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Nitrogen (Progressive Limitation Hypothesis - Miscellaneous) -- Summary
The progressive nitrogen limitation or PNL hypothesis - which contends that low concentrations of soil nitrogen will gradually reduce the growth-promoting strength of the aerial fertilization effect of atmospheric CO2 enrichment - has its origins in the writings of Hungate et al. (2003) and Luo et al. (2004). Interestingly, however, the first of these two papers contains considerable evidence that argues against its own authors' contentions, as does a subsequent publication (Luo et al., 2006) whose senior author was also the senior author of the second paper.

Hungate et al. (2003), for example, reported that the C:N ratio of tree biomass increases with increases in the air's CO2 concentration, citing the work of Hungate (1999) and Rastetter et al. (1992). This fact indicates that ever more carbon can be stored in tree tissues per unit of nitrogen stored therein as the air's CO2 content continues to rise; and Hungate and his coauthors went on to state that "soil C:N could also increase with rising atmospheric CO2 concentration, allowing soil carbon accumulation without additional nitrogen."

Lou et al. (2006) conducted a meta-analysis of various C and N processes in plants and soils in response to atmospheric CO2 enrichment based on experimentally-derived data contained in 104 scientific publications. This work revealed that in response to atmospheric CO2 enrichment, the carbon and nitrogen contents in all the plant and soil pools studied significantly increased, "leading to more net C and N accumulations in ecosystems at elevated than ambient CO2." More specifically, they found that the mean CO2-induced increases in C pools of shoot, root, whole plant, litter and soil were 22.4%, 31.6%, 23.0%, 20.6% and 5.6%, respectively, while the corresponding CO2-induced increases in N pools were 4.6%, 10.0%, 10.2%, 25.4% and 11.2%. In addition, they reported that "N accumulations in ecosystems have long been documented in association with C accumulations during both primary and secondary successions (Crocker and Major, 1955; Binkley et al., 2000; Vitousek, 2004)." And as a result, they concluded that "the net C and N accumulations revealed in this study," which were produced by atmospheric CO2 enrichment, "together with studies of C and N dynamics during succession over hundreds to millions of years, suggest that ecosystems may have intrinsic capabilities to stimulate N accumulation by C input," which latter phenomenon is typically increased by atmospheric CO2 enrichment. They further concluded that "net N accumulation likely supports long-term C sequestration in response to rising atmospheric CO2 concentration." And last of all, to underscore this point, they stated that "concomitant increases in C and N contents in plant and soil pools at elevated CO2 as shown in this study point toward a long-term trend of terrestrial C sequestration in response to rising atmospheric CO2 concentration," which is just the opposite of what is predicted by the PNL hypothesis.

Norby and Iverson (2006) reviewed what they learned about the PNL hypothesis from "a six-year record of N dynamics of a sweetgum (Liquidambar styraciflua) stand exposed to elevated CO2 in the free-air CO2 enrichment (FACE) experiment at Oak Ridge, Tennessee, USA," focusing on N uptake, content, distribution, turnover, and N-use efficiency. As they describe it, "net primary productivity in this stand has been significantly higher in CO2-enriched plots, and the response has been sustained through time, thereby meeting one of the criteria for the development of PNL." However, as they reported, "none of the measured responses of plant N dynamics in this ecosystem indicated the occurrence of PNL."

Hungate et al. (2006) tested the PNL hypothesis against what they observed over a period of seven years in an open-top chamber study of a scrub oak woodland dominated by Quercus myrtifolia, Q. geminata and Q. chapmanii on an island enclosed within the borders of NASA's Kennedy Space Center on the coast of central Florida, USA, which test commenced just a few months after a complete burning of the ecosystem that is located on well-drained nutrient-poor soil. They reported finding that "litterfall production (one measure of aboveground primary productivity) increased initially in response to elevated CO2, but the CO2 stimulation declined during years five through seven, concurrent with the accumulation of N in the O [soil] horizon and the apparent restriction of plant N availability." These changes in N cycling were said by them to be "likely to reduce the response of plant production to elevated CO2." Yet, as they were forced to acknowledge, "at the level of aboveground plant biomass (estimated by allometry), progressive N limitation was less apparent." In fact, there was a persistent CO2-induced increase in aboveground plant carbon, which led them to conclude that "some mechanisms are partially alleviating progressive N limitation," just as was concluded by Finzi et al. (2006) in their study of loblolly pines, where by some unknown means the pines obtained the extra nitrogen they needed to thwart the negative consequences predicted by the PNL hypothesis.

It is interesting to note, in this regard, that a large initial CO2-induced increase in aboveground biomass production, followed by a rapid but slowing decline in this parameter, was also observed by Idso and Kimball (2001) in their long-term sour orange tree study. And because the trees of their experiment were periodically fertilized so as to never lack for nitrogen, the similar productivity vs. time pattern observed by Hungate et al. may well have had nothing to do with "restriction of plant N availability," which they characterized as being merely "apparent." It is also important to note that the slow decline in the CO2-induced growth stimulation of the sour orange trees finally came to a halt at the ten-year point of the experiment, when the declining growth stimulation finally leveled out at an essentially constant value that was maintained to the end of the 17-year study: a 69% increase in yearly total biomass production in response to a 75% increase in the air's CO2 content (Kimball et al., 2007). Consequently, as was found to be the case in the studies of Norby and Iverson (2006) and Finzi et al. (2006), the pattern of CO2-induced growth stimulation in the scrub oak ecosystem studied by Hungate et al. provides no evidence for the PNL hypothesis. In fact, it and other of their observations point to one or more unknown means of ecosystem N acquisition that allow the aerial fertilization effect of atmospheric CO2 enrichment to just keep chugging along (albeit at a somewhat lower level of impact than that of its peak manifestation), even in the face of "apparent" N limitations.

Johnson et al. (2006) studied the effects of elevated CO2 (ambient, +175, +350 ppm) and N fertilization (unfertilized, +100, +200 kg N ha-1 yr-1, provided as ammonium sulfate) on C and N accumulations in the biomass of ponderosa pines (Pinus ponderosa Laws, grown from seed) and the soils that supported them in a six-year open-top chamber experiment conducted near Placerville, California, USA. This study, like several others, according to Johnson et al., "showed that growth response to elevated CO2 more than offset declines in tissue N concentrations, necessitating increased N uptake by trees," which led them to ask: "How did the trees manage to obtain this 'extra' N in an N-limited environment?"

In the fertilized treatments, the four researchers say the extra N could readily have been supplied by the added fertilizer; but in the unfertilized treatments they opined that a substantial amount of the N uptake "probably came from the soil," as both wet and dry deposition were not great enough to have supplied all of the extra N and "no symbiotic N fixer was present in the study plots." Citing a number of other investigators' results as supplying circumstantial evidence for what they finally concluded, they decided that "the additional N needed to respond to elevated CO2 came from the soil and was facilitated by greater root exploration under elevated CO2." Acknowledging that they could not "provide an accurate prediction from the results of this study," Johnson et al. nevertheless stated that they could "see no evidence that either growth or additional N uptake at the +350 ppm CO2 level are being inhibited by PNL as of year 6 in this study."

Studying the same trees, Phillips et al. (2006) collected video images every two months of roots growing against the surfaces of three minirhizotron tubes installed in each chamber. This work revealed that yearly values of fine-root standing crop, production and mortality were consistently higher in the elevated CO2 treatments throughout the study; and they reported that "in this same study, Johnson et al. (2000) found that elevated CO2 increased fine-root life span." However, because elevated CO2 also increased fine-root length, they found that "the amount of root length dying per year was actually greater." 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." In addition, they say that Tingey et al. (2005) found that "in the elevated CO2 treatments, fine roots explored the soil more extensively and deeper, and filled in the explored areas more intensively." With respect to the PNL hypothesis, therefore, Phillips et al. stated that "the increased fine-root length reported here explains how additional N was provided to support the increased whole plant growth in elevated CO2 treatments, and corresponds with the increased extent and intensity of the root system architecture discussed by Tingey et al. (2005)." And this "mining of soil N," as they continued, "can in some cases go on for substantial lengths of time, and there is no evidence that PNL occurred during the course of this study."

Changing gears just a bit, Barnard et al. (2006) injected 15N-labelled NH4 into the soil of mesocosms of Holcus lanatus (L.) that had been grown for over 15 months at either ambient or elevated atmospheric CO2 concentrations, in order to determine whether the uptake capacity of soil micro-organisms had remained higher at elevated CO2, and to shed further light on the short-term (48 hours) partitioning of N between plants and soil micro-organisms. In doing so, they found that their results and data from other plant-microbial 15N partitioning experiments at elevated CO2 suggested that "the mechanisms controlling the effects of CO2 on short- vs. long-term N uptake and turnover differ." More importantly, they determined that "short-term immobilization of added N by soil micro-organisms at elevated CO2 does not appear to lead to long-term increases in N in soil microbial biomass," noting that the increased soil microbial C:N ratios that they observed at elevated CO2 "suggest that long-term exposure to CO2 alters either the functioning or structure of these microbial communities." As a result, Barnard et al. concluded that "short-term immobilization of inorganic soil nitrogen or exploitation of nutrient pulses may be altered under conditions of elevated atmospheric CO2 concentration," and that this alteration is such that it takes most of the wind out of the sails of the PNL hypothesis, likely allowing long-lived plants and ecosystems to maintain positive growth responses to atmospheric CO2 enrichment for as long as the enrichment continues.

Noting that the photosynthetic down-regulation posited by the PNL hypothesis "may occur in ecosystems that have a low soil N availability, such as piedomont loblolly pine forests" - which is the type of setting in which the long-term Duke Forest FACE study was being conducted - Springer and Thomas (2007) set out to test the validity of the PNL hypothesis on some of the site's understory tree species, initially assuming it would be proven to be correct. As they describe it, they "hypothesized that after seven years of exposure to elevated CO2, significant photosynthetic down-regulation would be observed in these tree species," which included red maple (Acer rubrum L.), hickory (Carya glabra Mill.), redbud (Cercis canadensis L.) and sweetgum (Liquidambar styraciflua L.).

During the first year of the Duke Forest FACE experiment, DeLucia and Thomas (2000) had examined the photosynthetic responses of these particular saplings to the 200-ppm increase in atmospheric CO2 concentration employed in that study. Consequently, Springer and Thomas "reexamined the photosynthetic responses of saplings of the same four understory species to determine whether the enhancement of photosynthesis observed during the first year of exposure to elevated CO2 was sustained in the seventh year of the experiment." This work provided, in their words, "no evidence of photosynthetic down-regulation in any species in either early or late summer." In fact, not only did their measurements not reveal any down-regulation of photosynthesis, they actually observed "a small increase in the photosynthetic capacity of all of the study species in response to elevated CO2," such as they say "has been demonstrated in several studies (Campbell et al., 1988; Ziska and Teramura, 1992; Idso et al., 1991)."

In summing up the situation, Springer and Thomas once again stated, in the opening sentence of the concluding paragraph of their paper, that "the progressive N limitation hypothesis predicts a diminished response of plant productivity to elevated CO2 as N availability decreases because of the increased nutrient demands of greater plant biomass production (Luo et al., 2004)," and in the final sentence of that paragraph, they reiterate that "after seven years of elevated CO2 treatment in the Duke Forest FACE experiment, we see little evidence of progressive N limitation in the leaf level processes of these four species of understory trees." In fact, they found evidence of just the opposite response.

Working at the EUROFACE facility in central Italy near Viterbo, Liberloo et al. (2007) grew three different species of poplar trees - robusta poplar (Populus x euramericana), white poplar (P. alba) and black poplar (P. nigra) - for two three-year periods, between which times the trees were coppiced and allowed to re-grow, in either ambient air or air enriched with an extra 180 ppm of CO2 (an approximate 49% enhancement). No fertilization was applied to any of the plots over the first growth cycle, while half of the trees were fertilized over the second growth cycle. Then, during the last year of the last cycle, a number of plant processes and parameters were measured and compared with similar observations made throughout earlier years of the experiment.

The five researchers report that after six years of growth under elevated atmospheric CO2, the poplar trees did not experience any down-regulation of leaf net photosynthesis; and the long-term stimulation they observed was huge. In response to the 49% increase in the atmosphere's CO2 concentration, the CO2-induced stimulation of net photosynthesis, averaged over the three species, was also 49%. In addition, they report there was no difference in CO2-induced net photosynthetic stimulation between sun and shade leaves, nor was there any difference in CO2 effects between the fertilized and non-fertilized trees.

After thus finding that the "photosynthetic stimulation of poplar leaves was sustained in elevated CO2 after six years of fumigation, even under non-fertilized conditions," Liberloo et al. concluded that "these results give optimistic perspectives for the future, as the maintained enhancement of photosynthesis in poplar trees is likely to continue over several rotations, thereby providing more carbon for growth in a closed canopy forest."

In an important review paper, Finzi et al. (2007) evaluated the PNL hypothesis based on data obtained from four well-known FACE experiments conducted on forests - the Rhinelander, Duke and Oak Ridge National Laboratory (ORNL) studies in the United States, and the POP-EUROFACE study in Europe - where previous research described by Norby et al. (2005) showed that net primary production (NPP) increased by 23 2% in response to a CO2 concentration increase of 174 ppm (46%) above the mean ambient-air concentration.

The CO2-induced increase in forest productivity at the POP-EUROFACE site, which Finzi et al. say was "located on former agricultural land where soil nitrogen availability was high and not limiting," was found by them to not have been supported by greater nitrogen uptake from the soil, but by an increase in nitrogen use efficiency (NUE). At the other three sites, however, the CO2-induced increase in forest productivity was supported by greater N uptake from the soil, with no change in NUE; and they note that this result was "unexpected," especially for the Duke and ORNL sites, where they say that "tree growth is demonstrably N-limited."

Focusing on the findings of the three U.S. studies, Finzi et al. state that "the response of N uptake and NUE in these young temperate forests exposed to FACE is the opposite of that predicted by the current generation of biogeochemical models," i.e., those that are based upon the PNL hypothesis; and after discussing some possible ways by which these forests might be obtaining the seemingly-impossible-to-obtain nitrogen that they need to maintain their significantly-CO2-enhanced growth rates, they conclude by stating that "regardless of the specific mechanism, this analysis demonstrates that larger quantities of carbon entering the below-ground system under elevated CO2 result in greater N uptake, even in N-limited ecosystems."

In another study published in 2007, Zak et al. initiated a year-long ecosystem-level 15N tracer experiment at the Rhinelander, Wisconsin (USA) FACE facility at the seven-year point of a long-term study of aspen (Populus tremuloides) and aspen-birch (P. tremuloides-Betula papyrifera) communities exposed to factorial treatments of CO2 (ambient and elevated to 200 ppm above ambient) and O3 (ambient and elevated to 30-40 ppb above ambient). One year after adding tracer amounts of 15NH4+ to the forest floor of the young tree stands, they determined that "both forest communities exposed to elevated CO2 obtained greater amounts of 15N (29%) and N (40%) from soil, despite no change in soil N availability or plant N-use efficiency," which they attributed to greater belowground root growth and a more thorough exploration of the soil for growth-limiting nitrogen in the CO2-enriched treatment. In contrast, they found that the elevated O3 treatment "decreased the amount of 15N (-15%) and N (-29%) in both communities." These decreases, however, were significantly smaller than the corresponding CO2-induced increases. Consequently, Zak et al. concluded that "progressive nitrogen limitation is presently not a factor governing plant growth response to elevated CO2 in these young, developing forest communities." In addition, they stated that their findings "are consistent with those in young sweet gum (Liquidambar styraciflua) and loblolly pine (Pinus taeda) forests exposed to elevated CO2 (Finzi et al., 2006; Norby and Iversen, 2006)."

Most recently, Langley et al. (2009) "employed 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," which work was conducted at the multiple open-top-chamber facility at NASA's Kennedy Space Center. In doing so, they learned that elevated atmospheric CO2 (to 350 ppm above ambient concentrations) tended to increase net N mineralization in the top 10 cm of the soil, but that it also decreased total soil organic carbon content there by 21%. However, that loss of carbon mass was only equivalent to "roughly one-third of the increase in plant biomass that occurred in the same experiment." In addition, they state that the strongest increases in net N mineralization were observed in the 10-30 cm depth increment, and that "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%." Once again, therefore, yet another experiment demonstrates that atmospheric CO2 enrichment generally enables plants to find the extra nitrogen they need to take full advantage of the aerial fertilization effect of elevated atmospheric CO2 concentrations, with the result that total ecosystem carbon content is increased, resulting in a negative feedback to anthropogenic CO2 emissions.

In conclusion, although the PNL hypothesis sounds logical enough - and many scientists initially embraced it as fact - a vast array of observational data has subsequently proven it to be fiction.

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Binkley, D., Son, Y. and Valentine, D.W. 2000. Do forests receive occult inputs of nitrogen? Ecosystems 3: 321-331.

Campbell, W.J., Allen, L.H. and Bowes, G. 1988. Effects of CO2 concentration on rubisco activity, amount, and photosynthesis in soybean leaves. Plant Physiology 88: 1310-1316.

Crocker, R.L. and Major, J. 1955. Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. Journal of Ecology 43: 427-448.

DeLucia, E.H. and Thomas, R.B. 2000. Photosynthetic responses to CO2 enrichment of four hardwood species in a forest understory. Oecologia 122: 11-19.

Finzi, A.C., Moore, D.J.P., DeLucia, E.H., Lichter, J., Hofmockel, K.S., Jackson, R.B., Kim, H.-S., Matamala, R., McCarthy, H.R., Oren, R., Pippen, J.S. and Schlesinger, W.H. 2006. Progressive nitrogen limitation of ecosystem processes under elevated CO2 in a warm-temperate forest. Ecology 87: 15-25.

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.

Hungate, B.A. 1999. Ecosystem responses to rising atmospheric CO2: Feedbacks through the nitrogen cycle. In: Luo, Y. and Mooney, H. (Eds.), Carbon Dioxide and Environmental Stress. Academic Press, San Diego, CA, USA., pp. 265-285.

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.

Idso, S.B. and Kimball, B.A. 2001. CO2 enrichment of sour orange trees: 13 years and counting. Environmental and Experimental Botany 46: 147-153.

Idso, S.B., Kimball, B.A. and Allen, S.G. 1991. CO2 enrichment of sour orange trees: 2.5 years into a long-term experiment. Plant, Cell and Environment 14: 351-353.

Johnson, D.W., Hoylman, A.M., Ball, J.T. and Walker, R.F. 2006. Ponderosa pine responses to elevated CO2 and nitrogen fertilization. Biogeochemistry 77: 157-175.

Johnson, M.G., Phillips, D.L., Tingey, D.T. and Storm, M.J. 2000. Effects of elevated CO2, N-fertilization, and season on survival of ponderosa pine fine roots. Canadian Journal of Forest Research 30: 220-228.

Kimball, B.A., Idso, S.B., Johnson, S. and Rillig, M.C. 2007. Seventeen years of carbon dioxide enrichment of sour orange trees: final results. Global Change Biology 13: 2171-2183.

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., 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., Hui, D. and Zhang, D. 2006. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: A meta-analysis. Ecology 87: 53-63.

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.

Norby, R.J., DeLucia, E.H., Gielen, B., Calfapietra, C., Giardina, C.P., King, S.J., Ledford, J., McCarthy, H.R., Moore, D.J.P., Ceulemans, R., De Angelis, P., Finzi, A.C., Karnosky, D.F., Kubiske, M.E., Lukac, M., Pregitzer, K.S., Scarasci-Mugnozza, G.E., Schlesinger, W.H. and Oren, R. 2005. Forest response to elevated CO2 is conserved across a broad range of productivity. Proceedings of the National Academy of Sciences 102: 10.1073/pnas.0509478102.

Norby, R.J. and Iversen, C.M. 2006. Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87: 5-14.

Phillips, D.L., Johnson, M.G., Tingey, D.T., Storm, M.J., Ball, J.T. and Johnson, D.W. 2006. CO2 and N-fertilization effects on fine-root length, production, and mortality: a 4-year ponderosa pine study. Oecologia 148: 517-525.

Rastetter, E. B., McKane, R. B., Shaver, G. R., Melillo, J. M., Nadelhoffer, K. J., Bobbie, J. E. and Aber, J. D. 1992. Changes in C storage by terrestrial ecosystems: how C-N interactions restrict responses to CO2 and temperature. Water, Air and Soil Pollution 64: 327-344.

Springer, C.J. and Thomas, R.B. 2007. Photosynthetic responses of forest understory tree species to long-term exposure to elevated carbon dioxide concentration at the Duke Forest FACE experiment. Tree Physiology 27: 25-32.

Tingey, D.T., Johnson, M.G. and Phillips, D.L. 2005. Independent and contrasting effects of elevated CO2 and N-fertilization of root architecture in Pinus ponderosa. Trees 19: 43-50.

Vitousek, P.M. 2004. Nutrient Cycling and Limitation: Hawaii as a Model System. Princeton University Press, Princeton, New Jersey, USA.

Zak, D.R., Holmes, W.E. and Pregitzer, K.S. 2007. Atmospheric CO2 and O3 alter the flow of 15N in developing forest ecosystems. Ecology 88: 2630-2639.

Ziska, L.H. and Teramura, A.H. 1992. Intraspecific variation in the response of rice (Oryza sativa) to increased CO2 concentration - photosynthetic, biomass, and reproductive characteristics. Physiologia Plantarum 84: 269-274.

Last updated 5 August 2009