NG, McCarthy MC, Price CA (2007). A general integrative model for scaling plant growth, carbon flux, and functional trait spectra. Nature, 449, 218-222.
[42] Falge E, Baldocchi D, Tenhunen J, Aubinet M, Bakwin P, Berbigier P, Bernhofer C, Burba G, Clement R, Davis KJ, Elbers JA, Goldstein AH, Grelle A, Granier A, Gu?mundsson J, Hollinger D, Kowalski AS, Katul G, Law BE, Malhi Y, Meyers T, Monson RK, Munger JW, Oechel W, Paw UKT, Pilegaard K, Rannik U, Rebmann C, Suyker A, Valentini R, Wilson K, Wofsy S (2002). Seasonality of ecosystem respiration and gross primary production as derived from FLUXNET measurements. Agricultural and Forest Meteorology, 113, 53-74.
[43] Figueira AMeS, Miller SD, de Sousa CAD, Menton MC, Maia AR, da Rocha HR, Goulden ML (2008). Effects of selective logging on tropical forest tree growth. Journal of Geophysical Research, 113, G00B05. doi: 10.1029/2007JG000577.
[44] Fisher JB, Sitch S, Malhi Y, Fisher RA, Huntingford C, Tan SY (2010). Carbon cost of plant nitrogen acquisition: a mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation. Global Biogeochem- ical Cycles, 24, GB1014. doi: 10.1029/2009GB003621.
[45] Frantz JM, Bugbee B (2005). Acclimation of plant populations to shade: photosynthesis, respiration, and carbon use ef?ciency. Journal of the American Society for Horticultural Science, 130, 918-927.
[46] Frantz JM, Cometti NN, Bugbee B (2004). Night temperature has a minimal effect on respiration and growth in rapidly growing plants. Annals of Botany, 94, 155-166.
[47] Frantz JM, Cometti NN, van Iersel MW, Bugbee B (2007). Rethinking acclimation of growth and maintenance respiration of tomato in elevated CO2: effects of a sudden change in light at different temperatures. Journal of Plant Ecology (Chinese Version)(植物生态学报), 31, 695-710.
[48] Frey SD, Lee J, Melillo JM, Six J (2013). The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change, 3, 395-398.
[49] Friend AD, Woodward FI (1990). Evolutionary and ecophysiological responses of mountain plants to the growing environment. Advances in Ecological Research, 20, 59-124.
[50] Giardina CP, Ryan MG, Binkley D, Fownes JH (2003). Primary production and carbon allocation in relation to nutrient supply in a tropical experimental forest. Global Change Biology, 9, 1438-1450.
[51] Gielen B, Calfapietra C, Lukac M, Wittig VE, de Angelis P, Janssens IA, Moscatelli MC, Grego S, Cotrufo MF, Godbold DL, Hoosbeek MR, Long SP, Miglietta F, Polle A, Bernacchi CJ, Davey PA, Ceulemans R, Scarascia- Mugnozza GE (2005). Net carbon storage in a poplar plantation (POPFACE) after three years of free-air CO2 enrichment. Tree Physiology, 25, 1399-1408.
[52] Gifford RM (1994). The global carbon cycle: a viewpoint on the missing sink. Australian Journal of Plant Physiology, 21, 1-15.
[53] Gifford RM (1995). Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long-term vs. short-term distinctions for modeling. Global Change Biology, 1, 385-396.
[54] Gifford RM (2003). Plant respiration in productivity models: conceptualisation, representation and issues for global terrestrial carbon-cycle research. Functional Plant Biology, 30, 171-186.
[55] Girardin CAJ, Silva Espejob JE, Doughty CE, Huasco WH, Metcalfe DB, Durand-Baca L, Marthews TR, Aragao LEOC, Farfán-Rios W, García-Cabrera K, Halladay K, Fisher JB, Galiano-Cabrera DF, Huaraca-Quispe LP, Alzamora-Taype I, Eguiluz-Mora L, Salinas-Revilla N, Silman MR, Meir P, Malhi Y (2014). Productivity and carbon allocation in a tropical montane cloud forest in the Peruvian Andes. Plant Ecology & Diversity, doi: 10.1080/17550874.2013.820222.
[56] Girardin MP, Guo XJ, Bernier PY, Raulier F, Gauthier S (2012). Changes in growth of pristine boreal North American forests from 1950 to 2005 driven by landscape demographics and species traits. Biogeosciences, 9, 2523-2536.
[57] Goetz SJ, Prince SD (1998). Variability in carbon exchange and light utilization among boreal forest stands: implications for remote sensing of net primary production. Canadian Journal of Forest Research, 28, 375-389.
[58] Goulden ML, Daube BC, Fan SM, Sutton DJ, Bazzaz A, Munger JW, Wofsy SC (1997). Physiological responses of a black spruce forest to weather. Journal of Geophysical Research, 102, 28987-28996.
[59] Goulden ML, McMillan AMS, Winston GC, Rocha AV, Maniesw KL, Hardenw JW, Bond-Lamberty BP (2011). Patterns of NPP, GPP, respiration, and NEP during boreal forest succession. Global Change Biology, 17, 855-871.
[60] Gower ST (2002). Net primary production. In: Mooney HA, Canadell JG eds. Encyclopedia of Global Environmental Change: the Earth System: Biological and Ecological Dimensions of Global Environmental Change. Wiley, New York.
[61] Grace J, Lloyd J, McIntyre J, Miranda AC, Meir P, Miranda HS, Nobre C, Moncrieff J, Massheder J, Malhi Y, Wright I, Gash J (1995). Carbon dioxide uptake by an undisturbed tropical rain forest in Southwest Amazonia, 1992 to 1993. Science, 270, 778-780.
[62] Griffin KL (1994). Calorimetric estimates of construction cost and their use in ecological studies. Functional Ecology, 8, 551-562.
[63] Hamilton JG, DeLucia EH, George K, Naidu SL, Finzi AC, Schlesinger WH (2002). Forest carbon balance under elevated CO2. Oecologia, 131, 250-260.
[64] Huasco WH, Girardin CAJ, Doughty CE, Metcalfe DB, Baca LD, Silva-Espejo JE, Cabrera DG, Arag?o LEOC, Davila AR, Marthews TR, Huaraca-Quispe LP, Alzamora-Taype I, Mora LE, Farfán-Rios W, Cabrera KG, Halladay K, Salinas-Revilla N, Silman MR, Meir P, Malhi Y (2014). Seasonal production, allocation and cycling of carbon in two mid-elevation tropical montane forest plots in the Peruvian Andes. Plant Ecology & Diversity. doi: 10.1080/17550874.2013.819042.
[65] Ise T, Litton CM, Giardina CP, Ito A (2010). Comparison of modeling approaches for carbon partitioning: impact on estimates of global net primary production and equilibrium biomass of woody vegetation from MODIS GPP. Journal of Geophysical Research, 115, G04025. doi: 10.1029/2010JG001326.
[66] Jarvis PG, Leverenz JW (1983). Productivity of temperate, deciduous and evergreen forests. Encyclopedia of Plant Physiology, 12, 233-280.
[67] Kerkhoff AJ, Enquist BJ, Elser JJ, Fagan WF (2005). Plant allometry, stoichiometry and the temperature-dependence of primary productivity. Global Ecology and Biogeography, 14, 585-598.
[68] Kinerson RS, Ralston CW, Wells CG (1977). Carbon cycling in a loblolly pine plantation. Oecologia, 29, 1-10.
[69] Kira T (1977). Production rates. In: Shidei T, Kira T eds. Primary Productivity of Japanese Forests. University of Tokyo Press, Tokyo. 101-114.
[70] Kira T (1978). Community architecture and organic matter dynamics in tropical lowland rain forests of Southeast Asia with special reference to Pasoh Forest, West Malaysia. In: Tomlinson PB, Zimmerman MH eds. Tropical Trees as Living Systems. Cambridge University Press, New York. 561-590.
[71] Kira T, Shidei T (1967). Primary production and turnover of organic matter in different forest ecosystems of the western Pacific. Japanese Journal of Ecology, 17, 70-87.
[72] Kwon Y, Larsen CPS (2013). Effects of forest type and environmental factors on forest carbon use efficiency assessed using MODIS and FIA data across the eastern USA. International Journal of Remote Sensing, 34, 8425-8448.
[73] Lai CT, Katul G, Butnor J, Siqueira M, Ellsworth D, Maier C, Johnsen K, Mckeand S, Oren R (2002). Modelling the limits on the response of net carbon exchange to fertilization in a southeastern pine forest. Plant, Cell & Environment, 25, 1095-1119.
[74] Landsberg JJ, Gower ST (1997) Applications of Physiological Ecology to Forest Management. Academic Press, San Diego, USA.
[75] Landsberg JJ, Sands P (2011). Physiological Ecology of Forest Production. Academic Press, Amsterdam, The Netherlands.
[76] Landsberg JJ, Waring RH (1997). A generalized model of forest productivity using simplified concepts of radiation-use efficiency, carbon balance and partitioning. Forest Ecology and Management, 95, 209-228.
[77] Lavigne MB (1988). Stem growth and respiration of young balsam fir trees in thinned and unthinned stands. Canadian Journal of Forest Research, 18, 483-489.
[78] Lavigne MB (1996). Comparing stem respiration and growth of jack pine provenances from southern and northern locations. Tree Physiology, 16, 847-852.
[79] Lavigne MB, Ryan MG (1997). Growth and maintenance respiration rates of aspen, black spruce and jack pine stems at northern and southern BOREAS sites. Tree Physiology, 17, 543-551.
[80] Law BE, Ryan MG, Anthoni PM (1999). Seasonal and annual respiration of a ponderosa pine ecosystem. Global Change Biology, 5, 169-182.
[81] Levy PE, Cannell MGR, Friend AD (2004). Modelling the impact of future changes in 811 climate, CO2 concentration and land use on natural ecosystems and the terrestrial 812 carbon sink. Global Environmental Change, 14, 21-30.
[82] Lieth H (1975a). Modeling the primary productivity of the world. In: Lieth H, Whittaker RH eds. Primary Productivity of the Biosphere. Springer-Verlag, Berlin. 237-263.
[83] Lieth H (1975b). Primary productivity in ecosystems: comparative analysis of global patterns. In: van Dobben WH, Lowe-McConnell RH eds. Unifying Concepts in Ecology. Publishers and Wageningen Center for Agricultural Publishing and Documentation, The Hague, The Netherlands. 300-321.
[84] Lindroth A, Grelle A, Morén AS (1998). Long-term measurements of boreal forest carbon balance reveal large temperature sensitivity. Global Change Biology, 4, 443-450.
[85] Litton CM, Giardina CP (2008). Below-ground carbon flux and partitioning: global patterns and response to temperature. Functional Ecology, 22, 941-954.
[86] Litton CM, Raich JW, Ryan MG (2007). Carbon allocation in forest ecosystems. Global Change Biology, 13, 2089-2109.
[87] Lloyd J, Pati?o S, Paiva RQ, Nardoto GB, Quesada CA, Santos AJB, Baker TR, Brand WA, Hilke I, Gielmann H, Raessler M, Luiz?o FJ, Martinelli LA, Mercado LM (2010). Optimisation of photosynthetic carbon gain and within-canopy gradients of associated foliar traits for Amazon forest trees. Biogeosciences, 7, 1833-1859.
[88] Maier CA, Albaugh TJ, Leeallen H, 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. Global Change Biology, 10, 1335-1350.
[89] M?kel? A, Landsberg J, Ek AR, Burk TE, Ter-Mikaelian M, ?gren GI, Oliver CD, Puttonen P (2000). Process-based models for forest ecosystem management: current state of the art and challenges for practical implementation. Tree Physiology, 20, 289-298.
[90] M?kel? A, Valentine HT (2001). The ratio of NPP to GPP: evidence of change over the course of stand development. Tree Physiology, 21, 1015-1030.
[91] Malhi Y (2012). The productivity, metabolism and carbon cycle of tropical forest vegetation. Journal of Ecology, 100, 65-75.
[92] Malhi Y, Arag?o LEOC, Metcalfe DB, Paiva R, Quesada CA, Almeida S, Anderson L, Brando P, Chambers JQ, da Costa ACL, Hutyra LR, Oliveira P, Pati?o S, Pyle EH, Robertson AL, Teixeira LM (2009). Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Global Change Biology, 15, 1255-1274.
[93] Malhi Y, Baldocchi DD, Jarvis PG (1999). The carbon balance of tropical, temperate and boreal forests. Plant, Cell & Environment, 22, 715-740.
[94] Malhi Y, Doughty C, Galbraith D (2011). The allocation of ecosystem net primary productivity in tropical forests. Philosophical Transactions of the Royal Society B, 366, 3225-3245.
[95] Malhi Y, Farfán Amézquita F, Doughty CE, Silva-Espejo JE, Girardin CAJ, Metcalfe DB, Aragao LEOC, Huaraca- Quispe LP, Alzamora-Taype I, Eguiluz-Mora L, Marthews TR, Halladay K, Robertson AL, Fisher JB, Zaragoza- Castells J, Rojas-Villagra CM, Pelaez-Tapia Y, Salinas N, Meir P, Phillips OL, Malhi Y (2014). The productivity, metabolism and carbon cycle of two lowland tropical forest plots in SW Amazonia, Peru. Plant Ecology and Diversity, 7, 85-105.
[96] Malhi Y, Grace J (2000). Tropical forests and atmospheric carbon dioxide. Tree, 15, 332-337.
[97] Manzoni S, Taylor P, Richter A, Porporato A, ?gren GI (2012). Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist, 196, 79-91.
[98] Marthews TR, Malhi Y, Girardin CAJ, Espejo JES, Arag?o LOC, Metcalfe DB, Rapp JM, Mercado LM, Fisher RA, Galbraith DR, Fisher JB, Salinas-Revilla N, Friend AD, Restrepo-Coupe N, Williams RJ (2012). Simulating forest productivity along a neotropical elevational transect: temperature variation and carbon use efficiency. Global Change Biology, 18, 2882-2898.
[99] Maseyk K, Grunzweig JM, Rotenberg E, Yakir D (2008). Respiration acclimation contributes to high carbon-use efficiency in a seasonally dry pine forest. Global Change Biology, 14, 1553-1567.
[100] Medlyn BE, Dewar RC (1999). Comment on the article by R.H. Waring, J.J. Landsberg and M. Williams relating net primary productivity to gross primary productivity. Tree Physiology, 19, 137-138.
[101] Metcalfe DB, Meir P, Arag?o LE, Lobo-do-Vale R, Galbraith D, Fisher RA, Chaves MM, Maroco JP, da Costa AC, de Almeida SS, Braga AP, Gon?alves PH, de Athaydes J, da Costa M, Portela TT, de Oliveira AA, Malhi Y, Williams M (2010). Shifts in plant respiration and carbon use efficiency at a large-scale drought experiment in the eastern Amazon. New Phytologist, 187, 608-621.
[102] Monje O, Bugbee B (1998). Adaptation to high CO2 concentration in an optimal environment: radiation capture, canopy quantum yield and carbon use efficiency. Plant, Cell & Environment, 21, 315-324.
[103] Monteith JL (1981). Climatic variation and the growth of crops. Quarterly Journal of the Royal Meteorological Society, 107, 749-774.
[104] Mooney HA (1991). Biological response to climate change: an agenda for research. Ecological Applications, 1, 112-117.
[105] Moser LE, Volenec JJ, Nelson CJ (1982). Respiration, carbohydrate content, and leaf growth of tall fescue. Crop Science, 22, 781-786.
[106] Nemali KS, van Iersel MW (2004). Light effects on wax begonia: photosynthesis, growth respiration, maintenance respiration, and carbon use ef?ciency. Journal of the American Society for Horticultural Science, 129, 416-424.
[107] Niinemets ü, Anten N (2009). Packing the photosynthetic machinery: from leaf to canopy. Advances in Photosynthesis and Respiration, 29, 363-399.
[108] Norby RJ, Hanson PJ, O’Neill EG, Tschaplinski TJ, Weltzin JF, Hansen RA, Cheng WX, Wullschleger SD, Gunderson CA, Edwards NT, Johnson DW (2002). Net primary productivity of a CO2-enriched deciduous forest and the implications for carbon storage. Ecological Applications, 12, 1261-1266.
[109] Ogawa K (2009). Mathematical analysis of change in forest carbon use efficiency with stand development: a case study on Abies veitchii Lindl. Ecological Modelling, 220, 1419-1424.
[110] Ogawa K (2011). Theoretical analysis of change in forest carbon use efficiency with stand development: a case study on hinoki cypress (Chamaecyparis obtusa(Sieb. et Zucc.) Endl.) plantation from the seedling stage. Ecological Modelling, 222, 437-441.
[111] Ogawa K, Takano Y (1997). Seasonal courses of CO2 exchange and carbon balance in fruits of Cinnamomum camphora. Tree Physiology, 17, 415-420.
[112] Penning de Vries FWT, Witlage JM, Kremer D (1979). Rates of respiration and of increase in structural dry matter in young wheat, ryegrass and maize plants in relation to temperature, to water stress and to their sugar content. Annals of Botany, 44, 595-609.
[113] Piao SL, Friedlingstein P, Ciais P, Viovy N, Demarty J (2007). Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Global Biogeochemical Cycles, 21, GB3018. doi: 10.1029/2006GB002888.
[114] Piao SL, Luyssaert S, Ciais P, Janssens IA, Chen AP, Cao C, Fang JY, Friedlingstein P, Luo YQ, Wang SP (2010). Forest annual carbon cost: a global-scale analysis of autotrophic respiration. Ecology, 91, 652-661.
[115] Potter CS, Randerson JT, Field CB, Matson PA, Vitousek PM, Mooney HA, Klooster SA (1993). Terrestrial ecosystem production: a process model based on global satellite and surface data. Global Biogeochemical Cycles, 7, 811-841.
[116] Raich JW, Russell AE, Kitayama K, Parton WJ, Vitousek PM (2006). Temperature influences carbon accumulation in moist tropical forests. Ecology, 87, 76-87.
[117] Rayment MB, Jarvis PG (1997). Seasonal variation in carbon accumulation by a high latitude forest ecosystem. Phyton-Annales Rei Botanicae, 39, 165-173.
[118] Reich PB, Tjoelker MG, Machado JL, Oleksyn J (2006). Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature, 439, 457-461.
[119] Reich PB, Walters MB, Ellsworth DS, Vose JM, Violin JC, Gresham C, Bowman WD (1998a). Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf lifespan: a test across biomes and functional groups. Oecologia, 114, 471-482.
[120] Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C (1998b). Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Functional Ecology, 12, 395-405.
[121] Reichstein M, Falge E, Baldocchi D, Papale D, Aubinet M, Berbigier P, Bernhofer C, Buchmann N, Gilmanov T, Granier A, Grunwald T, Havrankova K, Ilvesniemi H, Janous D, Knohl A, Laurila T, Lohila A, Loustau D, Matteucci G, Meyers T, Miglietta F, Ourcival JM, Pumpanen J, Rambal S, Rotenberg E, Sanz M, Tenhunen J, Seufert G, Vaccari F, Vesala T, Yakir D, Valentini R (2005). On the separation of net ecosystem exchange into assimilation and ecosystem respiration: review and improved algorithm. Global Change Biology, 11, 1424-1439.
[122] Running SW, Coughlan JC (1988). A general-model of forest ecosystem processes for regional applications: 1. Hydrologic balance, canopy gas-exchange and primary production processes. Ecological Modelling, 42, 125-154.
[123] Ryan MR (1991). Effects of climate change on plant respiration. Ecological Applications, 1, 157-167.
[124] Ryan MG (1990). Growth and maintenance respiration in stems of Pinus contorta and Picea engelmannii. Canadian Journal of Forest Research, 20, 48-57.
[125] Ryan MG (1995). Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content. Plant, Cell & Environment, 18, 765-772.
[126] 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 Physiology, 16, 333-343.
[127] Ryan MG, Lavigne MB, Gower ST (1997). Annual carbon cost of autotrophic respiration in boreal forest ecosystems in relation to species and climate. Journal of Geophysical Research-Atmospheres, 102, 28871-28883.
[128] Ryan MG, Linder S, Vose JM, Hubbard RM (1994). Dark respiration of pines. Ecological Bulletins, 43, 50-63.
[129] Sch?fer KVR, Oren R, Ellsworth DS, Lai CT, Herrick JD, Finzi AC, Richter DD, Katul GG (2003). Exposure to an enriched CO2 atmosphere alters carbon assimilation and allocation in a pine forest ecosystem. Global Change Biology, 9, 1378-1400.
[130] Sharp RE, Matthews MA, Boyer JS (1984). Kok effect and the quantum yield of photosynthesis: light partially inhibits dark respiration. Plant Physiology, 75, 95-101.
[131] Smith NG (2012). The carbon use efficiency of five deciduous tree seedlings in response to warming and altered precipitation in a northeastern old-field ecosystem. 97th ESA (Ecological Society of America) Annual Meeting, Portland, USA, August 5-10.
[132] Sprugel DG, Benecke U (1991). Measuring woody tissue respiration and photosynthesis. In: Lassoie JP, Hinckley TM eds. Techniques and Approaches in Forest Tree Ecophysiology. CRC Press, Boca Raton, USA. 329-355.
[133] Sprugel DG, Ryan MG, Brooks JR, Vogt KA, Martin TA (1995). Respiration from the organ level to the stand. In: Smith WK, Hinckley TM eds. Resource Physiology of Conifers: Acquisition, Allocation and Utilization. Academic Press, San Diego, USA. 255-299.
[134] Stockfors J, Linder S (1998). Effect of nitrogen on the seasonal course of growth and maintenance respiration in stems of Norway spruce trees. Tree Physiology, 18, 155-166.
[135] Street LE, Subke JA, Sommerkorn M, Sloan V, Ducrotoy H, Phoenix GK, Williams M (2013). The role of mosses in carbon uptake and partitioning in arctic vegetation. New Phytologist, 199, 163-175.
[136] Tan Z, Zhang Y, Yu G, Sha L, Tang J, Deng X, Song Q (2010). Carbon balance of a primary tropical seasonal rain forest. Journal of Geophysical Research: Atmospheres, 115, D00H26. doi: 10.1029/2009JD012913.
[137] Teskey RO, Sherff DW, Hollinger DY, Thomas RB (1995). External and internal factors regulating photosynthesis. In: Smith WK, Hinckley TM eds. Resource Physiology of Conifers. Academic Press, New York. 105-140.
[138] Thornley JHM, Johnson IR (1990). Plant and Crop Modelling: A Mathematical Approach to Plant and Crop Physiology. Clarendon Press, Oxford.
[139] Tjoelker MG, Oleksyn J, Lorenc-Plucinska G, Reich PB (2009). Acclimation of respiratory temperature responses in northern and southern populations of Pinus banksiana. New Phytologist, 181, 218-229.
[140] Tjoelker MG, Oleksyn J, Reich PB, Zytkowiak R (2008). Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations. Global Change Biology, 14, 782-797.
[141] Valentine HT, M?kel? A (2012). Modeling forest stand dynamics from optimal balances of carbon and nitrogen. New Phytologist, 194, 961-971.
[142] van Iersel MW (2003). Carbon use efficiency depends on growth respiration, maintenance respiration, and relative growth rate. A case study with lettuce. Plant, Cell & Environment, 26, 1441-1449.
[143] van Oijen M, Shapendonk A, H?glind M (2010). On the relative magnitudes of photosynthesis, respiration, growth and carbon storage in vegetation, Annals of Botany, 105, 793-797.
[144] Vicca S, Luyssaert S, Pe?uelas J, Campioli M, Chapin FS, Ciais P, Heinemeyer A, H?gberg P, Kutsch WL, Law BE, Malhi Y, Papale D, Piao SL, Reichstein M, Schulze ED, Janssens IA (2012). Fertile forests produce biomass more efficiently. Ecology Letters, 15, 520-526.
[145] Vose JM, Ryan MG (2002). Seasonal respiration of foliage, fine roots, and woody tissues in relation to growth, tissue N, and photosynthesis. Global Change Biology, 8, 182-193.
[146] Wang KY, Kellomaki S, Zha TS, Peltola H (2004). Seasonal variation in energy and water fluxes in a pine forest: an analysis based on eddy covariance and an integrated model. Ecological Modelling, 179, 259-279.
[147] Waring RH, Landsberg JJ, Williams M (1998). Net primary production of forests: a constant fraction of gross primary production? Tree Physiology, 18, 129-134.
[148] Waring RH, Schlesinger WH (1985). Forest Ecosystems: Concepts and Management. Academic Press, New York.
[149] White MA, Running SW, Thornton PE (1999). The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. International Journal of Biometeorology, 42, 139-145.
[150] Woodwell GM (1990). The effects of global warming. In: Leggett J ed. Global Warming: The Greenpeace Report. Cambridge University Press, Cambridge, UK. 116-132.
[151] Würth M, Peláez-Riedl S, Wright S, K?rner C (2005). Non-structural carbohydrate pools in a tropical forest. Oecologia, 143, 11-24.
[152] Xiao CW, Yuste JC, Janssens IA, Roskams P, Nachtergale L, Carrara A, Sanchez BY, Ceulemans R (2003). Above- and below-ground biomass and net primary production in a 73-year old Scots pine forest. Tree Physiology, 23, 505-516.
[153] Xiong FS, Mueller EC, Day TA (2000). Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperature regimes. American Journal of Botany, 87, 700-710.
[154] Zach A, Horna V, Leuschner C, Zimmermann R (2010). Patterns of wood carbon dioxide efflux across a 2,000 m elevation transect in an Andean moist forest. Oecologia, 162, 127-137.
[155] Zanotelli D, Montagnani L, Manca G, Tagliavini M (2012). Net primary productivity, allocation pattern and carbon use eciency in an apple orchard assessed by integrating eddy-covariance, biometric and continuous soil chamber measurements. Biogeosciences Discussions, 9, 14091-14143.
[156] Zha TS, Barr AG, Bernier PY, Lavigne MB, Trofymow JA, Amiro BD, Arain MA, Bhatti JS, Black TA, Margolis HA, McCaughey JH, Xing ZS, van Rees KCJ, Coursolle C (2013). Gross and aboveground net primary production at Canadian forest carbon flux sites. Agricultural and Forest Entomology, 174-175, 54-64.
[157] Zhang YJ, Xu M, Chen H, Adams J (2009). Global pattern of NPP to GPP ratio derived from MODIS data: effects of ecosystem type, geographical location and climate. Global Ecology and Biogeography, 18, 280-290.
[158] Zhang YJ, Yu GR, Yang J, Wimberly MC, Zhang XZ, Tao J, Jiang YB, Zhu JT (2013). Climate-driven global changes in carbon use efficiency. Global Ecology and Biogeography, doi: 10.1111/geb.12086.
[159] Ziska LH, Bunce JA (1998). The influence of increasing growth temperature and CO2 concentration on the ratio of respiration to photosynthesis in soybean seedlings. Global Change Biology, 4, 637-643.
Outlines

/

[an error occurred while processing this directive]