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Long-Term Studies (Woody Plants - Pine Trees: Loblolly Pine) -- Summary
It is important to know how earth's trees will likely respond to the ongoing rise in the air's CO2 content over the long-term; and the only way to obtain such knowledge is to enrich the air in which they grow in long-term experiments. In what follows, we review what has been learned in this regard with respect to loblolly pine (Pinus taeda L.) trees.

In what was originally considered to be a long-term study, Tissue et al. (1997) grew loblolly pine seedlings for four years in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 650 ppm. Throughout the summers of this experiment, the seedlings in the CO2-enriched chambers displayed photosynthetic rates that were 60-130% greater than those of the seedlings growing in ambient air; while during the colder winter months, they exhibited photosynthetic rates that were 14 to 44% greater. These persistent increases in the rate of net carbon uptake increased biomass accumulation rates in the CO2-enriched seedlings by fully 90%, prompting the scientists conducting the study to declare that loblolly pines growing in a CO2-enriched world of the future "could be a large sink for fossil fuel carbon emitted to the atmosphere."

In another study of the same trees, Telewski et al. (1999) determined that elevated CO2 did not significantly affect anatomical features of xylem cells, including their cell wall to cell interior ratio, resin canal area, and resin canal density, but that it did significantly increase annual growth-ring widths by 93, 29, 15 and 37% during the four consecutive years of the study. Also, although not significantly so, the extra CO2 increased average ring density in the same four years by 60, 4, 3 and 5%, leading the researchers to state that "projected increases in the atmospheric content of CO2 may result in increased wood production without a loss in structural strength." Indeed, the tendency for wood density to increase in CO2-enriched air portends the possibility of increased structural strength in the years ahead.

By far the longest study of loblolly pines, however, was the free-air CO2 enrichment or FACE experiment conducted at Duke Forest in the Piedmont region of North Carolina, USA, where in August of 1996 three 30-m-diameter CO2 delivery rings began to enrich the air around the 13-year-old trees they encircled to 200 ppm above the atmosphere's ambient CO2 concentration, while three other FACE rings served as ambient-air control plots, as described by Hendrey et al. (1999). In this study, LaDeau and Clark (2001) found that by the fall of 1999, the CO2-enriched trees "were twice as likely to be reproductively mature and produced three times more cones per tree." Similarly, the trees growing in the CO2-enriched air produced 2.4 times more cones in the fall of 2000. From August 1999 through July 2000, the two scientists also collected three times as many seeds in the CO2-enriched FACE rings as they did in the ambient-air control rings.

These findings are particularly important, for LaDeau and Clark report that naturally-regenerated loblolly pine stands of the southeastern United States "are profoundly seed-limited for at least 25 years." Hence, as the air's CO2 content continues to climb, the researchers state that "this period of seed limitation may be reduced," which is more good news for this highly-prized tree -- the other good news being the fact that, according to William Schlesinger, co-director of the Duke project (Tangley, 2001), "trees in the high-CO2 plots grew 25% faster than controls did during the first three growing seasons of the experiment."

One year later, Finzi et al. (2002) reported that over the first four years of differential CO2 exposure in this study, the trees in the CO2-enriched plots maintained average yearly rates of dry matter production that were 32% greater than those of the trees growing in ambient air, while the average uptake of nitrogen from the soil was enhanced by 28% in the CO2-enriched plots, and the CO2-enriched trees displayed a 10% increase in nitrogen-use efficiency.

Several other papers dealing with various aspects of the experiment were published about the same time. As recounted by Luo et al. (2003), these analyses revealed the existence of a CO2-induced "sustained photosynthetic stimulation at leaf and canopy levels [Myers et al., 1999; Ellsworth, 2000; Luo et al., 2001; Lai et al., 2002], which resulted in sustained stimulation of wood biomass increment [Hamilton et al., 2002] and a larger carbon accumulation in the forest floor at elevated CO2 than at ambient CO2 [Schlesinger and Lichter, 2001]." And based upon these findings and what they implied about rates of carbon removal from the atmosphere and its different residence times in plant, litter and soil carbon pools, Luo et al. (2003) developed a model for studying the sustainability of carbon sequestration in forests; and applying this model to a situation where the atmospheric CO2 concentration gradually rises from a value of 378 ppm in 2000 to a value of 710 ppm in 2100, they calculated that the carbon sequestration rate of the Duke Forest would rise from an initial value of 69 g m-2 yr-1 to a final value of 201 g m-2 yr-1. But this good news, and even further good news, was soon to be followed with almost unbridled pessimism.

As a case in point, Schafer et al. (2003) linked a leaf-level CO2 assimilation model (Katul et al., 2000) with a light attenuation model (Campbell and Norman, 1998; Stenberg, 1998) and measurements of sap-flux-based canopy conductance (Kostner et al., 1992; Ewers and Oren, 2000) to create what they called a canopy conductance-constrained CO2 assimilation model, which they tested with measurements of net ecosystem exchange and net ecosystem production in the ambient and CO2-erniched plots of the Duke Forest FACE study, after which they used it to asses the effects of elevated CO2 on carbon uptake and allocation to different components of the forest's carbon budget under ambient and CO2-enriched conditions. In doing so, they found that during the third and fourth years of the study, the extra 200 ppm of CO2 supplied to the CO2-enriched FACE plots increased the uptake of CO2 by 39% in the dominant Pinus taeda L. trees.

These results were most impressive. However, many of the scientists of that time were pessimistic about the future. Even Schafer et al. suggested that "if nutrient limitation imposes a constraint on future productivity," as was widely believed would be the case, "it is likely that carbon allocation to the production of wood will decrease in favor of the allocation to fine root production, rhizodeposition, and mycorrhizal symbionts," citing Norby et al. (1992, 2001), which they further suggested could "result in a rapid return of fixed carbon to the atmosphere (Merbach et al., 1999)," such that "high rates of carbon fixation under elevated CO2 will result in an acceleration of the carbon cycle through the forest ecosystem with little of the carbon remaining in long-term storage pools."

Indeed, it was well accepted at the time that the productivity of earth's temperate forests was limited by the availability of soil nitrogen (Vitousek and Howarth, 1991). Especially was this believed to be the case in the southeastern United States, where pine-hardwood forests often remove so much nitrogen from the soils in which they grow that they induce what Finzi and Schlesinger (2003) describe as "a state of acute nutrient deficiency that can only be reversed with fertilization." It would seem only natural, therefore, to presume (as they indeed hypothesized in the early stages of the Duke Forest FACE study), that "the increase in carbon fluxes to the microbial community under elevated CO2 would increase the rate of nitrogen immobilization over mineralization," which would ultimately lead to a decline in -- and perhaps the total negation of -- the significant CO2-induced stimulation of forest net primary production that developed over the first two years of the experiment (DeLucia et al., 1999; Hamilton et al., 2002).

To test this hypothesis, Finzi and Schlesinger (2003) measured and analyzed the 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 in the Duke Forest FACE study, where half of the plots were fumigated so as to maintain them at a mean CO2 concentration 200 ppm above ambient. This effort revealed that the extra CO2 "significantly increased the input of carbon and nitrogen to the forest floor and the mineral soil." Nevertheless, they found "there was no statistically significant change in the cycling rate of nitrogen derived from soil organic matter under elevated CO2." Indeed, they discovered that "neither the rate of net nitrogen mineralization nor gross 15NH4+ dynamics were significantly altered by elevated CO2." In addition, they acknowledged "there was no statistically significant difference in the concentration or net flux of organic and inorganic nitrogen in the forest floor and top 30-cm of mineral soil after five years of CO2 fumigation," concluding that "microbial biomass was not a larger sink for nitrogen."

On the basis of these results from the first five years of the Duke Forest FACE study, Finzi and Schlesinger rejected their original hypothesis, which was that elevated levels of atmospheric CO2 would significantly increase the rate of nitrogen immobilization by the microbial community, although they continued to contend that "elevated CO2 will only increase the productivity of this forest during the initial stages of stand development, with nitrogen limitation constraining additional carbon sequestration under elevated CO2 well before this stand reaches its equilibrium biomass." And at that point in time, we wrote the following in our review of their paper:

Will the two researchers ultimately be proven to be correct? Or will the real world surprise them once again? We will have to wait and see, trusting that their diligence and attention to details of observation and analysis will someday reveal the truth of the matter ... whatever it may be ... whenever it is clearly evident.

So what occurred subsequently?

Crous and Ellsworth (2004) measured the photosynthetic rates of different-age needles at different crown positions on the loblolly pine trees at the Duke Forest FACE facility in the sixth year of the study, after which they compared their results with the results of similar measurements made over the prior five years. Although they reported there was "some evidence of moderate photosynthetic down-regulation ... in 1-year-old needles across the fifth to sixth year of CO2 exposure," the two researchers said that "strong photosynthetic enhancement in response to elevated CO2 (e.g., +60% across age classes and canopy locations) was observed across the years."

Also at the conclusion of the sixth year of the study, Lichter et al. (2005) reviewed what had been learned about the effects of the extra CO2 on the soil carbon dynamics of Duke Forest. Their work revealed that since the beginning of the study, organic carbon had accumulated in the forest floor of the elevated CO2 plots at a rate that was 52 16 g C m-2 yr-1 greater than would have been expected during reforestation under ambient CO2 conditions, as represented by the rate of carbon accumulation in the forest floor of the ambient CO2 plots. This additional carbon sink, in the words of the researchers, "resulted from increased carbon inputs of 50 30 g C m-2 yr-1 to the forest floor in response to CO2 enhancement of primary production." And since there was "no evidence that the overall rate of decomposition of the forest floor decreased under the elevated CO2 treatment," they concluded that "the additional carbon sink in the forest floor of the elevated CO2 treatment ... is wholly dependent on the net primary production enhancement and increased carbon inputs," which after a total of six years had increased the forest floor's organic carbon content by approximately 27%, as best we could determine from their plotted data. What is more, the data gave no indication that this trend was on the verge of declining anytime soon.

With respect to the underlying mineral soil, Lichter et al. said they could detect no statistically significant treatment effects on the carbon content of the bulk mineral soil or the intra-aggregate particulate organic matter and mineral-associated organic matter fractions after six years of CO2 enrichment. Nevertheless, there was a nearly statistically significant (P = 0.11) increase of 18.5% in the free light fraction of the organic matter in the top 15 cm of the soil profile, as well as a 3.9% increase in the total intra-aggregate particulate organic matter there; and the sum of the organic carbon in these two different categories plus the mineral-associated organic carbon was 11.5% greater in the CO2-enriched plots than in the ambient treatment plots.

Although the scientists who conducted the work were still pessimistic and continued to believe that "forest soils are unlikely to sequester significant additional quantities of atmospheric carbon associated with CO2 fertilization because of the low rates of carbon input to refractory and protected soil organic matter pools," the CO2-enriched trees of their study continued to demonstrate a large and unabated growth advantage over the ambient-CO2 trees; and both the forest floor and the surface soil horizon beneath the CO2-enriched trees continued to accumulate more organic carbon than the forest floor and surface soil horizon beneath the ambient-CO2 trees.

Returning to the subject of tree fecundity, LaDeau and Clark (2006) once again determined the reproductive responses (cone and seed production) of the loblolly pine trees at the Duke Forest FACE site to atmospheric CO2 enrichment; and in doing so they determined that "carbon dioxide enrichment affected mean cone production both through early maturation and increased fecundity," so that "trees in the elevated CO2 plots produced twice as many cones between 1998 and 2004 as trees in the ambient plots." They also reported finding that trees grown in elevated CO2 "made the transition to reproductive maturation at smaller [trunk] diameters," and that they "not only reached reproductive maturation at smaller diameters, but also at younger ages." By 2004, for example, they say that "roughly 50% of ambient trees and 75% of fumigated trees [had] produced cones." In addition, they observed that "22% of the trees in high CO2 produced between 40 and 100 cones during the study, compared with only 9% of ambient trees."

As for the significance of their findings, the two scientists said they indicate that their previously documented "short-term responses indeed persist," in contradiction of the opinions of what we could call biological pessimists, who attempt to downplay the immense biological benefits of atmospheric CO2 enrichment. Furthermore, noting that "P. taeda trees that produce large seed crops early in their life span tend to continue to be prolific producers (Schutlz, 1997)," they concluded that this fact, together with their own findings, suggests that "individual responses seen in this young forest may be sustained over their life span."

At the eight-year point of the long-term FACE experiment, Moore, et al. (2006) conducted a study that represented a turning point in most scientists' thinking with regard to what had come to be known as the Progressive Nitrogen Limitation hypothesis, wherein they analyzed measurements of the basal areas of the trees' trunks at approximately 1.4 m above ground level that had been made at monthly intervals since the inception of the experiment. This work revealed that in response to the 50% increase in atmospheric CO2 concentration employed in the Duke Forest FACE study, there was "a sustained increase in basal area increment over the first 8 years of the experiment" that varied between 13 and 27% with variations in weather and the timing of growth. What is more, the six scientists found "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 was pretty amazing to many people (including several who were working on the experiment themselves), considering the low-fertility state of the soil in which the experiment was being conducted. Nevertheless, and in spite of the presumptions of many researchers that the CO2-induced growth stimulation of long-lived woody plants would gradually (and drastically) decline with the passage of time, there was no evidence that such was occurring in the Duke Forest FACE study, where the trees just kept chugging along at a significantly elevated rate, even when nutrient limitations would have "normally" been expected to have kept them from doing so.

Two years later, Pritchard et al. (2008a) used minirhizotrons to characterize the fine root development of the trees from the Autumn of 1998 through the Autumn of 2004. Averaged over all six years of the study, they found that the extra 200 ppm of CO2 increased average fine-root standing crop by 23%, in good agreement with the stimulation of the forest's net primary productivity of 18-24% observed over the period 1996-2002.

In summing up their findings, the nine researchers wrote that "the positive effects of CO2 enrichment on fine root growth persisted 6 years following minirhizotron tube installation (8 years following initiation of the CO2 fumigation)," which observations once again provided no hint of any progressive nitrogen limitation of the stimulatory effect of atmospheric CO2 enrichment in a situation where one might have expected to have encountered it. In partial explanation of this important positive finding, Pritchard et al. noted 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." And in this regard, we note that nearly all evidence obtained to date continues to suggest that earth's trees can indeed sustain a significant CO2-induced increase in net primary productivity over the long haul, and that the reason they can do so may well reside in the CO2-induced stimulation of the growth of their important fine-root tips, as suggested by Pritchard et al.

In a related contemporaneous paper, Pritchard et al. (2008b) wrote that data from long-term FACE experiments "have yet to provide convincing evidence in support of the progressive nitrogen limitation hypothesis." In fact, they reported that exposure to elevated concentrations of atmospheric CO2 had increased net primary productivity by 59%, 24%, 23% and 30% at the Rhinelander, Wisconsin (USA), Oak Ridge National Laboratory (USA), Tuscania (Italy), and Duke, North Carolina (USA) FACE sites, respectively, "with little evidence to indicate a diminished response through time," citing the analysis of Finzi et al. (2007) in this regard.

The leading hypothesis to explain these sustained high growth responses has been that atmospheric CO2 enrichment leads to greater fine-root production and increased allocation of carbon to ectomycorrhizal fungi that live in symbiotic association with plant roots, which dual phenomenon leads to (1) the exploration of a greater volume of soil by plants in search of much needed nitrogen, as well as (2) a more thorough search of each unit volume of soil. Consequently, Pritchard et al. (2008b) focused their attention on the role played by ectomycorrhizal fungi over a period of five years in the Duke Forest FACE study.

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 a whopping 194% throughout the 15-30 cm depth interval. In addition, they report that production of soil rhizomorph length was 27% greater in CO2-enriched plots than it was in the ambient-air plots.

In discussing their findings, Pritchard et al. note 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 study has been determined to be approximately 12 g N per m2 per year, which is well above estimated rates of N acquisition by the combined phenomena of N deposition, heterotrophic N fixation, and net N mineralization, which range from 3.4 to 6.0 g N per m2 per year, as per the findings of Finzi et al. (2006, 2007), Hofmockel and Schlesinger (2007) and Hofmockel et al. (2007). Consequently, in concluding their commentary 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 nitrogen-limited ecosystems more than previously expected."

Last of all, we come to the study of Jackson et al. (2009), who describe new belowground data they obtained at the Duke Forest FACE site, after which they present a synthesis of these and other results obtained for the period running from 1996 through 2008, seeking to determine "which, if any, variables show evidence for a decrease in their response to atmospheric CO2 during that time frame." Their various analyses indicate, among many other things, 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 report that "biomass sampled in 2008 was "twice as great in elevated CO2." In fact, we calculate 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 say that "overall, the effect of elevated CO2 belowground shows no sign of diminishing."

In discussing their findings, the four researchers state 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 they say that "in fact 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 [italics added]," 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).

As a result of these most recent findings, plus all that preceded them, there are many extremely well documented observational -- as opposed to theoretical -- reasons 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.

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Last updated 3 March 2010