The Progressive Nitrogen Limitation Hypothesis (Part 2)
Land plants grow best when supplied with optimum levels of soil nitrogen. When this reactive nitrogen (Nr) is present in soils in concentrations that are less than optimal, terrestrial vegetation grows less vigorously and removes less CO2 from the atmosphere. As a result, there have been claims that less-than-optimal soil nitrogen concentrations will eventually cause a significant reduction in the strength of the growth stimulation provided by the aerial fertilization effect of the ongoing rise in the air’s CO2 content because the limited amount of Nr in the soil simply cannot supply enough of this essential nutrient to maintain the increase in growth stimulated by the rising CO2. This string of suppositions has come to be called the progressive nitrogen limitation hypothesis (Hungate et al., 2003; Luo et al., 2004).
Expressing the opposite concern about Nr are scientists such as Fujimaki et al. (2009), who contend “anthropogenic addition of reactive nitrogen to the biosphere”—“through production of fertilizers, cultivation of N-fixing plants, and utilization of fossil fuels”—“is increasing globally and some terrestrial ecosystems are suffering from a state of excess Nr.” They contend “excess Nr has a harmful impact on vegetation cover and species diversity,” as a result of “increasing competitive abilities for a small number of nitrophilic species, increase of herbivory, decreases in mutualistic fungi, increases in pathogenic fungi, and enhanced invasibility by exotic species that are highly competitive under conditions of high soil nitrate.” Both sides of this debate feel strongly about their positions, and both foresee undesirable consequences in the fairly near future if certain aspects of the way modern societies operate are not radically changed.
What neither side seems to consider, however, is that the two extreme phenomena might work together to produce a harmonious outcome. Instead of suppressing economic activity (to reduce CO2 emissions) and agricultural production (to reduce addition of nitrogen to the soil), we could simply let each phenomenon proceed unimpaired by overt human intervention. Thus the addition of nitrogen to the soil should provide what is needed (more reactive nitrogen) to enable the world’s terrestrial vegetation to capture and sequester more of the carbon supplied to the air by anthropogenic CO2 emissions. This will be needed to increase the productivity of the world’s cropped and naturally vegetated land in order to feed the still-growing human population.
Evidence that such a laissez-faire approach to the two concerns is indeed reasonable is provided by the fact that even Fujimaki et al. admit “ecosystem net primary production seems to be under N limitation,” and “in global trends to date, plant growth itself tends to be stimulated with increase of N deposition.” This observation leads them to conclude, “if N deposition continues at the present rates in the next few decades, ecosystem net primary production would be released from the limitation of N availability.” Better yet, there is evidence that vegetation growing in CO2-enriched air can find the nitrogen it needs even when it seems not to be there.
Consider the Duke Forest free-air CO2-enrichment (FACE) study: a long-term experiment designed to investigate the effects of an extra 200 ppm of atmospheric CO2 on the growth and development of a plantation of loblolly pine (Pinus taeda) trees with an understory of various broadleaf species (Liriodendron tulipifera, Liquidambar styraciflua, Acer rubrum, Ulmus alata, and Cornus florida), plus various other trees, shrubs, and vines, all growing on a soil that Finzi and Schlesinger (2003) have described as being in “a state of acute nutrient deficiency that can only be reversed with fertilization.” Many people had long thought this fertility deficiency would stifle the ability of the extra aerial supply of CO2 to significantly stimulate the forest’s productivity on a continuing basis. Based on data for the years 1996–2004, however, McCarthy et al. (2010) calculated the net primary productivity (NPP) for the pines, the hardwoods, and the entire stand as the sum of the production of coarse wood (stems, branches, and coarse roots), leaf litter (lagged for pines), fine roots, and reproductive structures. They found “elevated CO2 increased pine biomass production, starting in 1997 and continuing every year thereafter,” and “the CO2-induced enhancement remained fairly consistent as the stand developed.”
They also found “elevated CO2 increased stand (pine plus all other species) biomass production every year from 1997 onwards with no trend over time,” such that the average yearly increase in NPP caused by the approximate 54 percent increase in the air’s CO2 content was a solid 28 percent. Thus, and in spite of the original belief of many scientists that low levels of soil nitrogen—especially an acute deficiency—would preclude the persistence of any growth stimulation provided by atmospheric CO2 enrichment, the suite of trees, bushes, and shrubs that constitute the Duke Forest has continued to maintain the extra CO2-enabled vitality exhibited right from the start of the study, with no sign of it even beginning to taper off.
Also working at the Duke Forest FACE facility, Jackson et al. (2009) described belowground data they obtained there, after which they presented a synthesis of these and other results they obtained between 1996 and 2008, seeking to determine “which, if any, variables show evidence for a decrease in their response to atmospheric CO2 during that time frame.”
Among many other things, Jackson et al. report “on average, in elevated CO2, fine-root biomass in the top 15 cm of soil increased by 24%,” and in recent years the fine-root biomass increase “grew stronger, averaging ~30% at high CO2.” Regarding coarse roots having diameters greater than 2 mm and extending to a soil depth of 32 cm, they report “biomass sampled in 2008 was twice as great in elevated CO2.” We calculate from the graphical representation of their results that the coarse-root biomass was fully 130 percent greater, while the extra 200 ppm of CO2 supplied to the air surrounding the CO2-enriched trees represented an enhancement of only about 55 percent above ambient conditions. In the concluding sentence of their paper’s abstract, they state, “overall, the effect of elevated CO2 belowground shows no sign of diminishing.”
The four researchers thus conclude, “if progressive nitrogen limitation were occurring in this system, we would expect differences in productivity to diminish for trees in the elevated vs. ambient CO2 plots,” but “there is little evidence from estimates of aboveground or total net primary productivity in the replicated Duke experiment that progressive nitrogen limitation is occurring there or at other forest FACE experiments,” even “after more than a decade of manipulation” of the air’s CO2 content, citing, with respect to the latter portion of their statement, Finzi et al. (2007). Consequently, there is good reason to believe the “aerial fertilization effect” of atmospheric CO2 enrichment will continue to significantly benefit Earth’s forests as long as the atmosphere’s CO2 concentration continues to rise.
Working with photosynthesis data they and others collected over 11 years at the Aspen FACE site near Rhinelander, Wisconsin (USA), Darbah et al. (2010) evaluated the merits of the progressive nitrogen limitation hypothesis for two different quaking aspen (Populus tremuloides Michx.) clones (42E and 271) exposed to all combinations of ambient and elevated (560 ppm) CO2 and ambient and elevated (1.5 times ambient) ozone (O3). They also investigated whether the same hypothesis applied to leaf stomatal conductance.
The eight researchers say their results “suggest no long-term photosynthetic and stomatal acclimation to elevated CO2, O3 or CO2 + O3 in aspen trees exposed to elevated CO2 and/or O3 gases for 11 years,” adding the aspen trees “have sustained their maximum instantaneous photosynthesis stimulation for over a decade.” Commenting further, they say their findings support the observations of (1) Liberloo et al. (2007), who measured a 49 percent increase in net photosynthetic rate in poplar trees after six years of exposure to elevated CO2, (2) Sholtis et al. (2004), who reported a 44 percent stimulation of net photosynthesis in sweetgum trees after three years of exposure to elevated CO2, (3) Crous and Ellsworth (2004), who found a photosynthetic enhancement of 51–69 percent in Pinus taeda trees after six years of exposure to elevated CO2, as well as (4) Davey et al. (2006) and (5) Paoletti et al. (2007), of whose work Darbah et al. state “there was no photosynthetic acclimation (down-regulation) occurring in Quercus ilex under long-term CO2 enrichment.” In addition, Darbah et al. remark that (6) even in white clover (Trifolium repens), Ainsworth et al. (2003) found photosynthetic stimulation “remained after nine years of exposure to elevated CO2.”
Focusing her efforts belowground, Colleen Iversen of the Oak Ridge National Laboratory in Oak Ridge, Tennessee (USA) reviewed the pertinent scientific literature “to examine the potential mechanisms for, and consequences of, deeper rooting distributions under elevated CO2 as they relate to ecosystem carbon and nitrogen cycling,” focusing primarily on forests (Iversen, 2010). She found “experimental evidence from a diverse set of forested ecosystems indicates that fine roots of trees exposed to elevated CO2 are distributed more deeply in the soil profile relative to trees grown under ambient CO2.” As an example, she reports, “in a FACE experiment in a sweetgum (Liquidambar styraciflua) plantation, Iversen et al. (2008) found that, over nine years, there was a 220% stimulation in cumulative carbon inputs from fine roots under elevated CO2 at 45-60 cm soil depth, compared with a 30% stimulation of root carbon inputs at 0-15 cm depth,” and she notes “Pritchard et al. (2008a) found a similar response in a CO2-enriched loblolly pine (Pinus taeda) plantation.” In fact, she found, “of those experiments that examined rooting depth responses to elevated CO2, 73% found deeper rooting distributions.” In addition, she notes “increased proliferation at depth in the soil has not been limited to fine roots: increased production of mycorrhizas (Pritchard et al., 2008b) and coarse roots (Liberloo et al., 2006) also occurred deeper in the soil under CO2 enrichment.”
Regarding the progressive nitrogen limitation hypothesis, therefore, Iversen writes, “a disconnect between observed root dynamics and modeled nutrient availability has confounded projections of forest responses to elevated CO2.” She notes “while models predict that soil nitrogen availability will limit forest responses to elevated CO2 (Thornton et al., 2007), many of the forested FACE experiments found a sustained increase in nitrogen uptake from the soil in response to CO2 enrichment (Finzi et al., 2007).” She goes on to state “there has been much speculation on the source of this ‘extra’ nitrogen (Johnson, 2006), and a greater cumulative amount of nitrogen available at depth in the soil may be the answer (i.e. a ‘bigger box’ of nitrogen when deeper soil depths are considered).”
Shifting from forests to grasslands, Dijkstra et al. (2008) used open-top chambers to examine the effects of elevated atmospheric CO2 concentration (720 vs. 368 ppm) on nitrogen dynamics in a semi-arid grassland ecosystem in northeastern Colorado (USA), where they studied the impacts of elevated CO2 on nitrogen mineralization and plant N uptake by tracking initially applied 15N and total N in both plants and soil over a period of five years. This work revealed an increase in aboveground biomass on the order of 40 percent in response to their specific degree of elevated CO2; and they state it “did not lead to a progressive decline in soil N availability.” On the contrary, the six scientists write, “soil N availability remained higher after 5 years of elevated than ambient CO2,” likely due to “a greater mineralization rate under elevated CO2.” As for why this was so, they speculate the “elevated CO2 increased soil moisture due to decreased plant transpiration at [their] site (Nelson et al., 2004), which could have stimulated microbial activity and N mineralization.”
In another illuminating experiment, McCormack et al. (2010) constructed 12 identical mini-ecosystems—each consisting of three longleaf pine (Pinus palustris) seedlings, three wiregrass (Aristida stricta) C4 grass plants, two sand post oak (Quercus margaretta) seedlings, one rattlebox (Croatalaria rotundifolia) C3 perennial herbaceous legume, and one butterfly weed (Asclepias tuberose) herbaceous C3 dicotyledonous perennial—which they allowed to grow for three years in an outdoor soil bin at the National Soil Dynamics Laboratory in Auburn, Alabama (USA), within 12 open-top chambers (half of which were maintained for three years at 365 ppm CO2 and half of which were maintained at 720 ppm CO2 for the same period). During this time the “standing crops” of fine-root length, rhizomorph length, and number of mycorrhizal root tips were assessed in the upper (0–17 cm) and lower (17–34 cm) halves of the plants’ root zones at four-week intervals via microvideo cameras installed within each of two mini-rhizotron tubes located within each of the 12 plots into which the soil bin was divided.
They found the greatest impacts of the 97 percent increase in the air’s CO2 content were generally observed in the lower halves of the ecosystems’ root zones, where the standing crops of fine roots, rhizomorphs, and mycorrhizal root tips were increased, respectively, by 59 percent, 66 percent, and 64 percent, although the mean standing crop of rhizomorphs in the upper halves of the ecosystems’ root zones was increased by 114 percent.
Based on these findings, McCormack et al. state that as the atmosphere’s CO2 concentration continues to rise, “greater biomass production in deeper soils in the coming decades has the potential to contribute to greater carbon storage in forest soils,” because “carbon in deeper soil turns over (decomposes) more slowly than litter nearer the soil surface,” citing Trumbore (2000) and Schoning and Kogel-Knabner (2006). In addition, they note “fungal tissues consist largely of chitin, a potentially recalcitrant compound that may build up soil organic matter and persist for long periods of time relative to more labile carbon,” citing Langley and Hungate (2003). Thus they suggest “regenerating longleaf pine-wiregrass systems may act as a carbon sink as atmospheric CO2 rises in the coming decades through increased biomass production and potentially through directed allocation of carbon to deeper soils,” This, they note, is “consistent with the recent assertion that greater allocation of forest carbon to deeper soil is a general response to atmospheric CO2-enrichment,” citing Iversen (2010). And, very importantly, they state “significant increases in mycorrhizae and rhizomorphs,” as they found in their study, “may explain why the magnitude of the increase in forest net primary productivity caused by elevated CO2, in several long-term demonstrably nitrogen-limited FACE experiments, has not decreased after nearly a decade (Finzi et al., 2007).” This observation helps explain why the progressive nitrogen limitation hypothesis repeatedly has been shown to be wrong.
Also studying roots were Alberton et al. (2010), who write, “roots of a very large number of plant species are regularly colonized by a group of ascomycete fungi with usually dark-pigmented (melanized) septate hyphae (Mandyam and Jumpponen, 2005; Sieber and Grunig, 2006)” that are referred to as “dark septate root endophytic (DSE) fungi,” with “most species belonging to the Leotiomycetes (Kernaghan et al., 2003; Hambleton and Sigler, 2005; Wang et al., 2006).” To study these fungi further, the authors grew Scots pine (Pinus sylvestris) plants from seed for 125 days in Petri dishes—both with and without inoculation with one of seven different species/strains of DSE fungi—within controlled environment chambers maintained at atmospheric CO2 concentrations of either 350 or 700 ppm, destructively harvesting some of the seedlings at the 98-day point of the study and the rest at the end of the experiment.
At the conclusion of their study, the three researchers found, “across all plants (DSE-inoculated and control plants) under elevated CO2, shoot and root biomass increased significantly by 21% and 19%, respectively, relative to ambient,” with “higher values over the final four weeks (increases of 40% and 30% for shoots and roots, respectively).” In addition, they state “on average, shoot nitrogen concentration was 57% lower under elevated CO2,” and “elevated CO2 decreased root nitrogen concentration on average by 16%.” Nevertheless, they emphasize that “surprisingly, even under reduced nitrogen availability, elevated CO2 led to increases in both above-ground and below-ground plant biomass.”
In explaining how this happened, the Brazilian and Dutch researchers write, “a potential mechanism for the increase of plant biomass even when plant nutrient uptake decreases is the production of phytohormones by DSE fungi.” They report “earlier authors noted that DSE fungi enhance plant growth by producing phytohormones or inducing host hormone production without any apparent facilitation of host nutrient uptake or stimulation of host nutrient metabolism (Addy et al., 2005; Schulz and Boyle, 2005),” further demonstrating that low levels of nitrogen availability need not impede significant CO2-induced increases in plant growth and development.
In another pertinent study, Langley et al. (2009) once again state “it has been suggested that stimulation of productivity with elevated CO2 ties up nitrogen in plant litter, which, if not offset by increases in N-use efficiency or N supply, will limit the ecosystem CO2 response (Reich et al., 2006).” To test this hypothesis, they used “an acid-hydrolysis-incubation method and a net nitrogen-mineralization assay to assess stability of soil carbon pools and short-term nitrogen dynamics in a Florida scrub-oak ecosystem after six years of exposure to elevated CO2,” This work was conducted at a multiple open-top-chamber facility on a barrier island located at NASA’s Kennedy Space Center on the east coast of central Florida, USA.
The researchers found elevated atmospheric CO2 (to 350 ppm above ambient concentrations) tended to increase net N mineralization in the top 10 cm of the soil, but it also decreased total soil organic carbon content there by 21 percent. However, that loss of carbon mass was equivalent only to “roughly one-third of the increase in plant biomass that occurred in the same experiment.” In addition, they state the strongest increases in net N mineralization were observed in the 10–30 cm depth increment, and “release of N from this depth may have allowed the sustained CO2 effect on productivity in this scrub-oak forest,” which over the four years leading up to their study “increased litterfall by 19–59%,” citing Hungate et al. (2006) for the latter figures. This is yet another experimental demonstration that plants are generally able to find the extra nitrogen they need to take full advantage of the aerial fertilization effect of elevated atmospheric CO2 concentrations, which increases total ecosystem carbon content and thus results in a negative feedback to anthropogenic CO2 emissions.
We conclude our review of the progressive nitrogen limitation hypothesis with a brief analysis of the paper of Thornton et al. (2009), who provided powerful political fodder for the claim that there will be even greater global warming in the future than the amount that already has been predicted by climate models, due to the supposedly smaller amount of CO2 being removed from the air by the supposedly less-vigorously growing vegetation, due to the imagined gradual weakening of CO2’s aerial fertilization effect on plants growing in nitrogen-limited soils.
As for why we should believe this model-based projection, the ten authors of the study state their conclusion “is supported by previous studies,” including “stand-alone ecosystem models (McGuire et al., 2001), [an] offline land component of a coupled climate model (Thornton et al., 2007), [a] coupled model of intermediate complexity (Sokolov et al., 2008), and now here for the case of a fully-coupled climate system model.” In addition, they state, “each of these studies is based on either the TEM or the CLM-CN model.”
You may get the impression that Thornton et al.’s work depends just a little too heavily on models, as compared to real-world experimental data. That is indeed the case, as numerous experimental studies provide no evidence for the progressive nitrogen limitation hypothesis, even in plants growing in soils of extremely low nitrogen content, where evidence for it surely would be expected to be found if the hypothesis were correct.
Historically, far too many falsehoods have been foisted on the world by mere hypotheses and models to justify accepting the outcome of Thornton et al.’s study, especially when the numerous results of the many real-world experiments reviewed here clearly indicate the study’s conclusion is false. As ever-more long-term experiments are conducted on long-lived plants growing outdoors and rooted in the earth, where their roots are not artificially confined to a limited volume of soil, it is becoming abundantly clear that plants generally do not experience any significant decline in the initial photosynthetic stimulation provided them by the extra CO2 to which they are exposed in CO2 enrichment studies.
Addy, H.D., Piercey, M.M., and Currah, R.S. 2005. Microfungal endophytes in roots. Canadian Journal of Botany 83: 1–13.
Ainsworth, A.E., Rogers, A., Blum, H., Nosberger, J., and Long, S.P. 2003. Variation in acclimation of photosynthesis in Trifolium repens after eight years of exposure to free air CO2 enrichment (FACE). Journal of Experimental Botany 54: 2769–2774.
Alberton, O., Kuyper, T.W., and Summerbell, R.C. 2010. Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil 328: 459–470.
Crous, K.Y. and Ellsworth, D.S. 2004. Canopy position affects photosynthetic adjustments to long-term elevated CO2 concentration (FACE) in aging needles in a mature Pinus taeda forest. Tree Physiology 24: 961–970.
Darbah, J.N.T., Kubiske, M.E., Nelson, N., Kets, K., Riikonen, J., Sober, A., Rouse, L., and Karnosky, D.F. 2010. Will photosynthetic capacity of aspen trees acclimate after long-term exposure to elevated CO2 and O3? Environmental Pollution 158: 983–991.
Davey, P.A., Olcer, H., Zakhleniuk, O., Bernacchi, C.J., Calfapietra, C., Long, S.P., and Raines, C.A. 2006. Can fast growing plantation trees escape biochemical down-regulation of photosynthesis when growing throughout their complete production cycle in the open air under elevated carbon dioxide? Plant, Cell and Environment 29: 1235–1244.
Dijkstra, F.A., Pendall, E., Mosier, A.R., King, J.Y., Milchunas, D.G., and Morgan, J.A. 2008. Long-term enhancement of N availability and plant growth under elevated CO2 in a semi-arid grassland. Functional Ecology 22: 975–982.
Finzi, A.C., Norby, R.J., Calfapietra, C., Gallet-Budynek, A., Gielen, B., Holmes, W.E., Hoosbeek, M.R., Iversen, C.M., Jackson, R.B., Kubiske, M.E., Ledford, J., Liberloo, M., Oren, R., Polle, A., Pritchard, S., Zak, D.R., Schlesinger, W.H., and Ceulemans, R. 2007. Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proceedings of the National Academy of Sciences, USA 104: 14,014–14,019.
Finzi, A.C. and Schlesinger, W.H. 2003. Soil-nitrogen cycling in a pine forest exposed to 5 years of elevated carbon dioxide. Ecosystems 6: 444–456.
Fujimaki, R., Sakai, A., and Kanedo, N. 2009. Ecological risks in anthropogenic disturbance of nitrogen cycles in natural terrestrial ecosystems. Ecological Research 24: 955–964.
Hambleton, S. and Sigler, L. 2005. Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (= Hymenoscyphus ericae), Leotiomycetes. Studies in Mycology 53: 1–27
Hungate, B.A., Dukes, J.S., Shaw, M.R., Luo, Y., and Field, C.B. 2003. Nitrogen and climate change. Science 302: 1512–1513.
Hungate, B.A., Johnson, D.W., Dijkstra, P., Hymus, G., Stiling, P., Megonigal, J.P., Pagel, A.L., Moan, J.L., Day, F., Li, J., Hinkle, C.R., and Drake, B.G. 2006. Nitrogen cycling during seven years of atmospheric CO2 enrichment in a scrub oak woodland. Ecology 87: 26–40.
Iversen, C.M. 2010. Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytologist 186: 346–357.
Iversen, C.M., Ledford, J., and Norby, R.J. 2008. CO2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest. New Phytologist 179: 837–847.
Jackson, R.B., Cook, C.W., Pippen, J.S., and Palmer, S.M. 2009. Increased belowground biomass and soil CO2 fluxes after a decade of carbon dioxide enrichment in a warm-temperate forest. Ecology 90: 3352–3366.
Johnson, D.W. 2006. Progressive N limitation in forests: review and implications for long-term responses to elevated CO2. Ecology 87: 64–75.
Kernaghan, G., Sigler, L., and Khasa, D. 2003. Mycorrhizal and root endophytic fungi of containerized Picea glauca seedlings assessed by rDNA sequence analysis. Microbial Ecology 45: 128–136.
Langley, J.A. and Hungate, B.A. 2003. Mycorrhizal controls on belowground litter quality. Journal of Ecology 84: 2302–2312.
Langley, J.A., McKinley, D.C., Wolf, A.A., Hungate, B.A., Drake, B.G., and Megonigal, J.P. 2009. Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem exposed to elevated CO2. Soil Biology & Biochemistry 41: 54¬–60.
Liberloo, M., Calfapietra, C., Lukac, M., Godbold, D., Luo, Z.-B., Polle, A., Hoosbeek, M.R., Kull, O., Marek, M., Raines, C., Rubino, M., Taylor, G., Scarascia-Mugnozza, G., and Ceulemans, R. 2006. Woody biomass production during the second rotation of a bio-energy Populus plantation increases in a future high CO2 world. Global Change Biology 12: 1094–1106.
Liberloo, M., Tulva, I., Raim, O., Kull, O., and Ceulemans, R. 2007. Photosynthetic stimulation under long-term CO2 enrichment and fertilization is sustained across a closed Populus canopy profile (EUROFACE). New Phytologist 173: 537–549.
Luo, Y., Su, B., Currie, W.S., Dukes, J.S., Finzi, A., Hartwig, U., Hungate, B., McMurtrie, R.E., Oren, R., Parton, W.J., Pataki, D.E., Shaw, M.R., Zak, D.R., and Field, C.B. 2004. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. BioScience 54: 731–739.
Mandyam, K. and Jumpponen, A. 2005. Seeking the elusive function of the root-colonizing dark septate endophytic fungi. Studies in Mycology 53: 173–189.
McCarthy, H.R., Oren, R., Johnsen, K.H., Gallet-Budynek, A., Pritchard, S.G., Cook, C.W., LaDeau, S.L., Jackson, R.B., and Finzi, A.C. 2010. Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development. New Phytologist 185: 514–528.
McCormack, M.L., Pritchard, S.G., Breland, S., Davis, M.A., Prior, S.A., Runion, G.B., Mitchell, R.J., and Rogers, H.H. 2010. Soil fungi respond more strongly than fine roots to elevated CO2 in a model regenerating longleaf pine-wiregrass ecosystem. Ecosystems 13: 901–916.
McGuire, A.D., Sitch, S., Clein, J.S., Dargaville, R., Esser, G., Foley, J., Heimann, M., Joos, F., Kaplan, J., Kicklighter, D.W., Meier, R.A., Melillo, J.M., Moore III, B., Prentice, I.C., Ramankutty, N., Reichenau, T., Schloss, A., Tian, H., Williams, L.J., and Wittenberg, U. 2001. Carbon balance of the terrestrial biosphere in the twentieth century: analyses of CO2, climate and land use effects with four process-based ecosystem models. Global Biogeochemical Cycles 15: 183–206.
Nelson, J.A., Morgan, J.A., LeCain, D.R., Mosier, A., Milchunas, D.G., and Parton, B.A. 2004. Elevated CO2 increases soil moisture and enhances plant water relations in a long-term field study in semi-arid shortgrass steppe of Colorado. Plant and Soil 259: 169–179.
Paoletti, E., Seufert, G., Della Rocca, G., and Thomsen, H. 2007. Photosynthetic response to elevated CO2 and O3 in Quercus ilex leaves at a natural CO2 spring. Environmental Pollution 147: 516–524.
Pritchard, S.G., Strand, A.E., McCormack, M.L., Davis, M.A., Finzi, A.C., Jackson, R.B., Matamala, R., Rogers, H.H., and Oren, R. 2008a. Fine root dynamics in a loblolly pine forest are influenced by free-air-CO2-enrichment: a six-year-minirhizotron study. Global Change Biology 14: 588–602.
Pritchard, S.G., Strand, A.E., McCormack, M.L., Davis, M.A., and Oren, R. 2008b. Mycorrhizal and rhizomorph dynamics in a loblolly pine forest during 5 years of free-air-CO2-enrichment. Global Change Biology 14: 1–13.
Reich, P.B., Hungate, B.A., and Luo, Y. 2006. Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annual Review of Ecology, Evolution and Systematics 37: 611–636.
Schoning, I. and Kogel-Knabner, I. 2006. Chemical composition of young and old carbon pools throughout Camisol and Luvisol profiles under forests. Soil Biology and Biochemistry 38: 2411–2424.
Schulz, B. and Boyle, C. 2005. The endophytic continuum. Mycological Research 109: 661–686.
Sholtis, J.D., Gunderson, C.A., Norby, R.J., and Tissue, D.T. 2004. Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand. New Phytologist 162: 343–354.
Sieber, T.N. and Grunig, C.R. 2006. Biodiversity of fungal root-endophyte communities and populations, in particular of the dark septate endophyte Phialocephala fortinii s.1.In Microbial Root Endophytes [of series], edited by B. Schulz, C. Boyle, and T.N. Sieber. Soil Biology 9: 107–132.
Sokolov, A.P., Kicklighter, D.W., Melillo, J.M., Felzer, B.S., Schlosser, C.A., and Cronin, T.W. 2008. Consequences of considering carbon-nitrogen interactions on the feedbacks between climate and the terrestrial carbon cycle. Journal of Climate 21: 3776–3796.
Thornton, P.E., Doney, S.C., Lindsay, K., Moore, J.K., Mahowald, N., Randerson, J.T., Fung, I., Lamarque, J.-F., Feddema, J.J., and Lee, Y.-H. 2009. Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model. Biogeosciences 6: 2120–2120.
Thornton, P.E., Lamarque, J.F., Rosenbloom, N.A., and Mahowald, N.M. 2007. Influence of carbon-nitrogen cycle coupling on land model response to CO2 fertilization and climate variability. Global Biogeochemical Cycles 21: 10.1029/2006GB002868.
Trumbore, S. 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecological Applications 10: 399–411.
Wang, Z., Johnston, P.R., Takamatsu, S., Spatafora, J.W., and Hibbett, D.S. 2006. Toward a phylogenetic classification of the Leotiomycetes based on rDNA data. Mycologia 98: 1065–1075.