Papers on CO2 fertilization effect

This is a list of papers on the CO2 fertilization effect to the plant growth. The list is not complete, and will most likely be updated in the future in order to make it more thorough and more representative.

Tree ring evidence for limited direct CO₂ fertilization of forests over the 20th century – Gedalof & Berg (2010) “The effect that rising atmospheric CO₂ levels will have on forest productivity and water use efficiency remains uncertain, yet it has critical implications for future rates of carbon sequestration and forest distributions. Efforts to understand the effect that rising CO₂ will have on forests are largely based on growth chamber studies of seedlings, and the relatively small number of FACE sites. Inferences from these studies are limited by their generally short durations, artificial growing conditions, unnatural step-increases in CO₂ concentrations, and poor replication. Here we analyze the global record of annual radial tree growth, derived from the International Tree ring Data Bank (ITRDB), for evidence of increasing growth rates that cannot be explained by climatic change alone, and for evidence of decreasing sensitivity to drought. We find that approximately 20 percent of sites globally exhibit increasing trends in growth that cannot be attributed to climatic causes, nitrogen deposition, elevation, or latitude, which we attribute to a direct CO₂ fertilization effect. No differences were found between species in their likelihood to exhibit growth increases attributable to CO₂ fertilization, although Douglas-fir (Pseudotsuga menziesii) and ponderosa pine (Pinus ponderosa), the two most commonly sampled species in the ITRDB, exhibit a CO₂ fertilization signal at frequencies very near their upper and lower confidence limits respectively. Overall these results suggest that CO₂ fertilization of forests will not counteract emissions or slow warming in any substantial fashion, but do suggest that future forest dynamics may differ from those seen today depending on site conditions and individual species’ responses to elevated CO₂.” Gedalof, Z., and A. A. Berg (2010), Global Biogeochem. Cycles, 24, GB3027, doi:10.1029/2009GB003699.

CO2 Enhancement of Forest Productivity Constrained by Limited Nitrogen Availability – Norby et al. (2009) “Here, we provide new evidence from a FACE experiment in a deciduous Liquidambar styraciflua (sweetgum) forest stand in Tennessee, USA, that N limitation has significantly reduced the stimulation of NPP by elevated atmospheric CO₂ concentration (eCO₂). Isotopic evidence and N budget analysis support the premise that N availability in this forest ecosystem has been declining over time, and declining faster in eCO₂. Model analyses and evidence from leaf- and stand-level observations provide mechanistic evidence that declining N availability constrained the tree response to eCO₂. These results provide a strong rationale and process understanding for incorporating N limitation and N feedback effects in ecosystem and global models used in climate change assessments.” Norby, Richard, Warren, Jeffrey, Iversen, Colleen, Garten, Charles, Medlyn, Belinda, and McMurtrie, Nature Precedings, hdl:10101/npre.2009.3747.1, 2009. [Full text]

Why is plant-growth response to elevated CO₂ amplified when water is limiting, but reduced when nitrogen is limiting? A growth-optimisation hypothesis – McMurtrie et al. (2008) “Experimental evidence indicates that the stomatal conductance and nitrogen concentration ([N]) of foliage decline under CO₂ enrichment, and that the percentage growth response to elevated CO₂ is amplified under water limitation, but reduced under nitrogen limitation. We advance simple explanations for these responses based on an optimisation hypothesis applied to a simple model of the annual carbon–nitrogen–water economy of trees growing at a CO₂-enrichment experiment at Oak Ridge, Tennessee, USA. The model is shown to have an optimum for leaf [N], stomatal conductance and leaf area index (LAI), where annual plant productivity is maximised. The optimisation is represented in terms of a trade-off between LAI and stomatal conductance, constrained by water supply, and between LAI and leaf [N], constrained by N supply. At elevated CO₂ the optimum shifts to reduced stomatal conductance and leaf [N] and enhanced LAI. The model is applied to years with contrasting rainfall and N uptake. The predicted growth response to elevated CO₂ is greatest in a dry, high-N year and is reduced in a wet, low-N year. The underlying physiological explanation for this contrast in the effects of water versus nitrogen limitation is that leaf photosynthesis is more sensitive to CO₂ concentration ([CO₂]) at lower stomatal conductance and is less sensitive to [CO₂] at lower leaf [N].” Ross E. McMurtrie, Richard J. Norby, Belinda E. Medlyn, Roderick C. Dewar, David A. Pepper, Peter B. Reich, Craig V. M. Barton, Functional Plant Biology, 2008, 35(6) 521–534, doi:10.1071/FP08128. [Full text]

The Power of Monitoring Stations and a CO₂ Fertilization Effect: Evidence from Causal Relationships between NDVI and Carbon Dioxide – Kaufmann et al. (2008) “Two hypotheses are tested: 1) monitoring stations (e.g., Mauna Loa) are not able to measure changes in atmospheric concentrations of CO₂ that are generated by changes in terrestrial vegetation at distant locations; 2) changes in the atmospheric concentration of carbon dioxide do not affect terrestrial vegetation at large scales under conditions that now exist in situ, by estimating statistical models of the relationship between satellite measurements of the normalized difference vegetation index (NDVI) and the atmospheric concentration of carbon dioxide measured at Mauna Loa and Point Barrow. To go beyond simple correlations, the notion of Granger causality is used. Results indicate that the authors are able to identify locations where and months when disturbances to the terrestrial biota “Granger cause” atmospheric CO₂. The authors are also able to identify locations where and months when disturbances to the atmospheric concentration of carbon dioxide generate changes in NDVI. Together, these results provide large-scale support for a CO₂ fertilization effect and an independent empirical basis on which observations at monitoring stations can be used to test hypotheses and validate models regarding effect of the terrestrial biota on atmospheric concentrations of carbon dioxide.” Kaufmann, R. K., L. F. Paletta, H. Q. Tian, R. B. Myneni, R. D. D’Arrigo, 2008, Earth Interact., 12, 1–23, doi: 10.1175/2007EI240.1. [Full text]

Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO₂ – Finzi et al. (2007) “Forest ecosystems are important sinks for rising concentrations of atmospheric CO₂. In previous research, we showed that net primary production (NPP) increased by 23 ± 2% when four experimental forests were grown under atmospheric concentrations of CO₂ predicted for the latter half of this century. Because nitrogen (N) availability commonly limits forest productivity, some combination of increased N uptake from the soil and more efficient use of the N already assimilated by trees is necessary to sustain the high rates of forest NPP under free-air CO₂ enrichment (FACE). In this study, experimental evidence demonstrates that the uptake of N increased under elevated CO₂ at the Rhinelander, Duke, and Oak Ridge National Laboratory FACE sites, yet fertilization studies at the Duke and Oak Ridge National Laboratory FACE sites showed that tree growth and forest NPP were strongly limited by N availability. By contrast, nitrogen-use efficiency increased under elevated CO₂ at the POP-EUROFACE site, where fertilization studies showed that N was not limiting to tree growth. Some combination of increasing fine root production, increased rates of soil organic matter decomposition, and increased allocation of carbon (C) to mycorrhizal fungi is likely to account for greater N uptake under elevated CO₂. Regardless of the specific mechanism, this analysis shows that the larger quantities of C entering the below-ground system under elevated CO₂ result in greater N uptake, even in N-limited ecosystems. Biogeochemical models must be reformulated to allow C transfers below ground that result in additional N uptake under elevated CO₂.” Adrien C. Finzi, Richard J. Norby, Carlo Calfapietra, Anne Gallet-Budynek, Birgit Gielen, William E. Holmes, Marcel R. Hoosbeek, Colleen M. Iversen, Robert B. Jackson, Mark E. Kubiske, Joanne Ledford, Marion Liberloo, Ram Oren, Andrea Polle, Seth Pritchard, Donald R. Zak, William H. Schlesinger, and Reinhart Ceulemans, PNAS August 28, 2007 vol. 104 no. 35 14014-14019, doi: 10.1073/pnas.0706518104. [Full text]

Nitrogen limitation constrains sustainability of ecosystem response to CO₂ – Reich et al. (2006) “Enhanced plant biomass accumulation in response to elevated atmospheric CO₂ concentration could dampen the future rate of increase in CO₂ levels and associated climate warming. However, it is unknown whether CO₂-induced stimulation of plant growth and biomass accumulation will be sustained or whether limited nitrogen (N) availability constrains greater plant growth in a CO₂-enriched world. Here we show, after a six-year field study of perennial grassland species grown under ambient and elevated levels of CO₂ and N, that low availability of N progressively suppresses the positive response of plant biomass to elevated CO₂. Initially, the stimulation of total plant biomass by elevated CO₂ was no greater at enriched than at ambient N supply. After four to six years, however, elevated CO₂ stimulated plant biomass much less under ambient than enriched N supply. This response was consistent with the temporally divergent effects of elevated CO₂ on soil and plant N dynamics at differing levels of N supply. Our results indicate that variability in availability of soil N and deposition of atmospheric N are both likely to influence the response of plant biomass accumulation to elevated atmospheric CO₂. Given that limitations to productivity resulting from the insufficient availability of N are widespread in both unmanaged and managed vegetation, soil N supply is probably an important constraint on global terrestrial responses to elevated CO₂.” Peter B. Reich, Sarah E. Hobbie, Tali Lee, David S. Ellsworth, Jason B. West, David Tilman, Johannes M. H. Knops, Shahid Naeem and Jared Trost, Nature 440, 922-925 (13 April 2006) | doi:10.1038/nature04486.

Food for Thought: Lower-Than-Expected Crop Yield Stimulation with Rising CO₂ Concentrations – Long et al. (2006) “Model projections suggest that although increased temperature and decreased soil moisture will act to reduce global crop yields by 2050, the direct fertilization effect of rising carbon dioxide concentration ([CO₂]) will offset these losses. The CO₂ fertilization factors used in models to project future yields were derived from enclosure studies conducted approximately 20 years ago. Free-air concentration enrichment (FACE) technology has now facilitated large-scale trials of the major grain crops at elevated [CO₂] under fully open-air field conditions. In those trials, elevated [CO₂] enhanced yield by ∼50% less than in enclosure studies. This casts serious doubt on projections that rising [CO₂] will fully offset losses due to climate change.” Stephen P. Long, Elizabeth A. Ainsworth, Andrew D. B. Leakey, Josef Nösberger and Donald R. Ort, Science 30 June 2006, Vol. 312 no. 5782 pp. 1918-1921, DOI: 10.1126/science.1114722.

Effect of natural atmospheric CO₂ fertilization suggested by open-grown white spruce in a dry environment – Wang et al. (2006) “Evidence of an atmospheric CO₂-fertilization effect on radial growth rates was uncovered for open-grown white spruce in a mixed-grass prairie of southwestern Manitoba, Canada. Consistent upward trends of the residuals from dendroclimatic models indicated a decreased ability for climatic parameters to predict radial growth. Despite that a similar amount (61%) of the total variation in radial growth index was explained by climate for both young and old trees, residuals from young trees for the period of 1955–1999 demonstrated a stronger upward trend (R2=0.551, P<0.0001) than old trees for the period of 1900–1996 (R2=0.020, P=0.167). Similar to young trees, the residuals from the early growth period (1900–1929) of old trees also demonstrated a stronger upward trend (R2=0.480, P<0.0001) than the period of 1900–1996. Likewise, a comparable period (1970–1999) of young trees also demonstrated a stronger upward trend (R2=0.619, P<0.0001) than the early growth period (1900–1929) of old trees. In addition, postdrought growth response was much stronger for young trees (1970–1999) compared with old trees at the same development stage (1900–1929) (P=0.011) or within the same time period (1970–1999) (P=0.014). There was no difference (P=0.221) in drought recovery between the early (1900–1929) period and the late (1970–1999) period within old trees. Together, our results suggest that (1) open-grown white spruce trees improved their growth with time at the early developmental stage, and (2) at the same developmental stage, a greater growth response occurred in the late period when atmospheric CO₂ concentration, and the rate of atmospheric CO₂ increase were both relatively high. While it is impossible to rule out other factors, these results are consistent with expectations for CO₂-fertilization effects.” G. Geoff Wang, Sophan Chhin, William L. Bauerle, Global Change Biology, Volume 12, Issue 3, pages 601–610, March 2006, DOI: 10.1111/j.1365-2486.2006.01098.x.

Forest response to elevated CO₂ is conserved across a broad range of productivity – Norby et al. (2005) “Climate change predictions derived from coupled carbon-climate models are highly dependent on assumptions about feedbacks between the biosphere and atmosphere. One critical feedback occurs if C uptake by the biosphere increases in response to the fossil-fuel driven increase in atmospheric [CO₂] (“CO₂ fertilization”), thereby slowing the rate of increase in atmospheric [CO₂]. Carbon exchanges between the terrestrial biosphere and atmosphere are often first represented in models as net primary productivity (NPP). However, the contribution of CO₂ fertilization to the future global C cycle has been uncertain, especially in forest ecosystems that dominate global NPP, and models that include a feedback between terrestrial biosphere metabolism and atmospheric [CO₂] are poorly constrained by experimental evidence. We analyzed the response of NPP to elevated CO2 (≈550 ppm) in four free-air CO₂ enrichment experiments in forest stands. We show that the response of forest NPP to elevated [CO₂] is highly conserved across a broad range of productivity, with a stimulation at the median of 23 ± 2%. At low leaf area indices, a large portion of the response was attributable to increased light absorption, but as leaf area indices increased, the response to elevated [CO₂] was wholly caused by increased light-use efficiency. The surprising consistency of response across diverse sites provides a benchmark to evaluate predictions of ecosystem and global models and allows us now to focus on unresolved questions about carbon partitioning and retention, and spatial variation in NPP response caused by availability of other growth limiting resources.” Richard J. Norby, Evan H. DeLucia, Birgit Gielen, Carlo Calfapietra, Christian P. Giardina, John S. King, Joanne Ledford, Heather R. McCarthy, David J. P. Moore, Reinhart Ceulemans, Paolo De Angelis, Adrien C. Finzi, David F. Karnosky, Mark E. Kubiske, Martin Lukac, Kurt S. Pregitzer, Giuseppe E. Scarascia-Mugnozza, William H. Schlesinger, and Ram Oren, PNAS December 13, 2005 vol. 102 no. 50 18052-18056, doi: 10.1073/pnas.0509478102. [Full text]

Climate change impacts on crop yield and quality with CO₂ fertilization in China – Erda et al. (2005) “A regional climate change model (PRECIS) for China, developed by the UK’s Hadley Centre, was used to simulate China’s climate and to develop climate change scenarios for the country. Results from this project suggest that, depending on the level of future emissions, the average annual temperature increase in China by the end of the twenty-first century may be between 3 and 4 °C. Regional crop models were driven by PRECIS output to predict changes in yields of key Chinese food crops: rice, maize and wheat. Modelling suggests that climate change without carbon dioxide (CO₂) fertilization could reduce the rice, maize and wheat yields by up to 37% in the next 20–80 years. Interactions of CO₂ with limiting factors, especially water and nitrogen, are increasingly well understood and capable of strongly modulating observed growth responses in crops. More complete reporting of free-air carbon enrichment experiments than was possible in the Intergovernmental Panel on Climate Change’s Third Assessment Report confirms that CO₂ enrichment under field conditions consistently increases biomass and yields in the range of 5–15%, with CO₂ concentration elevated to 550 ppm Levels of CO₂ that are elevated to more than 450 ppm will probably cause some deleterious effects in grain quality. It seems likely that the extent of the CO₂ fertilization effect will depend upon other factors such as optimum breeding, irrigation and nutrient applications.” Lin Erda, Xiong Wei, Ju Hui, Xu Yinlong, Li Yue, Bai Liping and Xie Liyong, Phil. Trans. R. Soc. B 29 November 2005 vol. 360 no. 1463 2149-2154, doi: 10.1098/rstb.2005.1743. [Full text]

Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment – Norby et al. (2004) “Fine-root production and turnover are important regulators of the biogeochemical cycles of ecosystems and key components of their response to global change. We present a nearly continuous 6-year record of fine-root production and mortality from minirhizotron analysis of a closed-canopy, deciduous sweetgum forest in a free-air CO2 enrichment experiment. Annual production of fine roots was more than doubled in plots with 550 ppm CO2 compared with plots in ambient air. This response was the primary component of the sustained 22% increase in net primary productivity. Annual fine-root mortality matched annual production, and the mean residence time of roots was not altered by elevated CO2, but peak fine-root standing crop in midsummer was significantly higher in CO2-enriched plots, especially deeper in the soil profile. The preferential allocation of additional carbon to fine roots, which have a fast turnover rate in this species, rather than to stemwood reduces the possibility of long-term enhancement by elevated CO2 of carbon sequestration in biomass. However, sequestration of some of the fine-root carbon in soil pools is not precluded, and there may be other benefits to the tree from a seasonally larger and deeper fine-root system. Root-system dynamics can explain differences among ecosystems in their response to elevated atmospheric CO2; hence, accurate assessments of carbon flux and storage in forests in a globally changing atmosphere must account for this unseen and difficult-to-measure component.” Richard J. Norby, Joanne Ledford, Carolyn D. Reilly, Nicole E. Miller, and Elizabeth G. O’Neill, PNAS June 29, 2004 vol. 101 no. 26 9689-9693, doi: 10.1073/pnas.0403491101. [Full text]

Net primary productivity of a CO₂-enriched deciduous forest and the implications for carbon storage – Norby et al. (2002) “A central question concerning the response of terrestrial ecosystems to a changing atmosphere is whether increased uptake of carbon in response to increasing atmospheric carbon dioxide concentration results in greater plant biomass and carbon storage or, alternatively, faster cycling of C through the ecosystem. Net primary productivity (NPP) of a closed-canopy Liquidambar styraciflua (sweetgum) forest stand was assessed for three years in a free-air CO₂-enrichment (FACE) experiment. NPP increased 21% in stands exposed to elevated CO₂, and there was no loss of response over time. Wood increment increased significantly during the first year of exposure, but subsequently most of the extra C was allocated to production of leaves and fine roots. These pools turn over more rapidly than wood, thereby reducing the potential of the forest stand to sequester additional C in response to atmospheric CO₂ enrichment. Hence, while this experiment provides the first evidence that CO₂ enrichment can increase productivity in a closed-canopy deciduous forest, the implications of this result must be tempered because the increase in productivity resulted in faster cycling of C through the system rather than increased C storage in wood. The fate of the additional C entering the soil system and the environmental interactions that influence allocation need further investigation.” Richard J. Norby, Paul J. Hanson, Elizabeth G. O’Neill, Tim J. Tschaplinski, Jake F. Weltzin, Randi A. Hansen, Weixin Cheng, Stan D. Wullschleger, Carla A. Gunderson, Nelson T. Edwards, and Dale W. Johnson, 2002, Ecological Applications 12:1261–1266, doi:10.1890/1051-0761(2002)012[1261:NPPOAC]2.0.CO;2. [Full text]

Soil fertility limits carbon sequestration by forest ecosystems in a CO₂-enriched atmosphere – Oren et al. (2001) “Northern mid-latitude forests are a large terrestrial carbon sink. Ignoring nutrient limitations, large increases in carbon sequestration from carbon dioxide (CO₂) fertilization are expected in these forests. Yet, forests are usually relegated to sites of moderate to poor fertility, where tree growth is often limited by nutrient supply, in particular nitrogen. Here we present evidence that estimates of increases in carbon sequestration of forests, which is expected to partially compensate for increasing CO₂ in the atmosphere, are unduly optimistic. In two forest experiments on maturing pines exposed to elevated atmospheric CO₂, the CO₂-induced biomass carbon increment without added nutrients was undetectable at a nutritionally poor site, and the stimulation at a nutritionally moderate site was transient, stabilizing at a marginal gain after three years. However, a large synergistic gain from higher CO₂ and nutrients was detected with nutrients added. This gain was even larger at the poor site (threefold higher than the expected additive effect) than at the moderate site (twofold higher). Thus, fertility can restrain the response of wood carbon sequestration to increased atmospheric CO₂. Assessment of future carbon sequestration should consider the limitations imposed by soil fertility, as well as interactions with nitrogen deposition.” Ram Oren, David S. Ellsworth, Kurt H. Johnsen, Nathan Phillips, Brent E. Ewers, Chris Maier, Karina V.R. Schäfer, Heather McCarthy, George Hendrey, Steven G. McNulty & Gabriel G. Katul, Nature 411, 469-472 (24 May 2001) | doi:10.1038/35078064. [Full text]

Transient nature of CO₂ fertilization in Arctic tundra – Oechel et al. (1994) “THERE has been much debate about the effect of increased atmospheric CO₂ concentrations on plant net primary production and on net ecosystem CO₂ flux. Apparently conflicting experimental findings could be the result of differences in genetic potential and resource availability, different experimental conditions and the fact that many studies have focused on individual components of the system rather than the whole ecosystem. Here we present results of an in situ experiment on the response of an intact native ecosystem to elevated CO2. An undisturbed patch of tussock tundra at Toolik Lake, Alaska, was enclosed in greenhouses in which the CO₂ level, moisture and temperature could be controlled, and was subjected to ambient (340 p.p.m.) and elevated (680 p.p.m.) levels of CO₂ and temperature (+4 °C). Air humidity, precipitation and soil water table were maintained at ambient control levels. For a doubled CO₂ level alone, complete homeostasis of the CO₂ flux was re-established within three years, whereas the regions exposed to a combination of higher temperatures and doubled CO₂ showed persistent fertilization effect on net ecosystem carbon sequestration over this time. This difference may be due to enhanced sink activity from the direct effects of higher temperatures on growth and to indirect effects from enhanced nutrient supply caused by increased mineralization. These results indicate that the responses of native ecosystems to elevated CO₂ may not always be positive, and are unlikely to be straightforward. Clearly, CO₂ fertilization effects must always be considered in the context of genetic limitation, resource availability and other such factors.” Walter C. Oechel, Sid Cowles, Nancy Grulke, Steven J. Hastings, Bill Lawrence, Tom Prudhomme, George Riechers, Boyd Strain, David Tissue & George Vourlitis, Nature 371, 500 – 503 (06 October 1994); doi:10.1038/371500a0.

Tree growth in carbon dioxide enriched air and its implications for global carbon cycling and maximum levels of atmospheric CO₂ – Idso & Kimball (1993) “In the longest carbon dioxide enrichment experiment ever conducted, well-watered and adequately fertilized sour orange tree seedlings were planted directly into the ground at Phoenix, Arizona, in July 1987 and continuously exposed, from mid-November of that year, to either ambient air or air enriched with an extra 300 ppmv of CO₂ in clear-plastic-wall open-top enclosures. Only 18 months later, the CO₂-enriched trees had grown 2.8 times larger than the ambient-treated trees; and they have maintained that productivity differential to the present day. This tremendous growth advantage is due to two major factors: a CO₂-induced increase in daytime net photosynthesis and a CO₂-induced reduction in nighttime dark respiration. Measurements of these physiological processes in another experiment have shown three Australlian tree species to respond similarly; while an independent study of the atmosphere’s seasonal CO₂ cycle suggests that all earth’s trees, in the mean, probably share this same response. A brief review of the plant science literature outlines how such a large growth response to atmospheric CO₂ enrichment might possibly be maintained in light of resource limitations existing in nature. Finally, it is noted that a CO₂ “fertilization effect” of this magnitude should substantially slow the rate at which anthropogenic carbon dioxide would otherwise accumulate in the atmosphere, possibly putting an acceptable upper limit on the level to which the CO₂ content of the air may ultimately rise.” Idso, S. B., and B. A. Kimball (1993), Global Biogeochem. Cycles, 7(3), 537–555, doi:10.1029/93GB01164.