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  Elevated Atmospheric CO2 Concentrations Enhance Health-Promoting Properties of Foods

Antioxidants are of great importance to human health.  In some cases, the additional carbon fixed by plants during CO2-enrichment is invested in antioxidative compounds; and one of the most prominent of these products is ascorbate or vitamin C.  In the early studies of Barbale (1970) and Madsen (1971, 1975), a tripling of the atmospheric CO2 concentration produced a modest (7%) increase in this antioxidant in the fruit of tomato plants.  Kimball and Mitchell (1981), however, could find no effect of a similar CO2 increase on the same species, although the extra CO2 of their study stimulated the production of vitamin A.  In bean sprouts, on the other hand, a mere one-hour-per-day doubling of the atmospheric CO2 concentration actually doubled plant vitamin C contents over a 7-day period (Tajiri, 1985).

Probably the most comprehensive investigation of CO2 effects on vitamin C production in an agricultural plant -- a tree crop (sour orange) -- was conducted by Idso et al. (2002), where a 75% increase in the air's CO2 content was observed to increase sour orange juice vitamin C concentration by approximately 5% in run-of-the-mill years when total fruit production was typically enhanced by about 80%.  In aberrant years when the CO2-induced increase in fruit production was much greater, however, the increase in fruit vitamin C concentration was also greater, rising to a CO2-induced enhancement of 15% when fruit production on the CO2-enriched trees was 3.6 times greater than it was on the ambient-treatment trees.

These findings take on great significance when it is realized that scurvy -- which is induced by low intake of vitamin C -- may be resurgent in industrial countries, especially among children (Ramar et al., 1993; Gomez-Carrasco et al., 1994), and that subclinical scurvy symptoms are increasing among adults (Dickinson et al., 1994).  Furthermore, Hampl et al. (1999) have found that 12-20% of 12- to 18-year-old school children in the United States "drastically under-consume" foods that supply vitamin C; while Johnston et al. (1998) have determined that 12-16% of U.S. college students have marginal plasma concentrations of vitamin C.  Hence, since vitamin C intake correlates strongly with the consumption of citrus juice (Dennison et al., 1998), and since the only high-vitamin-C juice consumed in any quantity by children is orange juice (Hampl et al., 1999), the modest role played by the ongoing rise in the air's CO2 content in increasing the vitamin C concentration of orange juice could ultimately prove to be of considerable significance for public health in the United States and elsewhere.

Another important study to assess the impact of elevated levels of atmospheric CO2 on plant antioxidant production was that of Wang et al. (2003), who evaluated the effects of elevated CO2 on the antioxidant activity and flavonoid content of strawberry fruit in field plots at the U.S. Department of Agriculture's Beltsville Agricultural Research Center in Beltsville, Maryland, where they grew strawberry plants (Fragaria x ananassa Duchesne cv. Honeoye) in six clear-acrylic open-top chambers, two of which were maintained at the ambient atmospheric CO2 concentration, two of which were maintained at ambient + 300 ppm CO2, and two of which were maintained at ambient + 600 ppm CO2 for a period of 28 months (from early spring of 1998 through June 2000).  The scientists harvested the strawberry fruit, in their words, "at the commercially ripe stage" in both 1999 and 2000, after which they analyzed them for a number of different antioxidant properties and flavonol contents.

Before reporting what they found, Wang et al. provide some background by noting that "strawberries are good sources of natural antioxidants (Wang et al., 1996; Heinonen et al., 1998)."  They further report that "in addition to the usual nutrients, such as vitamins and minerals, strawberries are also rich in anthocyanins, flavonoids, and phenolic acids," and that "strawberries have shown a remarkably high scavenging activity toward chemically generated radicals, thus making them effective in inhibiting oxidation of human low-density lipoproteins (Heinonen et al., 1998)."  In this regard, they note that previous studies (Wang and Jiao, 2000; Wang and Lin, 2000) "have shown that strawberries have high oxygen radical absorbance activity against peroxyl radicals, superoxide radicals, hydrogen peroxide, hydroxyl radicals, and singlet oxygen."  In their experiment, therefore, they were essentially seeking to see if atmospheric CO2 enrichment could make a good thing even better.

So what did the Agricultural Research Service scientists find?  They determined, first of all, that strawberries had higher concentrations of ascorbic acid (AsA) and glutathione (GSH) "when grown under enriched CO2 environments."  In going from ambient to ambient + 300 ppm CO2 and ambient + 600 ppm CO2, for example, AsA concentrations increased by 10 and 13%, respectively, while GSH concentrations increased by 3 and 171%, respectively.  They also learned that "an enriched CO2 environment resulted in an increase in phenolic acid, flavonol, and anthocyanin contents of fruit."  For nine different flavonoids, for example, there was a mean concentration increase of 55 ± 23% in going from the ambient atmospheric CO2 concentration to ambient + 300 ppm CO2, and a mean concentration increase of 112 ± 35% in going from ambient to ambient + 600 ppm CO2.  In addition, they report that the "high flavonol content was associated with high antioxidant activity."  As for the significance of these findings, Wang et al. note that "anthocyanins have been reported to help reduce damage caused by free radical activity, such as low-density lipoprotein oxidation, platelet aggregation, and endothelium-dependent vasodilation of arteries (Heinonen et al., 1998; Rice-Evans and Miller, 1996)."

In summarizing their findings, Wang et al. say "strawberry fruit contain flavonoids with potent antioxidant properties, and under CO2 enrichment conditions, increased the[ir] AsA, GSH, phenolic acid, flavonol, and anthocyanin concentrations," further noting that "plants grown under CO2 enrichment conditions also had higher oxygen radical absorbance activity against [many types of oxygen] radicals in the fruit."  Hence, they determined that atmospheric CO2 enrichment truly did "make a good thing better." 

It should also be additionally noted in this regard that elevated levels of atmospheric CO2 also make more of that good thing.  Deng and Woodward (1998), for example, report that after growing strawberry plants in air containing an additional 170 ppm of CO2, total fresh fruit weights were 42 and 17% greater than weights displayed by control plants grown at high and low soil nitrogen contents, respectively; while Bushway and Pritts (2002) report that a two- to three-fold increase in the air's CO2 content boosted strawberry fruit yield by an average of 62%.  In addition, Campbell and Young (1986), Keutgen et al. (1997), and Bunce (2001) report positive strawberry photosynthetic responses to an extra 300 ppm of CO2 ranging from 9% to 197% (mean of 76% ? 15%); and Desjardins et al. (1987) report a 118% increase in photosynthesis in response to a 600 ppm increase in the air's CO2 concentration.

Other researchers have found similar enhancements of antioxidative compounds under enriched levels of atmospheric CO2.  Estiarte et al. (1999), for example, reported that a 180-ppm increase in the air's CO2 content increased the foliar concentrations of flavonoids, which protect against UV-B radiation damage, in field-grown spring wheat by 11 to 14%.  Caldwell et al. (2005), on the other hand, found that an ~75% increase in the air's CO2 content increased the total isoflavone content of soybean seeds by 8% when the air temperature during seed fill was 18°C, by 104% when the air temperature during seed fill was 23°C, by 101% when the air temperature was 28°C, and by 186% and 38%, respectively, when a drought-stress treatment was added to the latter two temperature treatments.  Lastly, in an experiment conducted under very high atmospheric CO2 concentrations, Ali et al. (2005) found that CO2 levels of 10,000 ppm, 25,000 ppm and 50,000 ppm increased total flavonoid concentrations of ginseng roots by 228%, 383% and 232%, respectively, total phenolic concentrations by 58%, 153% and 105%, cysteine contents by 27%, 65% and 100%, and non-protein thiol contents by 12%, 43% and 62%, all of which substances are potent antioxidants.  What is more, it is interesting to note that the increased consumption of such plant material - naturally enriched with antioxidative compounds as a consequence of the historical rise in the air's CO2 content - may have played a role in the observed decline in human mortality rates over the period 1950-1994 (Tuljapurkar et al., 2000).

Ali, M.B., Hahn, E.J. and Paek, K.-Y.  2005.  CO2-induced total phenolics in suspension cultures of Panax ginseng C.A. Mayer roots: role of antioxidants and enzymes.  Plant Physiology and Biochemistry 43: 449-457.

Barbale, D.  1970.  The influence of the carbon dioxide on the yield and quality of cucumber and tomato in the covered areas.  Augsne un Raza (Riga) 16: 66-73.

Bunce, J.A.  2001.  Seasonal patterns of photosynthetic response and acclimation to elevated carbon dioxide in field-grown strawberry.  Photosynthesis Research 68: 237-245.

Bushway, L.J. and Pritts, M.P.  2002.  Enhancing early spring microclimate to increase carbon resources and productivity in June-bearing strawberry.  Journal of the American Society for Horticultural Science 127: 415-422.

Caldwell, C.R., Britz, S.J. and Mirecki, R.M.  2005.  Effect of temperature, elevated carbon dioxide, and drought during seed development on the isoflavone content of dwarf soybean [Glycine max (L.) Merrill] grown in controlled environments.  Journal of Agricultural and Food Chemistry 53: 1125-1129.

Campbell, D.E. and Young, R. 1986. Short-term CO2 exchange response to temperature, irradiance, and CO2 concentration in strawberry. Photosynthesis Research 8: 31-40.

Deng, X. and Woodward, F.I. 1998. The growth and yield responses of Fragaria ananassa to elevated CO2 and N supply. Annals of Botany 81: 67-71.

Dennison, B.A., Rockwell, H.L., Baker, S.L.  1998.  Fruit and vegetable intake in young children.  J. Amer. Coll. Nutr. 17: 371-378.

Desjardins, Y., Gosselin, A. and Yelle, S.  1987.  Acclimatization of ex vitro strawberry plantlets in CO2-enriched environments and supplementary lighting.  Journal of the American Society for Horticultural Science 112: 846-851.

Dickinson, V.A., Block, G., Russek-Cohen, E. 1994. Supplement use, other dietary and demographic variables, and serum vitamin C in NHANES II. J. Amer. Coll. Nutr. 13: 22-32.

Estiarte, M., Penuelas, J., Kimball, B.A., Hendrix, D.L., Pinter Jr., P.J., Wall, G.W., LaMorte, R.L. and Hunsaker, D.J.  1999.  Free-air CO2 enrichment of wheat: leaf flavonoid concentration throughout the growth cycle.  Physiologia Plantarum 105: 423-433.

Gomez-Carrasco, J.A., Cid, J.L.-H., de Frutos, C.B., Ripalda-Crespo, M.J., de Frias, J.E.G.  1994.  Scurvy in adolescence.  J. Pediatr. Gastroenterol. Nutr. 19: 118-120.

Hampl, J.S., Taylor, C.A., Johnston, C.S.  1999.  Intakes of vitamin C, vegetables and fruits: Which schoolchildren are at risk?  J. Amer. Coll. Nutr. 18: 582-590.

Heinonen, I.M., Meyer, A.S. and Frankel, E.N.  1998.  Antioxidant activity of berry phenolics on human low-density lipoprotein and liposome oxidation.  Journal of Agricultural and Food Chemistry 46: 4107-4112.

Idso, S.B., Kimball, B.A., Shaw, P.E., Widmer, W., Vanderslice, J.T., Higgs, D.J., Montanari, A. and Clark, W.D.  2002.  The effect of elevated atmospheric CO2 on the vitamin C concentration of (sour) orange juice.  Agriculture, Ecosystems and Environment 90: 1-7.

Johnston, C.S., Solomon, R.E., Corte, C.  1998.  Vitamin C status of a campus population: College students get a C minus.  J. Amer. Coll. Health 46: 209-213.

Keutgen, N., Chen, K. and Lenz, F. 1997. Responses of strawberry leaf photosynthesis, chlorophyll fluorescence and macronutrient contents to elevated CO2. Journal of Plant Physiology 150: 395-400.

Kimball, B.A., Mitchell, S.T. 1981. Effects of CO2 enrichment, ventilation, and nutrient concentration on the flavor and vitamin C content of tomato fruit.  HortScience 16: 665-666.

Madsen, E.  1971.  The influence of CO2-concentration on the content of ascorbic acid in tomato leaves.  Ugeskr. Agron. 116: 592-594.

Madsen, E.  1975.  Effect of CO2 environment on growth, development, fruit production and fruit quality of tomato from a physiological viewpoint. In: P. Chouard, N. de Bilderling (Eds.), Phytotronics in Agricultural and Horticultural Research.  Bordas, Paris, pp. 318-330.

Ramar, S., Sivaramakrishman, V., Manoharan, K.  1993.  Scurvy - a forgotten disease.  Arch. Phys. Med. Rehabil. 74: 92-95.

Rice-Evans, C.A. and Miller, N.J. 1996. Antioxidant activities of flavonoids as bioactive components of food.  Biochemical Society Transactions 24: 790-795.

Tajiri, T.  1985.  Improvement of bean sprouts production by intermittent treatment with carbon dioxide.  Nippon Shokuhin Kogyo Gakkaishi 32(3): 159-169.

Tuljapurkar, S., Li, N. and Boe, C.  2000.  A universal pattern of mortality decline in the G7 countries.  Nature 405: 789-792.

Wang, H., Cao, G. and Prior, R.L. 1996. Total antioxidant capacity of fruits. Journal of Agricultural and Food Chemistry 44: 701-705.

Wang, S.Y., Bunce, J.A. and Maas, J.L.  2003.  Elevated carbon dioxide increases contents of antioxidant compounds in field-grown strawberries.  Journal of Agricultural and Food Chemistry 51: 4315-4320.

Wang, S.Y. and Jiao, H.  2000.  Scavenging capacity of berry crops on superoxide radicals, hydrogen peroxide, hydroxyl radicals, and singlet oxygen.  Journal of Agricultural and Food Chemistry 48: 5677-5684.

Wang, S.Y. and Lin, H.S.  2000.  Antioxidant activity in fruit and leaves of blackberry, raspberry, and strawberry is affected by cultivar and maturity.  Journal of Agricultural and Food Chemistry 48: 140-146.

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** For additional peer-reviewed scientific references and an in-depth discussion of the science supporting our position, please visit Climate Change Reconsidered: The Report of the Nongovernmental Planel on Climate Change (www.climatechangereconsidered.org), or CO2 Science (www.co2science.org).

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