In this regard, one can readily see and measure the carbon that goes into the aboveground components of forests. But what about the underground components? And how does the ongoing rise in the atmosphere's CO2 concentration -- which is the supposed cause of the problem -- contribute to its resolution? In this review, we summarize the findings of several studies of conifers that address this question.

Janssens et al. (1998) grew three-year-old Scots pine seedlings for a period of six months in open-top chambers maintained at ambient and 700 ppm atmospheric CO2 concentrations, finding that the extra CO2 increased total root length by 122% and total root dry mass by 135%. Likewise, in a study that employed close to the same degree of enhancement of the air's CO2 content, Pritchard et al. (2001a) grew ecosystems representative of regenerating longleaf pine forests of the southeastern USA for a period of 18 months in large soil bins located within open-top chambers, finding that the aboveground parts of the seedlings only experienced a growth enhancement of 20%, but that the root biomass of the trees was increased by more than three times as much (62%).

Working with FACE technology, Pritchard et al. (2001b) studied 14-year-old loblolly pine trees after a year of exposure to an extra 200 ppm of CO2, finding that total root length and root numbers were 16 and 34% greater, respectively, in the CO2-enriched plots than in the ambient-air plots. In addition, the elevated CO2 increased the diameter of living and dead roots by 8% and 6%, respectively, while annual root production was found to be 26% greater in the CO2-enriched plots. And for the degree of CO2 enrichment used in the prior two studies, this latter enhancement corresponded to a root biomass increase of about 45%.

In an open-top chamber study of a model ecosystem composed of a mixture of spruce and beech seedlings, Wiemken et al. (2001) investigated the effects of a 200 ppm increase in the air's CO2 concentration that prevailed for a period of four years. On nutrient-poor soils, the extra CO2 led to a 30% increase in fine-root biomass, while on nutrient-rich soils it led to a 75% increase. As before, these numbers corresponded to increases of about 52% and 130%, respectively, for atmospheric CO2 enhancements on the order of those employed by Janssens et al. (1998) and Pritchard et al. (2001a).

Another interesting aspect of the Wiemken et al. study was their finding that the extra CO2 increased the amount of symbiotic fungal biomass associated with the trees' fine roots by 31% on nutrient-poor soils and by 100% on nutrient-rich soils, which for the degree of atmospheric CO2 enrichment used in the studies of Janssens et al. (1998) and Pritchard et al. (2001a) translate into increases of about 52% and 175%, respectively.

Jumping ahead four years, Tingey et al. (2005) studied the effects of atmospheric CO2 enrichment (to approximately 350 ppm above ambient) on the fine-root architecture of seedlings of Ponderosa pine (Pinus ponderosa) growing in open-top chambers at the U.S. Forest Service's Institute of Forest Genetics near Placerville, California (USA). This they did over a period of four years via the use of minirhizotron tubes; and in so doing, they found that elevated CO2 increased both fine root extensity (the degree of soil exploration) and intensity (the extent that roots use explored areas) but that it had no effect on mycorrhizae, the latter of which observations was presumed to be due to the fact that soil nitrogen was not limiting to growth in their study. More specifically, they report that "extensity increased 1.5- to 2-fold in elevated CO2 while intensity increased only 20% or less," noting that similar extensity results had been obtained over shorter periods of four months to two years by Arnon (1997), Berntson and Bazzaz (1998), DeLucia et al. (1997) and Runion et al. (1997), while similar intensity results had been obtained by Berntson (1994).

Shortly thereafter, Phillips et al. (2006) grew well-watered (via drip irrigation) 1.5-year-old ponderosa pine seedlings for four additional years in open-top chambers maintained at the ambient atmospheric CO2 concentration and at ambient + 175 ppm and ambient + 300 ppm CO2, while simultaneously imposing three levels of soil nitrogen (N) fertilization (0, 10 and 20 g N m^-2 year^-1) upon the plants. Every two months throughout this period, they collected video images of the roots that were visible on the surfaces of three minirhizotron tubes installed in each chamber; and from this information they learned that yearly values of fine-root standing crop, production and mortality were consistently higher in the elevated CO2 treatments throughout the study. They also report that "in this same study, Johnson et al. (2000) found that elevated CO2 increased fine-root life span," and because the elevated CO2 increased fine-root length, the amount of root length that died each year was greater in the CO2 enriched treatments. Therefore, as they describe it, "the higher rates of mortality in absolute terms for elevated CO2 are driven by increased standing crop and not reduced life spans."

The work of Phillips et al. additionally came to bear upon the progressive nitrogen limitation (PNL) hypothesis, wherein it has been thought by some that the benefits of atmospheric CO2 enrichment must ultimately dwindle away, since the productivity of earth's temperate forests is often limited by insufficient soil nitrogen, as is typically the case in the southeastern United States, where the growth of pine and hardwood forests can remove so much nitrogen from the soils on which the forests grow that it induces what Finzi and Schlesinger (2003) have described as "a state of acute nutrient deficiency that can only be reversed with fertilization." What Phillips et al. found, however, was that the increased fine-root length they observed "explains how additional N was provided to support the increased whole plant growth observed in [their] elevated CO2 treatments, and corresponds with the increased extent and intensity of the root system architecture discussed by Tingey et al. (2005)." This "mining of soil N," as they described it, "can in some cases go on for substantial lengths of time," and they stated there was "no evidence that PNL occurred during the course of [their] study," citing the work of Johnson et al. (2006).

Two years later, Pritchard et al. (2008) described what they had learned from minirhizotrons they had employed in work conducted at the Duke Forest FACE facility to characterize the influence of free-air-CO2-enrichment (ambient + 200 ppm) on fine roots for a period of six years (Autumn 1998 through Autumn 2004) in an 18-year-old loblolly pine (Pinus taeda) plantation near Durham, North Carolina, USA. Over a period of six years, they observed that the extra 200 ppm of CO2 increased average fine-root standing crop by 23%, which is right in line with the overall stimulation of forest net primary productivity of 18-24% they observed over the period 1996-2002. And in light of their finding that "the positive effects of CO2 enrichment on fine root growth persisted six years following minirhizotron tube installation (eight years following initiation of the CO2 fumigation)," there was again no hint of any progressive nitrogen limitation of the stimulatory effect of atmospheric CO2 enrichment in a situation where one might have been expected it to be encountered. In partial explanation of this important 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," and nearly all evidence obtained to date continues to suggest that earth's forests can indeed do so.

In a paper published the following year, Phllips et al. (2009) wrote that "O3 stress often decreases carbon allocation to roots, leading to reductions in root biomass and growth," citing Andersen (2003) and Grantz et al. (2006), while adding that "reduced carbohydrate stores in roots can lead to increased susceptibility to other stresses even after O3 exposure ends," citing Andersen et al. (1997), but stating, on the other hand, that CO2 tends to promote just the opposite behavior by promoting fine-root production and the benefits this phenomenon provides, citing Norby et al. (2004, 2005). Therefore, in an experiment designed to determine which of the two trace gases (CO2 or O3) has the greater impact on the growth and development of the fine roots of ponderosa pine trees, they grew Pinus ponderosa seedlings for three years in one-meter-deep containers filled with reconstructed pine-forest soil within sunlit controlled-environment chambers maintained at mean atmospheric CO2 concentrations of either 420 or 690 ppm, and at mean O3 conditions described by daily SUM06 index values of either 0 or 15.7 ppm h (representing the sum of hourly O3 concentrations >= 0.06 ppm), while images of fine roots growing along the upper surfaces of four minirhizotron tubes installed within each soil bin were collected every 28 days by a color video camera.

The result of this work, in the researchers' words, was that "elevated CO2 increased both the number of fine roots produced and their life span," and that "increased O3 did not reduce the effect of elevated CO2." Consequently, they found that fine root biomass at the end of the study in the CO2-enriched treatment was consistently higher in each soil horizon and 16% higher in total. In addition, the greater fine-root survivorship in the elevated CO2 treatment was associated with increasing root depth and increasing fine-root diameter, as has also been observed by Eissenstat et al. (2000), Gao et al. (2008) and Joslin et al. (2006). Last of all, they reported that averaged over the course of the experiment, there was a slight (3.3%) decrease in soil respiration in the elevated CO2 treatment, as observed by Tingey et al. (2006). Consequently, in the words of the four U.S. Environmental Protection Agency scientists who conducted the work, "elevated O3 did not result in significant negative impacts on ponderosa pine seedling fine-root survival ... or in countering the increased survivorship caused by elevated CO2," as the good gas won and the bad gas lost, in a proxy representation of the much greater biospheric battle that will be played out in the years and decades to come, as the concentrations of the two trace gases of the atmosphere continue rising in tandem.

In their introduction to the last study reviewed in this summary, Johansson et al. (2009) write that "ectomycorrhizal (ECM) fungi, forming the dominant type of symbiotic association with trees in boreal forests, receive as much as 25% of the total carbon assimilated by plants," and that, in return, "the extraradical fungal mycelium is directly involved in mobilization and uptake of nutrients which are, in part, passed on to the host plant." This important function is performed by the fungal exudation of a variety of low molecular weight organic compounds, polymer degrading enzymes, siderophores, polymeric carbohydrates and fatty acids, the dominant components of which -- low molecular weight organic acids, saccharides, amino acids and peptides -- "play important roles in enhancing mineral weathering, nutrient mobilization and uptake by plants." Hence, they investigated certain aspects of this complex suite of phenomena in seedlings of Scots pine (Pinus sylvestris) trees that were grown in the laboratory in liquid culture for a period of six weeks with either no ECM fungi or one of eight different such species associated with their roots, during which period they were exposed to air of either 350 or 700 ppm CO2, and after which period a number of analyses were performed to identify and quantify the variety of exudates produced by the fungi.

Johansson et al. say they observed "a clear impact of elevated CO2 on exudation of soluble low molecular weight organic compounds," and that these exudates "increased by 120-270%" due to "the increased carbon availability to the plant-fungus system," which was driven by the elevated atmospheric CO2 concentration that increased net CO2 assimilation rates by approximately 40% for both ECM and non-mycorrhizal seedlings, and which led to a mean increase of 27% in the total biomass production of the seedlings infected with the eight different species of ECM fungi, but which led to only a 14% increase in the biomass of the non-infected seedlings. Therefore, the four researchers concluded that the phenomena they observed "may contribute to nutritional feedback mechanisms to sustain tree growth when nutrients become limiting," such as some have hypothesized might occur over time in trees growing on low-fertility soils in CO2-enriched air (for much more on this subject, see Nitrogen (Progressive Limitation Hypothesis) in our Subject Index). The findings of this study, however, as well as those of the study of de Graaff et al. (2009) -- which was published in the same issue of Soil Biology & Biochemistry -- clearly indicate that earth's plants should be well equipped to deal with this hypothetical, and now largely discredited, roadblock to higher plant productivity in a CO2-enriched world of the future.

In brief summation, we note that the numerous results described above add to the growing body of evidence that suggests that the ongoing rise in the atmosphere's CO2 concentration will enable earth's conifers to continue to increase the volume of soil from which they can access water and nutrients, and that it will enable them to more thoroughly explore that enlarged volume of soil, both of which responses should allow them to acquire more of these essential resources and thereby realize the enhanced potential for growth that is provided them by the aerial fertilization effect of atmospheric CO2 enrichment. Clearly, therefore, the ongoing rise in the air's CO2 content bodes well for the growth of the planet's coniferous forests and for all of the creatures that depend upon them for food and shelter, as well as for the ability of the trees to provide lumber for mankind and to sequester carbon while doing so. These consequences have great virtue in and of themselves; and as the latter one provides a powerful negative feedback or brake on CO2-induced global warming, there is still another reason for lauding their existence.

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