How does rising atmospheric CO2 affect marine organisms?

Click to locate material archived on our website by topic

Health-Promoting Effects of Elevated CO2 (Medicinal Plants) -- Summary
How will the ongoing rise in the air's CO2 content alter the amounts and concentrations of various health-promoting substances produced by medicinal or "health food" plants? This question was broached early on by Stuhlfauth et al. (1987), who found that a near-tripling of the air's CO2 content increased the dry weight production of the woolly foxglove plant (which produces the cardiac glycoside digoxin used in the treatment of cardiac insufficiency) by 63% under dry conditions and by 83% when well-watered, and that the concentration of digoxin within the plant dry mass was enhanced by 11% under well-watered conditions and by 14% under conditions of water stress, after which Stuhlfauth and Fock (1990) obtained similar results in a field study, with a near-tripling of the air's CO2 content leading to a 75% increase in plant dry weight production per unit land area and a 15% increase in digoxin per unit dry weight of plant material, which resulted in an actual doubling of total digoxin yield per hectare of cultivated land.

A full decade later, Idso et al. (2000) grew spider lily plants out-of-doors at Phoenix, Arizona in clear-plastic-wall open-top enclosures that had their atmospheric CO2 concentrations maintained at either 400 or 700 ppm for two consecutive two-year growth cycles. This work revealed that the 75% increase in the air's CO2 concentration increased aboveground plant biomass by 48% and belowground (bulb) biomass by 56%. In addition, the extra CO2 increased the concentrations of five bulb constituents possessing anticancer and antiviral properties. Mean percentage increases in these concentrations were, in the words of the researchers, "6% for a two-constituent (1:1) mixture of 7-deoxynarciclasine and 7-deoxy-trans-dihydronarciclasine, 8% for pancratistatin, 8% for trans-dihydronarciclasine, and 28% for narciclasine, for a mean active-ingredient percentage concentration increase of 12%." And combined with the 56% increase in bulb biomass, these percentage concentration increases resulted in a mean active-ingredient increase of 75% for the 75% increase in the air's CO2 concentration.

Why was this study so important? It was important because the substances studied had been demonstrated to be effective in fighting a number of devastating human maladies, including leukemia, ovary sarcoma, melanoma, and brain, colon, lung and renal cancers, as well as Japanese encephalitis and yellow, dengue, Punta Tora and Rift Valley fevers. And the finding that atmospheric CO2 enrichment increases both bulb biomass and the bulb concentrations of the substances that do these things bodes well for the CO2-induced stimulation of the production of still other botanical-based medicines in other plants.

A good example is the study of Zobayed and Saxena (2004), who worked with St. Johns' wort, a perennial herb native to Europe and West Asia that has been used for treatment of mild to moderate depression, inflammation and wound healing (Brolis et al., 1998; Stevinson and Ernst, 1999), and which has been reported to be a potential source for anticancer, antimicrobial and antiviral medicines (Schempp et al., 2002; Pasqua et al., 2003). In their case, the two scientists grew shoots of the plant for 42 days under well watered and fertilized conditions within a greenhouse, where the air's CO2 concentration averaged 360 ppm, as well as in computer-controlled environment chambers maintained at a mean CO2 concentration of 1000 ppm, with all other environmental conditions being comparable between the two treatments.

On the final day of the study, Zobayed and Saxena determined that the net photosynthetic rates of the plants in the CO2-enriched chambers were 124% greater than those of the plants growing in ambient air, and that their dry weights were 107% greater. In addition, the extra 640 ppm of CO2 in the high-CO2 treatment increased plant concentrations of hypericin and pseudohypericin (two of the major health-promoting substances in the plants) by just over 100%. Consequently, the 180% increase in the air's CO2 content more than doubled the dry mass produced by the well-watered and fertilized St. John's wort plants, while it also more than doubled the concentrations of hypericin and pseudohypericen found in their tissues, which means that the CO2 increase more than quadrupled the total production of these two health-promoting substances.

Mosaleeyanon et al. (2005) also studied St. John's wort, growing well watered and fertilized seedlings for 45 days in controlled-environment chambers at low, medium and high light intensities (100, 300 and 600 Ámol m-2 s-1, respectively) at atmospheric CO2 concentrations of 500, 1000 and 1500 ppm. Then, on the 45th day of their experiment, the plants were harvested, and the hypericin, pseudohypericin and hyperforin (another important health-promoting substance) they contained were extracted from their leaves and quantified.

Under all three light intensities employed in the study, the four researchers found that the 1000-ppm increase in atmospheric CO2 concentration experienced in going from 500 to 1500 ppm produced total plant biomass increases of approximately 32%. And over this same CO2 range, hypericin concentrations rose by 78, 57 and 53%, respectively, under the low, medium and high light intensities, while pseudohypericin concentrations rose by 70, 57 and 67%, and hyperforin concentrations rose by 102, 23 and 3%. Last of all, compared to plants growing out-of-doors in air of 380 ppm CO2 and at light intensities on the order of 1770 Ámol m-2 s-1, Mosaleeyanon et al. discovered that total plant biomass was fully 30 times greater in the high-light, high-CO2 controlled-environment treatment, while under the same conditions the concentrations of hypericin and pseudohypericin were 30 and 41 times greater. Thus, the researchers demonstrated that growing St. John's wort plants in CO2-enriched air in controlled-environment chambers can enormously enhance both plant biomass and hypericin and pseudohypericin contents.

In a concurrent study, Ziska et al. (2005) grew well watered and fertilized tobacco and jimson weed plants from seed in controlled-environment chambers maintained at atmospheric CO2 concentrations of either 378 ppm (ambient) or 690 ppm (elevated) and mean air temperatures of either 22.1 or 27.1°C for 50 and 47 days after planting for tobacco and jimson weed, respectively, while sampling the plants at weekly intervals beginning at 28 days after planting for tobacco and 16 days for jimson weed, in order to determine the effects of these treatments on three plant alkaloids possessing important pharmacological properties: nicotine, in the case of tobacco, and atropine and scopolamine, in the case of jimson weed. And in following these protocols, they found that at the time of final harvest the elevated CO2 had increased the aboveground biomass production of tobacco by approximately 89% at 22.1°C and 53% at 27.1°C, and to have increased that of jimson weed by approximately 23% and 14% at the same respective temperatures. The extra CO2 was also found to have reduced the concentration of nicotine in tobacco, increased the concentration of scopolamine in jimson weed, but to have had no significant effect on the concentration of atropine in jimson weed.

The two significant changes (reduced nicotine in tobacco and increased scopolamine in jimson weed) would likely be characterized as beneficial by most people; for the six scientists reported that nicotine is acknowledged to have significant negative impacts on human health, and that scopolamine is used as a sedative and as "an antispasmodic in certain disorders characterized by restlessness and agitation, (e.g., delirium tremens, psychosis, mania and Parkinsonism)."

Nevertheless, Ziska et al. said "it can be argued that synthetic production of these secondary compounds alleviates any concern regarding environmental impacts on their production from botanical sources," but they added that "developing countries (i.e., ~75% of the world population) continue to rely on ethno-botanical remedies as their primary medicine (e.g. use of alkaloids from jimson weed as treatment for asthma among native Americans and in India)," also noting that "for both developed and developing countries, there are a number of economically important pharmaceuticals derived solely from plants whose economic value is considerable (Raskin et al., 2002)."

Another plant with an impressive history of medicinal use is the ginseng plant. Well known for its anti-inflammatory, diuretic and sedative properties, and long acknowledged to be an effective healing agent (Gillis, 1997), ginseng is widely cultivated in China, South Korea and Japan, where it has been used for medicinal purposes since Greek and Roman times. Normally, four to six years are required for ginseng roots to accumulate the amounts of the various phenolic compounds that are needed to produce their health-promoting effects. Consequently, in an important step in the quest to develop an efficient culture system for the commercial production of ginseng root, Ali et al. (2005) investigated the consequences of growing ginseng plants in suspension culture in bioreactors maintained in equilibrium with air enriched to CO2 concentrations of 10,000 ppm, 25,000 ppm and 50,000 ppm for periods of up to 45 days.

Of most immediate concern in such an experiment would be the effects of the ultra-high CO2 concentrations on root growth. Would they be toxic and lead to biomass reductions or even root death? The answer was a resounding no. After 45 days of growth at 10,000 ppm CO2, root dry weight was increased by about 37% relative to the dry weight of roots produced in bioreactors in equilibrium with ambient air, while it was increased by a lesser 27% after 45 days at 25,000 ppm CO2 and by a still smaller 9% after 45 days at 50,000 ppm CO2. Consequently, although the optimum CO2 concentration for ginseng root growth likely resides somewhere below 10,000 ppm, the concentration at which root growth is reduced below that characteristic of ambient air resides somewhere above 50,000 ppm, for even at that extremely high CO2 concentration, root growth was still greater than it was in ambient air.

Almost everything else measured by Ali et al. was even more dramatically enhanced by the ultra-high CO2 concentrations they employed in their experiment. After 45 days of treatment, total root phenolic concentrations were 58% higher at 10,000 ppm CO2 than at ambient CO2, 153% higher at 25,000 ppm CO2 and 105% higher at 50,000 ppm CO2, as best as can be determined from the bar graphs of their results. Likewise, total root flavonoid concentrations were enhanced by 228%, 383% and 232%, respectively, at the same ultra-high CO2 concentrations, while total protein contents rose by 14%, 22% and 30%, non-protein thiol contents by 12%, 43% and 62%, and cysteine contents by 27%, 65% and 100% under the identical respective set of conditions. What is more, there were equally large CO2-induced increases in the activities of a large number of phenol biosynthetic enzymes.

What are the implications of these results? Ali et al. wrote that "the consumption of foodstuffs containing antioxidant phytonutrients such as flavonoids, polyphenolics, ascorbate, cysteine and non-protein thiol is advantageous for human health," citing Cervato et al. (2000) and Noctor and Foyer (1998). Hence, they concluded that their technique for the culture of ginseng roots in CO2-enriched bioreactors could be used for the large-scale production of an important health-promoting product that could be provided to the public in much greater quantities than is currently possible.

It should be further noted, in this regard, that as the air's CO2 content continues to climb, ginseng and other medicinal plants will likely see the concentrations of their health-promoting substances naturally increased, leading to better human health the world over. This phenomenon, in fact, has likely already played a role in the huge lengthening of human life span that has occurred since the dawn of the Industrial Revolution, as described by Horiuchi (2000) and Tuljapurkar et al. (2000), during which time the air's CO2 concentration rose from something on the order of 280 ppm to its current value of close to 400 ppm.

Another plant that serves as both a health-promoting food and a food delicacy (in China, Japan and Korea) is the brown seaweed Hizikia fusiforme, which was studied by Zou (2005), who collected specimens of it from intertidal rocks along the coast of Nanao Island, Shantou (China) and maintained them in glass aquariums in filtered natural seawater enriched with 60 ÁM NaNO3 and 6.0 ÁM NaH2PO4, where the plants were continuously aerated with either ambient air of 360 ppm CO2 or CO2-enriched air of 700 ppm CO2, while Zou measured the seaweed's relative growth and nitrogen assimilation rates, as well as its nitrate reductase activity. This work revealed that the slightly less than a doubling of the air's CO2 concentration increased the seaweed's mean relative growth rate by about 50%, its mean rate of nitrate uptake during the study's 12-hour light periods by some 200%, and its nitrate reductase activity by approximately 20% over a wide range of substrate nitrate concentrations.

In discussing the implications of these findings, Zou noted that "the extract of H. fusiforme has an immune-modulating activity on humans and this ability might be used for clinical application to treat several diseases such as tumors (Suetsuna, 1998; Shan et al., 1999)." He also wrote that the alga is "becoming one of the most important species for seaweed mariculture in China, owing to its high commercial value and increasing market demand," and it would seem that the ongoing rise in the air's CO2 content would bode well for both of these applications. In addition, Zou has stated that "the intensive cultivation of H. fusiforme would remove nutrients more efficiently with the future elevation of CO2 levels in seawater, which could be a possible solution to the problem of ongoing coastal eutrophication," which in turn suggests that rising atmospheric CO2 concentrations may additionally assist in the amelioration of this important environmental problem.

Also working with a marine alga - specifically, unicellular Nannochloropsis sp. - were Hoshida et al. (2005), who grew the alga in batch culture under normal (370 ppm) and elevated (3,000 and 20,000 ppm) air CO2 concentrations in an attempt to learn how elevated CO2 impacted the alga's ability to produce eicosapentaenoic acid (EPA), which is a major polyunsaturated omega-3 fatty acid that may play an important role in human health related to the prevention of certain cardiovascular diseases (e.g. atherosclerosis, thrombogenesis) and the inhibition of tumor growth and inflammation, as described by Dyerberg et al. (1978), Hirai et al. (1989), Kinsella et al. (1990) and Sanders (1993). In addition, the five researchers remarked that "Nitsan et al. (1999) showed that supplementing the diet of hens with Nannochloropsis sp. led to an increased content of n-3 fatty acids in the egg yolk, indicating an additional role in enhancing the nutritional value of eggs," and they reported that "feeding Nannochloropsis sp. to rats caused a significant increase in the content of n-3 polyunsaturated fatty acids (Sukenik et al., 1994)," suggesting that the alga may play an "important role as the source for n-3 polyunsaturated fatty acids in human nutrition."

But to return to their experiment, what the Japanese scientists found was that "maximum EPA production was obtained when 20,000 ppm CO2 was supplied 12 hours prior to the end of the exponential growth," and that "total EPA production during 4-day cultivation was about twice that obtained with ambient air." They also reported that other researchers had obtained similar results, noting that EPA is found mainly in thylakoid membranes (Sukenik et al., 1989; Hodgson et al., 1991), and that prior experiments had shown that "the amount of stroma thylakoid membrane increased in several plants under elevated CO2 concentrations (Griffin et al., 2001)." In addition, they stated that "in Synechococcus lividus, reduction and synthesis of thylakoid membrane occurred by CO2 deprivation and elevation, respectively (Miller and Holt, 1977)," and that "in Chlorella vulgaris, altering the ambient CO2 concentration varied fatty acid composition (Tsuzuki et al., 1990)."

Last of all, Hoshida et al. indicated that "the effect of CO2 on fatty acid composition and/or fatty acid content had been reported in algae and higher plants (Tsuzuki et al., 1990; Sergeenko et al., 2000; He et al., 1996; Radunz et al., 2000)," and that "increased EPA production caused by elevated CO2 concentration was reported in P. tricornutum (Yongmanitchai and Ward, 1991)." Consequently, as the air's CO2 concentration continues to rise, we can expect concentrations of omega-3 fatty acids to be widely enhanced in both aquatic and terrestrial plants, thereby benefiting much of the animal life of the planet.

Three years later, Ziska et al. (2008) noted that "among medicinal plants, the therapeutic uses of opiate alkaloids from poppy (Papaver spp.) have long been recognized," and they wrote that they felt it was important "to evaluate the growth and production of opiates for a broad range of recent and projected atmospheric carbon dioxide concentrations," which they thus proceeded to do for the wild poppy (P. setigerum), growing well watered and fertilized plants from seed within growth chambers maintained at atmospheric CO2 concentrations of 300, 400, 500 and 600 ppm for a period of 90 to 100 days, while quantifying plant growth and the production of the alkaloids morphine, codeine, papaverine and noscapine, which were derived from latex obtained from capsules produced by the plants.

The three researchers' data indicated that relative to the plants grown at 300 ppm CO2, those grown at 400, 500 and 600 ppm produced approximately 200, 275 and 390% more aboveground biomass, respectively, as best as can be determined from their bar graphs. In addition, they found that "reproductively, increasing CO2 from 300 to 600 ppm increased the number of capsules, capsule weight and latex production by 3.6, 3.0 and 3.7 times, respectively, on a per plant basis," with the ultimate result that "all alkaloids increased significantly on a per plant basis." Hence, they concluded that "as atmospheric CO2 continues to increase, significant effects on the production of secondary plant compounds of pharmacological interest (i.e. opiates) could be expected," which effects, in their words, "are commonly accepted as having both negative (e.g. heroin) and positive (e.g. codeine) interactions with respect to public health," with the obvious hope that the positive effects - which are determined by people - would prevail.

Shortly thereafter, Vurro et al. (2009) wrote that thyme (a well-known culinary and medicinal herb) had "a considerable economic value in the nutraceutical and pharmaceutical industry (Vardar-Uenlue et al., 2003; Konyalioglu et al., 2006)," and that "thyme essential oil possesses per se considerable antioxidant capacity (Economou et al., 1991), and may therefore contribute towards the control of antioxidant status in the leaves." Thus, they grew well-watered one-year-old thyme plants for three additional months (10 June - 10 September) in pots (filled with 40% sand, 25% clay and 35% silt) out-of-doors within a mini-FACE (free-air CO2-enrichment) system at Ravenna, Italy, where the air's CO2 concentration was maintained at approximately 500 ppm (during daylight hours only), and where control plants were continuously exposed to air of approximately 370 ppm CO2, while they measured a number of plant characteristics at the ends of each of the three months of the study.

In reporting their findings, the four researchers stated that "none of the plants grown under high levels of CO2 for 90 days presented either significant differences in fresh weight and dry weight compared with controls, or macroscopic alteration of morphogenesis (number and length of nodes/internodes, branching, leaf area and chlorosis, etc.), at any of the sampling times."

However, they did find that "in plants grown under elevated CO2, a relative increase in oil yield of 32, 34 and 32% was, respectively, recorded in the first, second and third sampling-time (July, August and September)," and they observed a "general depression of the oxidative stress under elevated CO2" that led to a "down-regulation of leaf reactive oxygen species-scavenging enzymes under elevated CO2." In layman's terms, therefore, the Italian scientists said their results pointed to "a 'low cost' life strategy for growth under elevated CO2, not requiring synthesis/activation of energy-intensive and expensive metabolic processes." And this change in behavior should allow the plants to invest more energy in the production of essential plant oils that have, as they have described it, "considerable economic value in the nutraceutical and pharmaceutical industry."

In introducing their study of the subject one year later, Oliveira et al. (2010) said "there is a growing interest in the use of inulin as a health food ingredient, as an alternative for low-calorie sweeteners, and as a dietary fiber and fat substitute (Ritsema and Smeekens, 2003)." In addition, they said "it is suggested" that a daily intake of low amounts of inulin or its derivatives promote the growth of beneficial bacteria in the intestinal tract, as well as anti-tumor effects, citing Roberfroid (2005). Hence, they decided to study Vernonia herbacea, a plant from the Brazilian Cerrado that accumulates inulin-type fructans in underground organs called rhizophores.

The five Brazilian researchers grew well watered and fertilized V. herbacea plants from rhizophore fragments for two months and then transferred them - in groups of three - to 3-L pots containing forest soil, after which they were maintained in open-top chambers within a glasshouse for 120 days at atmospheric CO2 concentrations of either 380 or 760 ppm, where they measured their net photosynthetic rates, water use efficiencies and fructan concentrations after 15, 30, 60, 90 and 120 days of treatment, as well as above- and below-ground biomass at the end of the experiment.

This work revealed, in the words of Oliveira et al., that the "plants under elevated CO2 presented increases in height (40%), photosynthesis (63%) and biomass of aerial (32%) and underground (47%) organs when compared with control plants." In addition, they stated that "water use efficiency was significantly higher in treated plants, presenting a 177% increase at day 60." However, they found that fructan concentration remained unchanged; but because of the significant CO2-induced increase in underground organ biomass, they were able to report that "a 24% increase in total fructan yield occurred." And because of that fact, plus the great increase in water use efficiency displayed by the plants, a CO2-enriched future would appear to bode well for the commercial production of V. herbacea plants throughout much of the central fifth of Brazil - the Cerrado.

In a paper published concurrently, Ghasemzadeh et al. (2010) wrote that "free radicals and single oxygen are recognized as major factors causing various chronic diseases such as cancer, diabetes, etc.," and as a result, they noted that "the health maintenance function of antioxidant components in various foods has received much attention," citing Byers and Guerrero (1995) and Namiki (1990). In this regard, they further indicated that "phenolic acids and flavonoids are antioxidants with health benefits such as anti-inflammatory and anti-tumor effects (Heijnen et al., 2001; Chun et al., 2003; Harborne and Williams, 2000; Chen, 2004)," specifically stating that "Sung-jin et al. (2008) showed that some flavonoid components in green tea are effective in inhibiting cancer or induce mechanisms that may kill cancer cells and inhibit tumor invasion."

Working with Malaysian young ginger (Zingiber officinale) - one of the medicinal/food plants that have been used by Polynesians for over 2,000 years for treating cancer, diabetes, high blood pressure, and many other illnesses - the Malaysian researchers thus grew two varieties of the plant (Halia Bentong and Halia Bara) from rhizomes planted in a drip-irrigated 1:1 mixture of burnt rice husk and coco peat in polyethylene bags placed within controlled-environment chambers that were maintained at atmospheric CO2 concentrations of either 400 or 800 ppm for a period of 16 weeks, after which the plants were harvested and their leaves and rhizomes analyzed for a wide variety of phenolics and flavonoids, along with their free radical scavenging power, which is a measure of their ability to prevent dangerous reactive oxygen species from attacking various parts of the body and causing a large number of potentially life-threatening maladies.

This work revealed, in the words of Ghasemzadeh et al., that on average, "flavonoid compounds increased 44.9% in leaves and 86.3% in rhizomes of Halia Bentong and 50.1% in leaves and 79% in rhizomes of Halia Bara when exposed to elevated carbon dioxide conditions," while phenolic compounds increased even more: by 79.4% in leaves and 107.6% in rhizomes of Halia Bentong and 112.2% in leaves and 109.2% in rhizomes of Halia Bara under the same conditions. In addition, they determined that when the CO2 concentration was increased from 400 to 800 ppm, the free radical scavenging power increased by 30.0% in Halia Bentong and 21.4% in Halia Bara. And they again found that "the rhizomes exhibited more enhanced free radical scavenging power, with 44.9% in Halia Bentong and 46.2% in Halia Bara."

In commenting on their findings, the three scientists said their results indicated that "the yield and pharmaceutical quality of Malaysian young ginger varieties can be enhanced by controlled environment production and CO2 enrichment." And it should also be noted that these same benefits will also accrue without any effort on man's part as the air's CO2 content continues to rise.

One year later, Ghasemzadeh and Jaafar (2011) indicated that ginger (Zingiber officinale Roscoe) "is an important horticultural crop in tropical Southeast Asia," noting that it is the Asian continent's "most widely used herb" and that it "contains several interesting bioactive constituents and possesses health promoting properties (Rozanida et al., 2005)." However, they lamented the fact that "no information is available on the effect of CO2 concentration on the polyphenolic content and scavenging capacity against active oxygen species of Malaysian young ginger varieties."

In an effort designed to address this lack of pertinent data, the two Malaysian scientists grew two varieties of ginger (Halia Bentong and Halia Bara) from rhizomes placed in polyethylene bags filled with a 1:1 mixture of burnt rice husk and coco peat for a period of 16 weeks in controlled-environment chambers maintained at two different atmospheric CO2 concentrations (400 and 800 ppm), during and after which time they measured a number of important plant properties. And what did they find?

In response to the increase in the air's CO2 content, Ghasemzadeh and Jaafar found that the rate of photosynthesis was increased by 65% in Halia Bentong and by 46% in Halia Bara, which led to total biomass increases of 48% in Halia Bentong and 76% in Halia Bara. In addition, they reported that total flavonoids in the new rhizomes of Halia Bentong and Halia Bara rose by 82% and 118%, respectively, while total phenolics in the same two varieties rose by 154% and 183%, respectively.

In commenting on their findings, the two researchers stated that their study had shown that "ginger has good free radical scavenging ability and therefore can be used as a radical inhibitor or scavenger, acting possibly as a primary antioxidant." And they added that increasing the CO2 content of the atmosphere "can enhance the antioxidant activity of ginger extract, especially in its rhizomes," which can be of great value in that it thereby "increases the concentrations of several therapeutic compounds."

Contemporaneously, Ibrahim and Jaafar (2011) reported that "the antioxidant properties in food have been a focus of interest in recent years due to the health maintenance functions of these components that can help reduce the risk of chronic diseases such as cancer, hypertension and diabetes," noting that this phenomenon "is attributed to the high scavenging activity of antioxidants towards free radicals that are usually associated with these diseases (Namiki, 1990; Byers and Guerrero, 1995)." And they thus went on to describe how they used a randomized complete block design 3 by 3 experiment to study and distinguish the relationships among production of secondary metabolites (total phenolics, total flavonoids, gluthatione, oxidized gluthatione, soluble carbohydrate and antioxidant activities of the Malaysian medicinal herb Labisia pumila Blume under three levels of CO2 enrichment (400, 800 and 1200 ppm) for 15 weeks.

This work revealed, in the words of the two Universiti Putra Malaysia researchers, that "secondary metabolites, glutathione, oxidized gluthathione and antioxidant activities in a descending manner came from the leaf enriched with 1200 ppm CO2 > leaf 800 ppm CO2 > leaf 400 ppm CO2 > stem 1200 ppm CO2 > stem 800 ppm CO2 > stem 400 ppm CO2 > root 1200 ppm CO2 > root 800 ppm CO2 > root 400 ppm CO2," and they said that "correlation analyses revealed strong significant positive coefficients of antioxidant activities with total phenolics, flavonoids, gluthatione and oxidized gluthatione," indicating that "an increase in antioxidative activity of L. pumila under elevated CO2 might be up-regulated by the increase in production of total phenolics, total flavonoids, glutathione, oxidized gluthatione and soluble sugar." So Ibrahim and Jaafar concluded by saying that their study results implied that "the medicinal potential of herbal plants such as L. pumila can be enhanced under elevated CO2, which simultaneously improved the antioxidative activity that was indicated by the high oxygen radical absorbance activity against peroxyl radicals, superoxide radicals, hydrogen peroxide and hydroxyl radicals."

Also experimenting concurrently were Moghaddam et al. (2011), who as background for their study wrote that Centella asiatica or Gotu Kola is a small herbaceous annual plant that has been used as a medicinal herb or nutraceutical in Ayurvedic, African and traditional Chinese medicine for more than 2000 years, where it is valued for its mildly antibacterial, antiviral and anti-inflammatory properties. It has additionally been used as a rejuvenating diuretic herb that is purported to clear toxins, to reduce inflammations and fevers, to improve healing and immunity, to improve memory, and to have a balancing effect on the nervous system, as well as a whole host of other uses to which it has been put over the ages and in different parts of the world. So what did the six scientists do with the little herb?

Well watered and fertilized C. asiatica plants were grown for four to five weeks in individual polybags filled with a 1:1:1 mix of sand, coco dust and compost within controlled environment chambers, where CO2 concentrations of 400 and 800 ppm were maintained, in the words of the researchers, "for two hours every day between 8:30 to 10:30 am," at the ends of which four- to five-week periods the plants were harvested and their leaves assessed for total biomass and total flavonoid content, the latter of which set of substances is considered to be the source of the many health benefits attributed to the species.

These efforts enabled Moghaddam et al. to report that the daily two-hour 400-ppm increase in the controlled environment chambers' atmospheric CO2 concentration led to a 193% increase in C. asiatica leaf biomass, a 264% increase in plant water use efficiency, as well as a 171% increase in leaf total flavonoid content, which findings led the six scientists to conclude that "collectively, the enhancement in yield and quality provides an economic motivation to produce a consistent pharmaceutical-grade product for commercial purposes," via what they described as "controlled environment plant production." And it also stands to reason that the ongoing rise in the atmosphere's CO2 concentration should be gradually increasing the medicinal potency of C. asiatica plants either growing wild or cultivated out-of-doors.

Moving one year closer to the present, Ibrahim and Jaafar (2012) studied the oil palm Elaeis guineensis (Jacq.) - the highest yielding vegetable oil producer in the world - which has gained wide recognition because of the health-promoting properties of some of its flavonoids and phenolics that the two scientists described as "natural antioxidants that may reduce oxidative damage to the human body," citing the work of Mandel and Youdim (2004). Over a period of 15 weeks, the two researchers grew initially-five-month-old seedlings of three progenies of oil palm (deli AVROS, Deli Yangambi and Deli URT) within growth chambers maintained at atmospheric CO2 concentrations of either 400, 800 or 1200 ppm, during which time they measured a large number of important plant properties and processes.

These efforts led them to discover that the production of total flavonoids and phenolics was highest under 1200 and lowest at 400 ppm CO2, and that "the antioxidant activity, as determined by the ferric reducing/antioxidant potential (FRAP) activity increased with increasing CO2 levels." In leaves, for example, they found that the quantity of "total flavonoids was enhanced by 86% and 132%, respectively, in 800 and 1200 ppm compared to 400 ppm CO2," while total phenolics "increased by 52% to 91% under elevated CO2 compared to the ambient CO2 condition." And as for what their findings implied, Ibrahim and Jaafar said they "suggest that enrichment with higher than ambient CO2 level is able to enhance the production of gallic acid and rutin in oil palm seedlings," which finding is important because these bioactive components, as they described them, "act as free radical scavengers, and hence can reduce the possibilities of major diseases such as cancers of leukemia, breast, bone and lung," citing Kaufman et al. (1999) and Wink (1999).

Closing out this topical review is the study of Jaafar et al. (2012), who introduced their contribution by writing that "plant antioxidants have been a focus of attention in recent years due to the health preservation functions of these components that can help reduce the threat of chronic diseases such as cancer, diabetes and hypertension," which benefits, in their words, are "attributed to the high scavenging activity of antioxidants towards free radicals that are usually associated with these diseases (Byers and Guerrero, 1995)." Among this group of plant compounds are phenolic acids and flavonoids, both of which exhibit, as they have described it, "high anti-inflammatory and anti-carcinogenic activities (Heijnen et al., 2001; Chun et al., 2003)." In addition, phenolics and flavonoids can function as reducing agents, free radical scavengers and quenchers of singlet oxygen formation (Chan et al., 2008); and many of the components of polyphenols have been proven to have significant roles in curing cancer and other human ailments (Harborne and Williams, 2000).

In describing their own work on the subject, Jaafar et al. said they conducted a split plot 3 x 3 experiment that was designed to examine the impact of 15 weeks of exposure to three different concentrations of CO2 (400, 800 and 1200 ppm) on the phenolic and flavonoid compound profiles - as well as the antioxidant activities - of three varieties (alata, pumila and lanceolata) of Labisia pumila Benth. or kacip fatimah as it is commonly known throughout Southeast Asia, which they describe as "a sub-herbaceous plant with creeping stems from the family Myrsinaceae that is found widespread in Indochina and throughout the Malaysian forest," and which has historically been used to help maintain a healthy female reproductive system.

Among a wide variety of findings, the three Malaysian researchers reported that when exposed to elevated CO2 (1200 ppm), "gallic acid increased tremendously, especially in var. alata and pumila (101-111%), whilst a large quercetin increase was noted in var. lanceolata (260%), followed closely by alata (201%)." They also found that "caffeic acid was enhanced tremendously in var. alata (338-1100%) and pumila (298-433%)," while "rutin continued to increase by 262% after CO2 enrichment." In addition, they found that naringenin was enhanced by 1100% in var. pumila. And last of all, they reported that "the increase in production of plant secondary metabolites in L. pumila was followed by enhancement of the antioxidant activity under exposure of elevated CO2."

In conclusion, therefore, and in light of everything discussed above, it is clear that atmospheric CO2 enrichment positively impacts the production of numerous health-promoting substances found in medicinal or "health food" plants, and that this phenomenon may have contributed to the increase in human life span that has occurred over the past century or so (Horiuchi, 2000; Tuljapurkar and Boe, 2000). Therefore, as the atmosphere's CO2 content continues to rise, there is reason to believe that humanity may be helped even more in this regard in the years and decades to come.

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.

Brolis, M., Gabetta, B., Fuzzati, N., Pace, R., Panzeri, F. and Peterlongo, F. 1998. Identification by high-performance liquid chromatography-diode array detection-mass spectrometry and quantification by high-performance liquid chromatography-UV absorbance detection of active constituents of Hypericum perforatum. Journal of Chromatography A 825: 9-16.

Byers, T. and Guerrero, N. 1995. Epidemilogic evidence for vitamin C and vitamin E in cancer prevention. American Journal of Clinical Nutrition 62: 1385-1392.

Cervato, G., Carabelli, M., Gervasio, S., Cittera, A., Cazzola, R.. and Cestaro, B. 2000. Antioxidant properties of oregano (Origanum vulgare) leaf extracts. Journal of Food Biochemistry 24: 453-465.

Chan, E.W.C., Lim, Y.Y., Wong, L.F., Lianto, F.S., Wong, S.K., Lim, K.K., Joe, C.E. and Lim, T.Y. 2008. Antioxidant and tyrosinase inhibition properties of leaves and rhizomes of ginger species. Food Chemistry 109: 477-483.

Chen, G. 2004. Effect of low fat and/or high fruit and vegetable diets on plasma level of 8-isoprostane-F2alpha in nutrition and breast health study. Nutrition and Cancer 50: 155-160.

Chun, O.K., Kim, D.O. and Lee, C.Y. 2003. Superoxide radical scavenging activity of the major polyphenols in fresh plums. Journal of Agriculture and Food Chemistry 51: 8067-8072.

Dyerberg, J., Bang, H.O., Stoffersen, E., Moncada, S. and Vane, J.R. 1978. Eicosapentaenoic acid and prevention of thrombosis and atherosclerosis. Lancet 2: 117-119.

Economou, K.D., Oreopoulou, V. and Thomopoulos, C.D. 1991. Antioxidant activity of some plant extracts of the family Labiatae. Journal of the American Oil Chemists' Society 68: 109-113.

Gillis, C.N. 1997. Panax ginseng pharmacology: a nitric oxide link? Biochemical Pharmacology 54: 1-8.

Ghasemzadeh, A. and Jaafar, H.Z.E. 2011. Effect of CO2 enrichment on synthesis of some primary and secondary metabolites in ginger (Zingiber officinale Roscoe). International Journal of Molecular Sciences 12: 1101-1114.

Ghasemzadeh, A., Jaafar, H.Z.E. and Rahmat, A. 2010. Elevated carbon dioxide increases contents of flavonoids and phenolic compounds, and antioxidant activities in Malaysian young ginger (Zingiber officinale Roscoe.) varieties. Molecules 15: 7907-7922.

Griffin, K.L., Anderson, O.R., Gastrich, M.D., Lewis, J.D., Lin, G., Schuster, W., Seemann, J.R., Tissue, D.T., Turnbull, M.H. and Whitehead, D. 2001. Plant growth in elevated CO2 alters mitochondrial number and chloroplast fine structure. Proceedings of the National Academy of Sciences, USA 98: 2473-2478.

Harborne, J.B. and Williams, C.A. 2000. Advances in flavonoid research science. Phytochemistry 55: 481-504.

He, P., Radunz, A., Bader, K.P. and Schmid, G.H. 1996. Quantitative changes of the lipid and fatty acid composition of leaves of Aleurites montana as a consequence of growth under 700 ppm CO2 in the atmosphere. Zeitschrift fur Naturforscher 51 C: 833-840.

Heijnen, C.G., Haenen, G.R., Vanacker, F.A., Vijgh, W.J. and Bast, A. 2001. Flavonoids as peroxynitrite scavengers: the role of the hydroxyl groups. Toxicology in Vitro 15: 3-6.

Hirai, A., Terano, T., Tamura, Y. and Yoshida, S. 1989. Eicosapentaenoic acid and adult diseases in Japan: Epidemiological and clinical aspects. Journal of Internal Medicine, Supplement 225: 69-75.

Hodgson, P.A., Henderson, R.J., Sargent, J.R. and Leftley, J.W. 1991. Patterns of variation in the lipid class and fatty acid composition of Nannochloropsis oculata (Eustigmatophyceae) during batch culture. I. The growth cycle. Journal of Applied Phycology 3: 169-181.

Horiuchi, S. 2000. Greater lifetime expectations. Nature 405: 744-745.

Hoshida, H., Ohira, T., Minematsu, A., Akada, R. and Nishizawa, Y. 2005. Accumulation of eicosapentaenoic acid in Nannochloropsis sp. in response to elevated CO2 concentrations. Journal of Applied Phycology 17: 29-34.

Ibrahim, M.H. and Jaafar, H.Z.E. 2011. Increased carbon dioxide concentration improves the antioxidative properties of the Malaysian herb Kacip Fatimah (Labisia pumila Blume). Molecules 16: 6068-6081.

Ibrahim, M.H. and Jaafar, H.Z.E. 2012. Impact of elevated carbon dioxide on primary, secondary metabolites and antioxidant responses of Eleais guineensis Jacq. (oil palm) seedlings. Molecules 17: 5195-5211.

Idso, S.B., Kimball, B.A., Pettit III, G.R., Garner, L.C., Pettit, G.R. and Backhaus, R.A. 2000. Effects of atmospheric CO2 enrichment on the growth and development of Hymenocallis littoralis (Amaryllidaceae) and the concentrations of several antineoplastic and antiviral constituents of its bulbs. American Journal of Botany 87: 769-773.

Jaafar, H.Z.E., Ibrahim, M.H. and Karimi, E. 2012. Phenolics and flavonoids compounds, phenylanine ammonia lyase and antioxidant activity responses to elevated CO2 in Labisia pumila (Myrisinaceae). Molecules 17: 6331-6347.

Kaufman, P.B., Cseke, L.J., Warber, S., Duke, J.A. and Brielmann, H.L. 1999. Natural Products from Plants. CRC Press, Boca Raton, Florida, USA.

Kinsella, J.E., Lokesh, B. and Stone, R.A. 1990. Dietary n-3 polyunsaturated fatty acids and amelioration of cardiovascular diseases: Possible mechanisms. American Journal of Clinical Nutrition 52: 10-28.

Konyalioglu, S., Ozturk, B. and Meral, G.E. 2006. Comparison of chemical compositions and antioxidant activities of the essential oils of two Ziziphora taxa from Anatolia. Pharmaceutical Biology 44: 121-126.

Mandel, S. and Youdim, M.B. 2004. Catechin polyphenols: Neurodegeneration and neuroprotection in neurodegenerative diseases. Free Radical Biology and Medicine 37: 304-317.

Miller L.S. and Holt, S.C. 1977. Effect of carbon dioxide on pigment and membrane content in Synechococcus lividus. Archives Microbiologie 115: 185-198.

Moghaddam, S.S., Jaafar, H.B., Aziz, M.A., Ibrahim, R., Rahmat, A.B. and Philip, E. 2011. Flavonoid and leaf gas exchange responses of Centella asiatica to acute gamma irradiation and carbon dioxide enrichment under controlled environment conditions. Molecules 16: 8930-8944.

Mosaleeyanon, K., Zobayed, S.M.A., Afreen, F. and Kozai, T. 2005. Relationships between net photosynthetic rate and secondary metabolite contents in St. John's wort. Plant Science 169: 523-531.

Namiki, M. 1990. Antioxidant/antimutagens in food. Critical Reviews in Food Science and Nutrition 29: 273-300.

Nitsan, Z., Mokady, S. and Sukenik, A. 1999. Enrichment of poultry products with omega 3 fatty acids by dietary supplementation with the alga Nannochloropsis and mantur oil. Journal of Agricultural and Food Chemistry 47: 5127-5132.

Noctor, G. and Foyer, C.H. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49: 249-279.

Oliveira, V.F., Zaidan, L.B.P., Braga, M.R., Aidar, M.P.M. and Carvalho, M.A.M. 2010. Elevated CO2 atmosphere promotes plant growth and inulin production in the cerrado species Vernonia herbacea. Functional Plant Biology 37: 223-231.

Pasqua, G., Avato, P., Monacelli, B., Santamaria, A.R. and Argentieri, M.P. 2003. Metabolites in cell suspension cultures, calli, and in vitro regenerated organs of Hypericum perforatum cv. Topas. Plant Science 165: 977-982.

Radunz, A., Alfermann, K. and Schmid, G.H. 2000. State of the lipid and fatty acid composition in chloroplasts of Nicotiana tabacum under the influence of an increased CO2 partial pressure of 700 p.p.m. Biochemical Society Transactions 28: 885-887.

Raskin, I., Ribnicky, D.M., Komarnytsky, S. et al. 2002. Plants and human health in the twenty-first century. Trends in Biotechnology 20: 522-531.

Ritsema, T. and Smeekens, S. 2003. Fructans: beneficial for plants and humans. Current Opinion in Plant Biology 6: 223-230.

Roberfroid, M.B. 2005. Introducing inulin-type fructans. British Journal of Nutrition 93: S13-S25.

Rozanida, A.R., Nurul Izza, N., Mohd Helme, M.H. and Zanariah, H. 2005. Xanwhite TM - A Cosmeceutical Product from Species in the Family Zingiberaceae. Forest Research Institute, Selangor Malaysia, pp. 31-36.

Sanders, T.A.B. 1993. Marine oils: Metabolic effects and role in human nutrition. Proceedings of the Nutrition Society 52: 457-472.

Schempp, C.M., Krikin, V., Simon-Haarhaus, G., Kersten, A., Kiss, J., Termeer, C.C., Gilb, B., Kaufmann, T., Borner, C., Sleeman, J.P. and Simon, J.C. 2002. Inhibition of tumour cell growth by hyperforin, a novel anticancer drug from St. John's wort that acts by induction of apoptosis. Oncogene 21: 1242-1250.

Sergeenko, T.V., Muradyan, E.A., Pronina, N.A., Klyachko-Gurvich, G.L., Mishina, I.M. and Tsoglin, L.N. 2000. The effect of extremely high CO2 concentration on the growth and biochemical composition of microalgae. Russian Journal of Plant Physiology 47: 632-638.

Shan, B.E., Yoshida, Y., Kuroda, E. and Yamashita, U. 1999. Immunomodulating activity of seaweed extract on human lymphocytes in vitro. International Journal of Immunopharmacology 21: 59-70.

Stevinson, C. and Ernst, E. 1999. Hypericum for depression: an update of the clinical evidence. European Neuropsychopharmacology 9: 501-505.

Stuhlfauth, T., Fock, H.P. 1990. Effect of whole season CO2 enrichment on the cultivation of a medicinal plant, Digitalis lanata. Journal of Agronomy and Crop Science 164: 168-173.

Stuhlfauth, T., Klug, K. and Fock, H.P. 1987. The production of secondary metabolites by Digitalis lanata during CO2 enrichment and water stress. Phytochemistry 26: 2735-2739.

Suetsuna, K. 1998. Separation and identification of angiotensin I-converting enzyme inhibitory peptides from peptic digest of Hizikia fusiformis protein. Nippon Suisan Gakkaishi 64: 862-866.

Sukenik, A., Cameli, Y. and Berner, T. 1989. Regulation of fatty acid composition by irradiance level in the eustigmatophyte Nannochloropsis sp. Journal of Phycology 25: 686-692.

Sukenik, A., Takahashi, H. and Mokady, S. 1994. Dietary lipids from marine unicellular algae enhance the amount of liver and blood omega-3 fatty acids in rats. Annals of Nutrition and Metabolism 38: 85-96.

Sung-Jin, P., Hoon, M., Young-Youn, K., Jun-Young, P., Jun-Woo, P., Myung-Jin, K. and Soon-Min, H. 2008. Anticancer effects of genistein, green tea catechins, and cordycepin on oral squamous cell carcinoma. Journal of Korean Oral and Maxillofacial Surgery 34: 1-10.

Tsuzuki, M., Ohnuma, E., Sato, N., Takaku, T. And Kawaguchi, A. 1990. Effects of CO2 concentration during growth on fatty acid composition in microalgae. Plant Physiology 93: 851-856.

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

Vardar-Uenlue, G., Candan, F., Soekmen, A., Daferera, D., Polissiou, M., Soekmen, M., Doenmez, E. and Tepe, B. 2003. Antimicrobial and antioxidant activity of the essential oil and methanol extracts of Thymus pectinatus Fisch. et Mey var. pectinatus (Lamiaceae). Journal of Agricultural and Food Chemistry 51: 63-67.

Vurro, E, Bruni, R., Bianchi, A. and di Toppi, L.S. 2009. Elevated atmospheric CO2 decreases oxidative stress and increases essential oil yield in leaves of Thymus vulgaris grown in a mini-FACE system. Environmental and Experimental Botany 65: 99-106.

Wink, M. 1999. Introduction: Biochemistry, Role and Biotechnology of Secondary Products. CRS Press, Boca Raton, Florida, USA, pp. 1-16.

Yongmanitchai, W. and Ward, O.P. 1991. Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Applied Environmental Microbiology 57: 419-425.

Ziska, L.H., Emche, S.D., Johnson, E.L., George, K., Reed, D.R. and Sicher, R.C. 2005. Alterations in the production and concentration of selected alkaloids as a function of rising atmospheric carbon dioxide and air temperature: implications for ethno-pharmacology. Global Change Biology 11: 1798-1807.

Ziska, L.H., Panicker, S. and Wojno, H.L. 2008. Recent and projected increases in atmospheric carbon dioxide and the potential impacts on growth and alkaloid production in wild poppy (Papaver setigerum DC.). Climatic Change 91: 395-403.

Zobayed, S. and Saxena, P.K. 2004. Production of St. John's Wort plants under controlled environment for maximizing biomass and secondary metabolites. In Vitro Cellular and Developmental Biology - Plant 40: 108-114.

Zou, D. 2005. Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250: 726-735.

Last updated 22 January 2014