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Progressive Nitrogen Limitation Hypothesis (Loblolly Pine) -- Summary
As part of one of the most outstanding of such studies ever to be conducted, Finzi and Schlesinger (2003) measured and analyzed pool sizes and fluxes of inorganic and organic nitrogen in the forest floor and top 30 cm of mineral soil during the first five years of differential atmospheric CO2 treatment of a stand of initially 13-year-old loblolly pine trees at the Duke Forest FACE facility in the Piedmont region of North Carolina (USA), where half of the experimental plots were maintained at an atmospheric CO2 concentration approximately 200 ppm above ambient. Under these conditions, they found that the extra CO2 significantly increased the input of carbon (C) and nitrogen (N) to the forest floor, as well as to the mineral soil in which the trees were growing. However, they reported "there was no statistically significant change in the cycling rate of N derived from soil organic matter under elevated CO2" and that "neither the rate of net N mineralization nor gross 15NH4+ dynamics were significantly altered by elevated CO2." In fact, they could find "no statistically significant difference in the concentration or net flux of organic and inorganic N in the forest floor and top 30-cm of mineral soil after 5 years of CO2 fumigation," adding that "microbial biomass was not a larger sink for N." And based on these findings, they actually rejected their own original hypothesis, which was essentially the same as the PNL hypothesis, i.e., that the extra CO2 provided to the experimental plots would significantly increase the rate of nitrogen immobilization by the soil microbial communities found within the CO2-enriched FACE arrays and thereby lead to a lack-of-N-induced reduction in the magnitude of the growth stimulation that was initially manifest in the CO2-enriched treatment.

Working at the same location, Schafer et al. (2003) measured net ecosystem exchange (NEE) and net ecosystem production (NEP) during the third and fourth years of the long-term CO2 enrichment study being conducted there. And in doing so, they found that the extra 200 ppm of CO2 supplied to the loblolly pine trees within the CO2-enriched FACE arrays increased the entire canopy's net uptake of CO2 (NEE) by fully 41%, and that canopy NEP was increased by 44%. In addition, they determined that 87% of the extra NEP "was sequestered in a moderately long-term C pool in wood." This large increase in solidly-sequestered carbon was truly amazing, especially in light of the remark of Finzi and Schlesinger (2003) that the soil at the Duke Forest FACE site was in "a state of acute nutrient deficiency that can only be reversed with fertilization," which, of course, was not provided.

Three years later, Finzi et al. (2006) once again tested the PNL concept "using data on the pools and fluxes of C and N in tree biomass, microbes and soils," which were obtained from the first six years of the Duke Forest FACE study. As was the case three years earlier, it was once again found that "there was no reduction in the average stimulation of net primary production by elevated CO2," even though "significantly more N was immobilized in tree biomass and in the O [soil] horizon under elevated CO2." Also, and "in contrast to the PNL hypothesis," as they described it, "microbial-N immobilization did not increase under elevated CO2, and although the rate of net N mineralization declined through time, the decline was not significantly more rapid under elevated CO2." In addition, the twelve researchers reported that "mass balance calculations demonstrated a large accrual of ecosystem N capital," and they said that the rate of extra N accrual was "much greater than the estimated rate of N input via atmospheric deposition or heterotrophic N fixation," noting further that "there are no plant species capable of symbiotic N fixation in this ecosystem." In other words, by some unknown means the loblolly pine trees obtained the extra N they needed to stave off the negative effects predicted by the PNL hypothesis, possibly, in the words of Finzi et al., by roots "actively taking up N and redistributing N from deeper in the soil profile."

With the passage of two additional years, Moore et al. (2006) reported finding "a sustained increase in basal area increment over the first 8 years of the experiment," which varied between 13 and 27% in harmony with variations in weather and the timing of growth. They also reported "there was no evidence of a decline in the relative enhancement of tree growth by elevated CO2 as might be expected if soil nutrients were becoming progressively more limiting," which would normally be expected, considering the unfertilized state of the soil in which the experiment was being conducted.

Two years later still, Pritchard et al. (2008a) published the results they had obtained from mini-rhizotrons they had employed to characterize the influence of the extra 200 ppm of CO2 on the fine roots of the Duke Forest loblolly pines over the six-year period 1998-2004. Averaged over all six years, they found that the extra CO2 had increased average fine-root standing crop by 23%, which compared well with the overall stimulation of tree net primary productivity of 18-24% observed over the period 1996-2002. Consequently, and in light of their noting that "the positive effects of CO2 enrichment on fine root growth persisted 6 years following mini-rhizotron tube installation (8 years following initiation of the CO2 fumigation)," as they described it, there was once again no hint of any progressive nitrogen limitation to the stimulatory effect of atmospheric CO2 enrichment in a situation where one would have expected to have encountered it. In partial explanation of this important positive finding, Pritchard et al. concluded their report by stating that the distal tips of fine roots are "the primary site for initiation of mycorrhizal partnerships which are critical for resource acquisition and could also influence whether or not forests can sustain higher productivity in a CO2-enriched world."

In a study designed to further explore this aspect of the ongoing long-term Duke Forest FACE experiment, Pritchard et al. (2008b) focused their attention on the role played by ectomycorrhizal (ECM) fungi over a period of five years, based on mini-rhizotron observations of fungal dynamics. Summed across all years of the study, the five researchers found that the extra 200 ppm of CO2 enjoyed by the trees in the high-CO2 treatment did not influence mycorrhizal production in the top 15 cm of the forest soil, but that it increased mycorrhizal root-tip production by 194% throughout the 15-30 cm depth interval. In addition, they reported that production of soil rhizomorph length was 27% greater in the CO2-enriched plots than it was in the ambient-air plots.

In discussing their findings, Pritchard et al. stated that the CO2-induced "stimulation of carbon flow into soil has increased the intensity of root and fungal foraging for nutrients," and that "the shift in distribution of mycorrhizal fungi to deeper soils may enable perennial plant systems to acquire additional soil nitrogen to balance the increased availability of ecosystem carbohydrates in CO2-enriched atmospheres," which additional acquisition of nitrogen in the CO2-enriched plots of the Duke Forest FACE study had been determined to be approximately 12 g N per m2 per year.

In further commenting on the results of their work, Pritchard et al. wrote that "the notion that CO2 enrichment expands the volume of soil effectively explored by roots and fungi, and that foraging in a given volume of soil also seems to intensify, provides compelling evidence to indicate that CO2 enrichment has the potential to stimulate productivity (and carbon sequestration) in N-limited ecosystems more than previously expected." On the other hand, they also said "it is unlikely that ecosystem productivity will be stimulated by CO2 enrichment indefinitely." Be that as it may, nature had to this point in time proved such negative hunches wrong, essentially every step of the way, as scientists probed ever deeper into this particular conundrum.

About this same time, in the introduction to their paper summarizing nine years of work at the Duke Forest FACE facility, Lichter et al. (2008) once again warned that progressive nitrogen limitation may "accompany carbon sequestration in plants and soils stimulated by CO2 fertilization, gradually attenuating the CO2 response," after which they went on to describe what they had learned about the PNL hypothesis over the prior nine years.

The team of nine scientists noted, first of all, that their data pertaining to forest-floor carbon pools indicated the existence of "a long-term steady-state sink" of about 30 g C per m2 per year, which represented, in their words, "a substantial increase in forest-floor C storage under elevated CO2 (i.e. 29%)," and which they attributed to "increased litterfall and root turnover during the first 9 years of the study." Secondly, down below the forest floor, they said that of the mineral soil carbon formed during the prior 9 years, "approximately 20% has been allocated to stable pools that will likely remain protected from microbial activity and associated release as CO2."

A third important finding of the research team was "a significant widening of the C/N ratio of soil organic matter in the upper mineral soil under both elevated and ambient CO2," which suggested, as they described it, that "enhanced rates of soil organic matter decomposition are increasing mineralization and uptake to provide the extra N required to support the observed increase in primary productivity under elevated CO2." At the Duke Forest FACE site, Pritchard et al. (2008b) said that this CO2-induced increase in productivity amounted to approximately 30% annually; and they added that there was "little evidence to indicate a diminished response through time," citing the analysis of Finzi et al. (2007), who had found the same to be true at the long-term forest FACE studies being conducted at Rhinelander, Wisconsin (USA), Oak Ridge National Laboratory (USA), and Tuscania (Italy).

Contrary to the early expectations of many scientists, it would thus appear that many of earth's forests that were thought to have had access to less-than-adequate soil nitrogen supplies may indeed be able to acquire the extra nitrogen they need to maintain the sizable increases in their growth rates that are driven by elevated concentrations of atmospheric CO2. In the case of North Carolina's Duke Forest, for example, "even after nine years of experimental CO2 fertilization," as Lichter et al. described it, "attenuation of the CO2-induced productivity enhancement has not been observed," as was also found to be the case by Finzi et al. (2006). And this finding at this specific location is extremely significant, because the growth of pine-hardwood forests in the southeastern United States often removes so much nitrogen from the soils in which they grow that they induce what Finzi and Schlesinger (2003) have described as "a state of acute nutrient deficiency that can only be reversed with fertilization," which operation, as noted earlier in this document, was not employed at the Duke Forest FACE study.

One year later, Jackson et al. (2009) described new belowground data they had obtained at the Duke Forest Face site, after which they presented a synthesis of these and other results that had been obtained over the period running from 1996 through 2008, seeking to determine which variables may have shown a decrease in their response to atmospheric CO2 enrichment during that time frame. Among many other things, they reported that "on average, in elevated CO2, fine-root biomass in the top 15 cm of soil increased by 24%," and that in recent years the fine-root biomass increase "grew stronger, averaging ~30% at high CO2," while in terms of coarse roots having diameters greater than 2 mm and extending to a soil depth of 32 cm, they reported that "biomass sampled in 2008 was "twice as great in elevated CO2." In fact, it can be calculated from the graphical representation of their results that the coarse-root biomass was fully 130% greater, which is really astounding, particularly in light of the fact that the extra 200 ppm of CO2 supplied to the air surrounding the CO2-enriched trees represented an enhancement of only about 55% above ambient conditions. And in the concluding sentence of their paper's abstract, they wrote that "overall, the effect of elevated CO2 belowground shows no sign of diminishing."

The four researchers also remarked that "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 in contrast they indicated "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 in this regard - with respect to the latter portion of their statement - the report of Finzi et al. (2007). Consequently, there is good reason to believe that the "aerial fertilization effect" of atmospheric CO2 enrichment will continue to significantly benefit earth's forests for as long as the atmosphere's CO2 concentration continues to rise.

Working with data for the years 1996-2004, McCarthy et al. (2010) introduced their study of the Duke Forest FACE experiment by calculating the net primary productivity (NPP) of the entire ecosystem - including the loblolly pines' understory of various broadleaf species (Liriodendron tulipifera, Liquidambar styraciflua, Acer rubrum, Ulmus alata, Cornus florida) plus various other trees, shrubs and vines - as "the sum of the production of coarse wood (stems, branches, coarse roots), leaf litter (lagged for pines), fine roots and reproductive structures." And in doing so, they found that (1) "elevated CO2 increased pine biomass production, starting in 1997 and continuing every year thereafter," that (2) "the CO2-induced enhancement remained fairly consistent as the stand developed," and that (3) "elevated CO2 increased stand (pine plus all other species) biomass production every year from 1997 onwards with no trend over time," while noting that (4) the average yearly increase in NPP caused by the approximate 54% increase in the air's CO2 content was 28%. Therefore, and in spite of the original belief of many of the scientists involved in the work that low levels of soil nitrogen - especially an acute deficiency - would preclude any initial growth stimulation provided by atmospheric CO2 enrichment from long persisting, the suite of trees, bushes and shrubs that constitute the Duke Forest has continued to maintain the extra CO2-enabled vitality that it exhibited right from the start of the study, with no subsequent sign of it even beginning to taper off.

In another analysis of the subject that was published the following year, Drake et al. (2011) described how the CO2-induced enhanced rates of net primary production at the Duke Forest FACE site were likely sustained by a carbon-cascade through the root-microbe-soil system, whereby "increases in the flux of carbon belowground under elevated CO2 stimulated microbial activity" that in turn "accelerated the rate of soil organic matter decomposition and stimulated tree uptake of nitrogen bound to this soil organic matter," which process "set into motion a positive feedback maintaining greater carbon gain under elevated CO2 as a result of increases in canopy nitrogen content and higher photosynthetic nitrogen-use efficiency," the consequence of which chain of events was "the dominance of carbon storage in tree biomass."

In discussing this chain of events, Drake et al. indicated that "the long-term increase in forest productivity under elevated CO2 at the Duke FACE site appears to be maintained by a belowground exchange of tree carbon for soil nitrogen, with the quantity of carbon allocated belowground set by the availability of nitrogen in the soil and the demand for nitrogen to meet growth requirements." In fact, they wrote that "all of the belowground carbon fluxes thought to increase decomposition rates increased under elevated CO2, including root production and mortality (Pritchard et al., 2008a), root exudation (Phillips et al., 2011), fungal rhizomorph production (Pritchard et al., 2008b) and allocation of carbon to mycorrhizal fungi (Garcia et al., 2008)." And, therefore, they concluded that "the preponderance of the evidence points to increased decomposition [of organic matter] in surface soils as the primary source of additional nitrogen taken up by the trees growing under elevated CO2."

Concurrently, Phillips et al. (2011) also opined that "increased root exploration alone is unlikely to sustain plant nitrogen requirements under rising CO2 unless accompanied by the concomitant stimulation of soil microbial activity and the release of nutrients from soil organic matter." But despite the presumed importance of root exudates in this scenario, they indicated that no studies had yet quantified the effects of CO2 enrichment on exudation by mature trees, which is what they thus set out to do, in an effort to better understand why progressive nitrogen limitation had not been observed in some long-term studies of trees growing on nutrient poor soil (Langley et al., 2009; McCarthy et al., 2010).

Working at the Duke Forest FACE facility, the three researchers examined plant-microbe interactions in the rhizospheres and bulk soils of the various treatments, measuring differences in rhizosphere microbial activity and root exudation rates. And what did they find?

Phillips et al. reported that, on an annual basis, "exudation increased by c. 50% for trees enriched with CO2 in non-fertilized plots," but they said that trees were unaffected in this manner by CO2 enrichment in fertilized plots, in a dramatic demonstration of the fact that "increased root carbon efflux from CO2-enriched trees stimulates rhizosphere N cycling in low fertility soils," providing additional evidence that "rhizosphere microbes such as actinomycetes, which produce NAGase enzymes and respond strongly to CO2 at this site (Billings and Ziegler, 2008), are using energy derived from exudates to synthesize enzymes that release nitrogen from soil organic matter (Cheng and Kuzyakov, 2005)." And they emphasized that "this dramatic contrast between the fertilized and unfertilized treatments provides evidence that enhanced exudation is a mechanism trees employ for increasing nitrogen availability."

In consequence of their experimental findings, Phillips et al. thus wrote that their study demonstrates that "the enhanced carbon flux from roots to soil in low fertility forests exposed to elevated CO2 creates hotspots for microbial activity that are associated with faster rates of soil organic matter turnover and N cycling," which phenomenon provides the trees the extra nitrogen they need to take full advantage of the enhanced potential for growth that is provided by atmospheric CO2 enrichment, thereby overcoming the incorrect implications of the progressive nitrogen limitation hypothesis. And to make this point perfectly clear, they stated that their results "provide field-based empirical support suggesting that sustained growth responses of forests to elevated CO2 in low fertility soils are maintained by enhanced rates of microbial activity and N cycling fueled by inputs of root-derived carbon."

Also publishing concurrently were Hofmockel et al. (2011), who reported the observational fact that "several free-air CO2 enrichment (FACE) experiments in North America have shown a continual stimulation in forest productivity under elevated CO2 over time scales nearly reaching a decade (Finzi et al., 2006; Norby and Iversen, 2006; Zak et al., 2007; McCarthy et al., 2010)." And in their most recent examination of the effects of elevated CO2 on nitrogen (N) cycling in the Duke Forest - where they indicated that elevated atmospheric CO2 concentrations had "consistently stimulated forest productivity" throughout the decade-long experiment being conducted there - they went on to provide "an integrated understanding" of this phenomenon that serves as "a basis for inferring how C and N cycling in this forest may respond to elevated CO2 beyond the decadal time scale."

"Using natural-abundance measures of nitrogen isotopes together with an ecosystem-scale 15N tracer experiment," as the six scientists described it, they "quantified the cycling of 15N in plant and soil pools under ambient and elevated CO2 over three growing seasons to determine how elevated CO2 changed nitrogen cycling between plants, soil and microorganisms," after having first measured natural-abundances of 15N in plant and soil pools within the two CO2 treatments over the prior year. And as a result of these efforts, they discovered that "at the Duke FACE site, the rate at which N is being sequestered in plant biomass is greater than the rate of atmospheric deposition and heterotrophic N fixation," which had also been established by the work of Finzi et al. (2002), Hofmockel and Schlesinger (2007) and Sparks et al. (2008), all of which findings suggesedt, in their words, that "soil organic matter decomposition supplies a significant fraction of plant N in both ambient and elevated-CO2 conditions, but that this is greater under elevated CO2."

Based on these real-world experimental observations, therefore, Hofmockel et al. concluded that "in pine forests of the southeastern United States, rising CO2 may elicit shifts in the mechanisms by which plants acquire nitrogen, allowing a sustained increase in net primary productivity for decades," while further opining that "increased mineralization of nitrogen in the organic and 0-15 cm mineral horizon and deeper rooting are likely sustaining the elevated CO2 enhancement of net primary productivity."

Moving ahead one more year, Ellsworth et al. (2012) "compiled a comprehensive dataset measured over ten years for a temperate pine forest of Pinus taeda, but also including deciduous species, primarily Liquidambar styraciflua," which they derived from "over one thousand controlled-response curves of photosynthesis as a function of environmental drivers (light, atmospheric CO2 concentration [Ca] and temperature) measured at canopy heights up to 20 meters over eleven years (1996-2006)," from which they generated "parameterizations for leaf-scale models for the Duke free-air CO2 enrichment (FACE) experiment."

This laborious effort revealed that the enhancement of light-saturated leaf net photosynthesis (Anet) in P. taeda trees produced by an elevated Ca of +200 ppm was 67% for current-year needles in the upper crown of the trees in summer conditions over the ten-year period, while previous-year foliage Anet was enhanced by 30%, with the result that "the mean stimulation in light-saturated Anet averaged over the growing season of all years and across canopy positions and needle age classes was 53 7%." And they added that "the photosynthetic enhancement responses to elevated Ca are mirrored in part by the pine biomass accumulation responses to elevated Ca across different years."

The eight researchers also reported that "co-dominant and sub-canopy L. styraciflua trees showed Anet enhancement of 62%," while "various understory deciduous tree species showed an average Anet enhancement of 42%." In addition, they noted that "the photosynthetic responses of shaded, understory leaves suggest a capacity to increase photosynthetic carbon capture in elevated Ca in shade-grown plants when measured in sunflecks," citing the work of DeLucia and Thomas (2000). And they noted that this response suggests "a competitive advantage to shade-tolerant species adapted for carbon capture in high sunlight or sunflecks in the understory over less shade-tolerant species."

This comprehensive set of photosynthesis measurements compiled over the course of the Duke Forest FACE study clearly rebuts the progressive nitrogen limitation hypothesis, which posits that the initial growth stimulation of atmospheric CO2 enrichment will dwindle away as time progresses, especially in the case of the pine-hardwood forests of the southeastern United States, which often remove so much nitrogen from the soils in which they grow that they induce what Finzi and Schlesinger (2003) have described as "a state of acute nutrient deficiency that can only be reversed with fertilization." However, as was demonstrated by Ellsworth et al.'s study, such is simply not the case. And in another satisfying implication of their findings, the eight researchers concluded that the observed "differences in photosynthetic responses between the over-story pines and deciduous tree sub-canopy suggest that increased Ca may have the potential to enhance the mixed-species composition of planted pine stands," and, by extension, "naturally regenerating pine-dominated stands."

Rounding out this review of the now-long-discredited progressive nitrogen limitation hypothesis, is the study of Phillips et al. (2012), who wrote that "after nearly two decades of research on forest ecosystem responses to global change, uncertainty about the role of roots and rhizosphere processes in soil C and N retention and loss has limited our ability to predict biogeochemical feedbacks to long-term forest productivity." But now ... working at the Duke Forest FACE site in Orange County, North Carolina (USA), where eight 30-meter-diameter plots of loblolly pine (Pinus taeda L.) trees were enriched with an extra 200 ppm of CO2 from 1996 to 2010, while four similar plots were maintained under then-current ambient-air conditions, Phillips et al. measured root-induced changes in soil C dynamics of trees exposed to CO2 and nitrogen enrichment by combining stable isotope analyses, molecular characterizations of soil organic matter, and microbial assays. And what did they learn?

When all was said and done, the six scientists concluded that the CO2-enriched trees "may be both enhancing the availability of N by stimulating microbial decomposition of soil organic matter via priming and increasing the rate at which N cycles through the microbial pools owing to the rapid turnover of N-rich fungal tissues," noting that "the accelerated turnover of hyphal tissues under elevated CO2 may represent an important source of N to plants and microbes." And referring to this CO2-induced phenomenon as the Rhizo-Accelerated Mineralization and Priming or RAMP hypothesis, Phillips et al. suggested that it may have "important consequences for N availability and forest productivity," which consequences could logically be expected to sustain CO2-enhanced tree growth over the lifetime of the trees. And all indications to date are that they cannot be far off the mark in this conclusion.

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Last updated 18 June 2014