These results represent a primarily positive response to atmospheric CO2 enrichment, although greater shoot protein concentrations would obviously have been desirable.  Nevertheless, the study's findings have been portrayed by various organizations, websites and publications as presaging significant negative consequences in the years and decades to come for almost all of earth's vegetation, including both agricultural crops and natural ecosystems.  Why?

One reason for the negativism may reside in the fact that the results obtained for the plants whose roots were bathed in the NH4⁺ solution were even more impressive.  Instead of "just" a 24% increase in leaf area in response to the 94% increase in the air's CO2 concentration, these plants exhibited a 49% increase; and instead of a "mere" 44% increase in total plant biomass, they exhibited a whopping 78% increase.  Also, whereas the plants whose roots were bathed in the NO3^- solution experienced a 13% decrease in shoot protein concentration, the plants whose roots were bathed in the NH4⁺ solution experienced a shoot protein concentration decline of only 6%.

Thus it was that on 4 February 2002 - one day before the Bloom et al. paper even appeared in print - NASA's Earth Observatory News posted an article on its website entitled High CO2 Levels Hamper Nitrate Incorporation by Plants, in which it was claimed that "nitrate fertilizer is not nearly as efficient as ammonium fertilizer when atmospheric carbon dioxide levels are unusually high," which is quite an expansive conclusion to draw from a study that lasted only two weeks, dealt with only one species, and utilized only seedlings growing only in nutrient solution.

This report was followed by several similar stories of much the same negative bent. Scientific American introduced their take on the Bloom et al. paper with an equally expansive title stating Rising CO2 Levels Could Force Shift in Fertilizer Use, which document was reproduced the very same day by the Climate Ark organization.  Simultaneously, AmeriScan displayed an article entitled Rising CO2 Hampers Fertilizers, which began with the declaration that "as carbon dioxide levels rise, plant life around the globe may lose the ability to incorporate certain forms of nitrogen, like those found in most fertilizers."  And it ended with the statement that "as atmospheric CO2 levels continue to rise, nitrate-sensitive plant and tree species in the wild could be at a competitive disadvantage," stating that "this could change the distribution of plants in natural ecosystems."

Some of the press reports also said that "for many years, scientists believed ... rising levels of carbon dioxide would actually benefit plants," as if to suggest that such was no longer the case.  They also matter-of-factly stated that the typically-observed initial positive growth response to atmospheric CO2 enrichment observed in most experiments "wasn't sustained," dropping back to just a few percent above normal "within a few days or weeks."

It is interesting to note, in this regard, that the environmental press so highly hyped so many purported, long-term, real-world, global ramifications of the Bloom et al. study (all negative, of course) for both agricultural and natural ecosystems, when the experiment upon which these projections were based was so short (only 14 days long) and had been performed under sterile laboratory conditions that included no soil, no competing plants, and a totally unnatural mix of antibiotics in the water surrounding the seedlings' roots, which was introduced to suppress naturally-occurring nitrogen-transforming processes that Bloom et al. note are "rapid in nonsterile cultures (Padgett and Leonard, 1993) and sensitive to atmospheric CO2 (Smart et al., 1997)," both of which situations - nonsterile conditions and rising atmospheric CO2 concentrations - are typical of the present real world of nature. Clearly, this study was not a microcosm of the real world.  In fact, it was far, far from it.

So what do we learn from longer experiments that have been conducted under more realistic conditions?  We first consider the three-part claim - which, to be fair to the press, was actually made by Bloom et al. - that (1) "a doubling of CO2 level initially accelerates carbon fixation in C3 plants by about 30%," that (2) this growth stimulation "after days to weeks" dramatically declines, and that (3) the CO2-induced growth enhancement thereafter "stabilizes at a rate that averages 12% above ambient controls."

All three parts of this unfortunate claim are grossly inaccurate generalizations of what is often called acclimation to CO2 enrichment.  A doubling of the air's CO2 content will often accelerate biomass production in young C3 plants in the early stages of CO2 enrichment by much more than 30%.  Even in their own experiment, Bloom et al. report that slightly less than a doubling of the air's CO2 content increased the biomass of their NO3^--treated plants by fully 44%, and that it increased the biomass of their NH4⁺-treated plants by what we have rightly called a whopping 78%.  In addition, the review-analysis of Idso (1999) includes at least twenty experiments where the initial growth stimulation exceeds 100%.

With respect to the declining growth stimulation purported to follow the initial CO2-induced growth spurt, sometimes it never occurs (Gunderson et al., 1993; Fernandez et al., 1998; Garcia et al., 1998).  In other instances, the reverse occurs; and the CO2-induced growth stimulation increases over time (Arp and Drake, 1991; Vogel and Curtis, 1995; Jacob et al., 1995).  And in those cases where there is a decline in the CO2 aerial fertilization effect, it sometimes does not begin until one to two years after the initiation of the experiment (Idso, 1999).

Finally, the degree of CO2-induced growth stimulation at which the aerial fertilization effect of atmospheric CO2 enrichment eventually stabilizes is often significantly larger than the 12% value suggested by Bloom et al. for a doubling of the air's CO2 content.  In the still-ongoing long-term sour orange tree study of Idso and Kimball (2001), for example, a smaller 75% increase in the air's CO2 content has ultimately led to a stabilized CO2-induced growth enhancement of fully 80% (down from a peak value in excess of 200% experienced at the 2.5-year point of the study), which has been maintained for the past five years.

Having thus clarified the record with respect to the erroneously-summarized aspects of the CO2 acclimation phenomenon in the Bloom et al. article, we turn our attention to their conclusion that plants respond better to atmospheric CO2 enrichment when they obtain their nitrogen in the ammonium form as opposed to the nitrate form; for in spite of their claim that theirs "may be the first study to examine CO2 responses under controlled levels of NH4⁺ vs. NO3^- as sole N sources," there are many other studies that provide important information about this topic.  And they do not all tell the same story.

Bauer and Berntson (2001) grew seedlings of Betula alleghanienis and Pinus strobus for 15 weeks - as opposed to the abbreviated 2 weeks of the Bloom et al. experiment - in growth chambers maintained at atmospheric CO2 concentrations of 400 and 800 ppm, while the seedlings' roots were suspended in nutrient solutions whose sole sources of N were, as in the study of Bloom et al., either NO3^- or NH4⁺.  In this experiment, the extra CO2 did not have any effect on the growth of the Pinus species in either solution; but it increased total seedling dry weight in the Betula species by 61% in the nitrate treatment and by 79% in the ammonium treatment.  Although this result is qualitatively the same as that obtained by Bloom et al., the ammonium/nitrate (A/N) response ratio, i.e., 79%/61% = 1.30, was much lower than the A/N ratio of the Bloom et al. experiment, i.e., 78%/44% = 1.77, suggesting that perhaps the A/N ratio could be undergoing a type of acclimation as experimental duration lengthens, thereby holding out the possibility that for still longer (and more realistic) periods of differential CO2 exposure, there may well be no plant preference at all with regard to N source.

Van der Merwe and Cramer (2000) grew tomato (Lycopersicon esculentum) seedlings for two weeks - bringing them to the same mean age as the wheat plants studied by Bloom et al. - in air of 360 ppm CO2, while the roots of the seedlings were enclosed in sealed vessels containing either NO3^- or NH4⁺ solutions, after which the solutions were equilibrated with air as high in CO2 concentration as 20,000 ppm.  This rhizospheric CO2 enrichment had no effect on the uptake of NH4⁺ by the tomato seedlings; but it resulted in an enhanced uptake of NO3^-, with the maximum effect occurring at a rhizospheric CO2 concentration of 5,000 ppm, which is to be compared to a normal root-zone CO2 concentration of something less than 5,000 ppm but more than 1,000 ppm, as is typical of soil airspace in most outdoor environments.  Although we cannot be confident about all the possible implications of this observation, it does indicate a preferential plant uptake of nitrate N at higher-than-normal rhizospheric CO2 concentrations, which is hard to understand if plants are supposed to prefer ammonium N at high CO2 concentrations, as suggested by the work of Bloom et al.

We additionally note, at this point, that attempting to discern and characterize a possible CO2-mediated plant preference for a particular form of nitrogen must involve considerably more complex investigations than simple laboratory experiments with individual plants whose roots have never been exposed to anything other than sterile nutrient solutions.  Actual nonsterile soils are required to host the plants we study, if we are ever going to learn how plants operate in this regard in the real world of nature.  Hence, we ease into this realm of investigation with a brief review of an intermediate sort of study conducted by Constable et al. (2001), who although not using totally natural soil at least got beyond the hydroponic stage of investigation for the major portion of their experiment and also dealt with the added complexity supplied by the presence of two types of fungal symbionts, which often live in close association with the roots of plants in their normal habitats and serve as a living link between them and the soil environment.

Constable et al. studied mycorrhizal- and non-mycorrhizal-infected seedlings of both sweetgum (Liquidambar styraciflua) and loblolly pine (Pinus taeda) that were rooted in pots filled with fine sand above a layer of mycorrhizal inoculum, or clay lacking such inoculum, and grown for six months out-of-doors in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm.  At the conclusion of this stage of their investigation, they brought the seedlings into the laboratory, washed the sand from their roots and from the fungal hyphae associated with the roots of half of the plants, and placed the roots and root/hyphae systems in hydroponic solutions of NO3^- and NH4⁺ for N uptake evaluations that were conducted within controlled environment chambers that were maintained at the same atmospheric CO2 concentrations to which the seedlings had been exposed while growing out-of-doors.

In this part of the experiment, both tree species exhibited a greater preference for NH4⁺ than for NO3^-, regardless of mycorrhizal treatment, as is commonly reported for trees exposed to normal atmospheric CO2 concentrations (Gessler et al., 1998; Wallenda and Read, 1999).  Nevertheless, the presence of mycorrhizae improved nitrogen acquisition in both species at both CO2 concentrations; and, as the authors reported, "this increase in uptake capacity was preferentially for NO3^- as opposed to NH4⁺."  Furthermore, they noted that "in loblolly pine, the relative enhancement of NO3^- uptake capacity by EM [ectomycorrhizal] fungi was significantly higher at elevated CO2 compared with ambient CO2," in direct opposition to what would be expected on the basis of the Bloom et al. experiment.  In sweetgum, on the other hand, the reverse was true; and the authors thus urged caution in concluding too much from observations derived from too few species of both plants and mycorrhizae - a caution, we might add, that seems to have not occurred to either Bloom et al. or the members of the press who wrote so confidently about the global applicability of the results of their wheat experiment.

In a still more realistic set of experiments, BassiriRad et al. (1999) grew two tree species - red maple (Acer rubrum) and sugar maple (Acer saccharum) - for nearly 1.5 years out-of-doors in open-top chambers (OTCs) maintained at atmospheric CO2 concentrations of ambient and ambient plus 300 ppm, as well as two crop species - soybean (Glycine max) and sorghum (Sorghum bicolor) - that were studied for one full growing season in OTCs maintained at atmospheric CO2 concentrations of ambient and ambient plus 360 ppm.  The trees were planted directly into the natural soil upon which the OTCs of their experiment were constructed; while the crops were planted in natural soil that filled a 2-meter-deep bin, measuring 6 meters wide and 76 meters long, upon which the OTCs of their experiment were constructed.

In both sets of experiments, small groups of fine roots were carefully exposed, cleaned, and inserted and subsequently sealed into tubes containing known volumes of 25, 50, 75, 100, 150 and 200 µM solutions of NH4NO3, after which the roots were allowed to take up whatever amounts of each form of N they preferred over periods of 30 to 60 minutes. The roots were then removed from the tubes and the portions that had been immersed in the nutrient solution excised, dried and weighed; while the volume of the remaining solution in each tube was noted and stored for later assessment of the amounts of NH4⁺ and NO3^- that had not been removed by the roots.

The results of these experiments indicated that all four species exhibited a distinct preference for NH4⁺ uptake over NO3^- uptake when grown in air of normal atmospheric CO2 concentration; but this preference was only to be expected, because the energy requirements associated with the uptake and assimilation of NO3^- are considerably greater than those associated with the uptake and assimilation of NH4⁺, as demonstrated by the work of Haynes and Goh (1978), Blacquiere (1987), and Glass and Siddiqi (1995).  Also noted by BassiriRad et al. in this regard is the fact that "the greater preference for NH4⁺ vs. NO3^- is almost a universal root characteristic in tree species and is often associated with an adaptation to forest soils that are relatively low in NO3^-."

So what happened with the plants in the CO2-enriched chambers?  Red maple did indeed exhibit a slight enhancement of its ambient-air preference for NH4⁺.  The other three species, however, showed no change in N preference at the higher CO2 concentration.  Hence, one of the four species studied provided weak support for the hypothesis of the Bloom et al. study; but the other three species provided no support.

So where does all this leave us?  For one thing, the body of literature we have discussed indicates that different species may well behave differently with respect to the effects of atmospheric CO2 enrichment on plant N uptake kinetics.  In a similar assessment of the issue, BassiriRad et al. additionally note that "using potted seedlings we have shown elsewhere (BassiriRad et al., 1997a, b) that high CO2 increased, decreased or had no significant effect on NO3^- uptake kinetics depending upon species tested," much as we have found to be the case in our brief review of the subject.  They also state that "in a hydroponic experiment using soybean and sunflower, we observed that root N uptake kinetics response to CO2 enrichment was highly dependent on the stages of development and root age."  Hence, they say that "a 'one point in time' determination" - such as that which comprised the study of Bloom et al. - "is not adequate and more measurements of root N uptake kinetics are necessary to draw valid conclusions about possible effects of CO2."

We couldn't agree more.  The Bloom et al. experiment in no way justifies any of the mountainous biospheric problems they and the environmental press have attempted to erect out of the results of their severely-restricted study.  We've got to get real.  Nature is complex.  Although laboratory experiments have an important role to play in attempting to determine the likely biological consequences of the ongoing rise in the air's CO2 content, they cannot capture anywhere near the totality of everything of significance to the subject that occurs in the world beyond the laboratory door.  To do that, we must step outside and drink deeply of the world of nature ... or drink not at all.

References
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