In one of the earliest papers to address this subject, Idso et al. (1990) grew water lilies in sunken metal stock tanks located out-of-doors and enclosed within clear-plastic-wall open-top chambers through which air of either 350 or 650 ppm CO2 was continuously circulated. Over the course of two growing seasons, he and his colleagues measured a number of plant responses to these two environmental treatments. Their results indicated that the water lilies in the CO2-enriched enclosures grew better than the water lilies in the ambient CO2 enclosures, as the leaves in the CO2-enriched tanks were larger and more substantial, and 75% more of them were produced over the course of the initial five-month growing season.

Each of the plants in the CO2-enriched tanks also produced twice as many flowers as the plants growing in normal air; and the flowers that blossomed in the CO2-enriched air were more substantial than those that bloomed in the air of normal CO2 concentration: they had more petals, the petals were longer, they had a greater percent dry matter content, and each flower consequently weighed about 50% more. In addition, the stems that supported the flowers were slightly longer in the CO2-enriched tanks; and the percent dry matter contents of both the flower and leaf stems were greater, so that the total dry matter in the flower and leaf stems in the CO2-enriched tanks exceeded that of the flower and leaf stems in the ambient-air tanks by approximately 60%.

Several years later, Deng and Woodward (1998) studied the direct and interactive effects of elevated CO2 and nitrogen supply by growing strawberries in controlled glasshouses exposed to atmospheric CO2 concentrations of 390 and 560 ppm at three levels of nitrogen for nearly three months. The two authors found that strawberries growing at the elevated CO2 concentration contained additional sugar and physical mass to support significantly greater numbers of flowers and fruits than in strawberry plants growing at 390 ppm CO2. This effect consequently led to total fresh fruit weights that were 42 and 17% greater in CO2-enriched plants that received the highest and lowest nitrogen levels, respectively.

By the turn of the century many more studies had been published, shedding more light on the subject. Lake and Hughes (1999), for example, found that a 380-ppm increase in the air's CO2 concentration elicited a 35% increase in the total plant biomass of nasturtiums (Tropaeolum majus). Atmospheric CO2 enrichment did not affect flower size in this species; but total flower nectar volume produced by the CO2-enriched nasturtiums was 2.4-fold greater than that produced by ambient-grown control plants. Likewise, Dag and Eisikowitch (2000) reported that atmospheric CO2 enrichment up to 1,000 ppm doubled both the average nectar volume and sugar production per flower in greenhouse-grown melons (Cucumis melo).

Also publishing in the year 2000, Johnson and Lincoln reported that an annual plant native to the southeastern USA (Heterotheca subaxillaris) increased its total biomass by 20% in response to a 300-ppm increase in the air's CO2 content. In addition, the elevated CO2 increased reproductive flower biomass and induced flowering much earlier in the CO2-enriched plants than it did in the ambient-air-grown plants. And in another experiment, Niu et al. (2000) found that yellow and primrose pansies (Viola x wittrockiana) increased their total dry weights by 10 to 30% in response to a 600-ppm increase in the CO2 content of the air, while atmospheric CO2 enrichment increased flower size by 4 to 10%.

One year later, Carvalho and Heuvelink (2001) reported that atmospheric CO2 enrichment positively influences several external quality characteristics of chrysanthemums, including increasing the plant's stem length, number of lateral branches, number of flowers and size of flowers. And in the study of Aloni et al. (2001), a 450-ppm increase in the air's CO2 content was shown to completely ameliorate a 75% high-temperature-induced reduction in bell pepper (Capsicum annuum L.) pollen production that was observed under ambient CO2 concentrations. In addition, although high temperature reduced the number of seeds produced per fruit in ambient-grown plants by 68%, it only reduced this parameter by 9% in CO2-enriched plants.

In another study, Deckmyn et al. (2001) grew white clover plants (Trifolium repens L., cv. Mervi) in four small greenhouses, two of which allowed 88% of the incoming UV-B radiation to pass through their roofs and walls, and two of which allowed 82% to pass through. One of the two greenhouses in each of the UV-B treatments was maintained at ambient CO2 (371 ppm) and the other was maintained at elevated CO2 (521 ppm). Midway through the four-month summer growing season, flower numbers were counted, revealing that the 40% increase in atmospheric CO2 concentration stimulated the production of flowers in the low UV-B treatment by 22% and in the slightly higher UV-B treatment by 43%.

By 2002, so many authors had weighed in on the subject that Jablonski et al. (2002) conducted a meta-analysis of 159 peer-reviewed scientific journal articles published between 1983 and 2000, dealing with the effects of atmospheric CO2 enrichment on the reproductive growth characteristics of several domesticated and wild plants. In calculating the mean responses reported in those papers, Jablonski et al. found that for increases in the air's CO2 concentration ranging from approximately 150 to 450 ppm (rough average of 300 ppm), across all species studied, the extra CO2 supplied to the plants resulted in 19% more flowers, 18% more fruits, 16% more seeds, 4% greater individual seed mass, 25% greater total seed mass (equivalent to yield), and 31% greater total mass.

More studies demonstrating similar positive effects of atmospheric CO2 enrichment on flowering characteristics followed. Silberbush et al. (2003), for example, grew small and large bulbs of Hippeastrum (which produces amaryllis flowers) in greenhouses receiving atmospheric CO2 concentrations of 350 and 1000 ppm for about four hours of each day for 233 days with different combinations of nitrogen and potassium fertilization, in order to study the interactive effects of these parameters on bulb size. Their results indicated that elevated CO2 consistently increased bulb size across all nitrogen and potassium concentrations, with initially larger bulbs yielding the greatest size of final bulbs. However, on a percentage basis, smaller bulbs were slightly more responsive to atmospheric CO2 enrichment than were larger bulbs. Indeed, under optimal nitrogen and potassium fertilization, the 650-ppm increase in the air's CO2 concentration increased the size of smaller and larger bulbs by about 18 and 14%, respectively, suggesting that as the CO2 content of the air increases, Hippeastrum bulbs will increase their size, thus leading to enhanced bulb quality and flower (amaryllis) production.

In another study, Palacios and Zimmerman (2007) piped flue gas generated by the Duke Energy-North America Power Plant at Moss Landing, California (USA) approximately 1 km to a site where it was bubbled through outdoor flow-through seawater aquaria at rates that produced four different aqueous CO2 treatments characteristic of: "(1) the present day atmosphere, with approximately 16 然 CO2(aq), (2) CO2 projected for 2100 that increases the CO2(aq) concentration of seawater to approximately 36 然 CO2(aq), (3) CO2 projected for 2200 that increases the CO2(aq) concentration of seawater to 85 然 CO2(aq), and (4) a dissolved aqueous CO2 concentration of 1123 然 CO2(aq)," which in the earlier study of Zimmerman et al. (1997) had tripled the light-saturated photosynthesis rate of the eelgrass they had studied. So what did the newer eelgrass experiment reveal?

The researchers report that the elevated CO2 "led to significantly higher reproductive output, below-ground biomass and vegetative proliferation of new shoots in light-replete treatments," i.e., those receiving light at 33% of the surface irradiance level. More specifically, they write that "shoots growing at 36 然 CO2(aq) were 25% larger than those in the unenriched treatment [16 然 CO2(aq)]," while "at 85 然 CO2(aq) shoots were 50% larger than those in the unenriched treatment and at 1123 然 CO2(aq) shoots were almost twice as large as those in the unenriched treatment." In addition, they found that at 1123 然 CO2(aq) "22% of the shoots differentiated into flowers, more than twice the flowering output of the other treatments at this light level."

These findings are of great significance and have far-reaching implications. Noting that "increased CO2(aq) is capable of increasing eelgrass reproductive output via flowering, and area-specific productivity via vegetative shoot proliferation under naturally replete light regimes," Palacios and Zimmerman state that "the resulting increases in eelgrass meadow density may initiate a positive feedback loop that facilitates the trapping of sediments and prevents their resuspension, thereby reducing turbidity and increasing light penetration in coastal habitats," such that the resulting increased light penetration "may allow seagrass colonization depths to increase even further."

The two researchers also suggest that the CO2-induced increase in the productivity of eelgrass may "enhance fish and invertebrate stocks as well." In fact, they go so far as to suggest that the "deliberate injection of CO2 to seawater may facilitate restoration efforts by improving the survival rates of recently transplanted eelgrass shoots," noting that "it can buffer the negative effects of transplant shock by increasing rhizome reserve capacity and promoting shoot proliferation in light-replete environments." In addition, they say it "may also facilitate eelgrass survival in environments where conditions are periodically limiting, such as long dark winters or unusually warm summers that produce unfavorable productivity to respiration ratios," and they state that "CO2 injection may also promote flowering and seed production necessary for expansion and maintenance of healthy eelgrass meadows." What is more, they suggest that "rising concentrations of CO2(aq) may increase vegetative propagation and seed production of other seagrass populations besides eelgrass."

In another review paper, Springer and Ward (2007) summarized "the results of 60 studies reporting flowering-time responses (defined as the time to first visible flower) of both crop and wild species at elevated CO2," and in doing so they found that "all possible responses have been observed both among species as well as within species, including accelerated, delayed and no change in flowering time in response to elevated CO2." However, they found that "flowering-time responses of wild species grown at elevated CO2 are much more evenly distributed, in that a similar number of studies report accelerated, delayed, or no change in flowering time, whereas crops primarily showed accelerated flowering (approx. 80% exhibited accelerated flowering)." They also report that "plants utilizing both the C3 and C4 photosynthetic pathways show altered flowering time with elevated CO2," but they say that "two crop species that account for a substantial portion of the world's agricultural production, soybean [a C3 crop] and maize [a C4 crop], do not show consistent patterns in the response of flowering time at elevated CO2."

The two researchers additionally determined that "studies performed within a genus also show a lack of consistent flowering-time response to elevated CO2," and that among only ten genotypes of a single well-studied species (Arabidopsis thaliana), "all possible flowering-time responses to elevated CO2, including delayed, accelerated and unaltered flowering times, were observed." Finally, they report that "a majority of multifactor studies that measured flowering time report no interaction between elevated CO2 and other environmental factors, such as temperature ... nutrient availability ... light ... and ozone," although they note that "a limited number of elevated CO2 studies do show significant interactive effects with other environmental factors."

Springer and Ward thus concluded that the studies they reviewed "clearly show that future increases in atmospheric CO2 will have major effects on the flowering time of both wild and crop species," but they say that "at this time it is not possible to account for the wide variation in flowering-time responses because knowledge of the underlying physiological and molecular mechanisms is incomplete."

Moving on, among a number of other things Darbah et al. (2008) studied the effects of long-term exposure of birch (Betula papyrifera) trees to elevated CO2 (an extra 200 ppm) on flower and pollen production at the Aspen FACE site in Rhinelander, Wisconsin (USA) in the eighth and ninth years (2006 and 2007) of the experiment. And according to the six researchers who performed the analysis, there was "an increase of 140% and 70% for 2006 and 2007, respectively, in the total number of trees that produced male flowers under elevated CO2 and an increase of 260% in 2006 and 100% in 2007, respectively, in the quantity of male flowers produced under elevated CO2."

In the words of the authors, "the increases in the number of trees and in the quantity of male flowers produced under elevated CO2 implies that more birch pollen will be produced," noting that "these results support the findings of Curtis et al. (1994, 1996), Johnson and Lincoln (2000), Edwards et al. (2001), Jablonski et al. (2002), Bunce (2005) and Ladeau and Clark (2006a,b) that elevated CO2 increases reproductive potential through increased pollination, and hence, fertilization and viable seed formation," in harmony with the hypothesis of Herms and Mattson (1992) that "birch trees under adequate carbohydrate status [such as provided by atmospheric CO2 enrichment] tend to favor male flower production." Last of all, they conclude by noting that "since sexual reproductive development is an important stage in the life cycle of plants, any change in the processes involved might have significant implications for the productivity of the plants and their survival," which implications in the case of birch trees and atmospheric CO2 enrichment would clearly be positive.

In the introduction to their study of CO2 and flowers, Johnston and Reekie (2008) write that "there have been marked changes in plant phenology over the past century," and they indicate that these changes "have been interpreted as a consequence of the increase in temperature that has been observed over this time." In addition, they speculate that "the concentration of atmospheric CO2 may also directly affect time of flowering, even in the absence of temperature change." Exploring this dual possibility, Johnston and Reekie examined the effects of elevated atmospheric CO2 concentration by itself (ambient and ambient + 330 ppm) as well as the combined effect of elevated CO2 and elevated air temperature (ambient + 1.5°C) on the flowering phenology of 22 species of plants in the family Asteraceae, which were grown under natural seasonally-varying temperature and daylength in separate compartments of a glasshouse in Wolfville, Nova Scotia, Canada. And what did they find?

The two researchers report that, "on average, elevated CO2 by itself advanced flowering by four days," while "increasing temperature as well as CO2 advanced flowering by an additional three days." They also found that "CO2 was more likely to hasten phenology in long- than in short-day species," and that "early- and late-flowering species did not differ in response to elevated CO2, but the combined effect of elevated CO2 and temperature hastened flowering more in early- than late-flowering species." In light of their several findings, Johnston and Reekie thus concluded that, with respect to time of flowering in Asteraceae species, "the direct effect of CO2 on phenology may be as important as its indirect effect through climate change."

The several observations presented above suggest that a CO2-enriched world will likely produce more and larger flowers, as well as induce other flower-related changes bearing significant implications for plant productivity and survival, almost all of which are positive.

References
Aloni, B., Peet, M., Pharr, M. and Karni, L. 2001. The effect of high temperature and high atmospheric CO2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. Physiologia Plantarum 112: 505-512.

Bunce, J.A. 2005. Seed yield of soybeans with daytime or continuous elevation of carbon dioxide under field conditions. Photosynthetica 43: 435-438.

Carvalho, S.M.P. and Heuvelink, E. 2001. Influence of greenhouse climate and plant density on external quality of chrysanthemum (Dendranthema grandiflorum (Ramat.) Kitamura): first steps toward a quality model. Journal of Horticultural Science & Biotechnology 76: 249-258.

Curtis, P.S., Snow, A.A. and Miller, A.S. 1994. Genotype-specific effects of elevated CO2 on fecundity in wild radish (Raphanus raphanistum). Oecologia 97: 100-105.

Curtis, P.S., Klus, D.J., Kalisz, S. and Tonsor, S.J. 1996. Intraspecific variation in CO2 responses in Raphanus raphinistum and Plantago lanceolata: assessing the potential for evolutionary change with rising atmospheric change. In: Korner, C. and Bazzaz, F.A. (Eds.), Carbon Dioxide, Populations and Communities. Academic Press, New York, NY, USA, pp. 13-22.

Dag, A. and Eisikowitch, D. 2000. The effect of carbon dioxide enrichment on nectar production in melons under greenhouse conditions. Journal of Apicultural Research 39: 88-89.

Darbah, J.N.T., Kubiske, M.E., Nelson, N., Oksanen, E., Vaapavuori, E. and Karnosky, D.F. 2008. Effects of decadal exposure to interacting elevated CO2 and/or O3 on paper birch (Betula papyrifera) reproduction. Environmental Pollution 155: 446-452.

Deckmyn, G., Caeyenberghs, E. and Ceulemans, R. 2001. Reduced UV-B in greenhouses decreases white clover response to enhanced CO2. Environmental and Experimental Botany 46: 109-117.

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.

Edwards, G.R., Clark, H. and Newton, P.C.D. 2001. The effects of elevated CO2 on seed production and seedling recruitment in a sheep grazed pasture. Oecologia 127: 383-394.

Goldsberry, K.L. 1986. CO2 fertilization of carnations and some other flower crops. In: H.Z. Enoch and B.A. Kimball (Eds.), Carbon Dioxide Enrichment of Greenhouse Crops. Vol. II. Physiology, Yield, and Economics. CRC Press, Baca Raton, FL, pp. 117-140.

Hanan, J.J. 1986. CO2 enrichment for greenhouse rose production. In: H.Z. Enoch and B.A. Kimball (Eds.), Carbon Dioxide Enrichment of Greenhouse Crops. Vol. II. Physiology, Yield, and Economics. CRC Press, Baca Raton, FL, pp. 141-149.

Idso, S.B., Allen, S.G. and Kimball, B.A. 1990. Growth response of water lily to atmospheric CO2 enrichment. Aquatic Botany 37: 87-92.

Jablonski, L.M., Wang, X. and Curtis, P.S. 2002. Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytologist 156: 9-26.

Johnson, S.L. and Lincoln, D.E. 2000. Allocation responses to CO2 enrichment and defoliation by a native annual plant Heterotheca subaxillaris. Global Change Biology 6: 767-778.

Johnston, A. and Reekie, E. 2008. Regardless of whether rising atmospheric carbon dioxide levels increase air temperature, flowering phenology will be affected. International Journal of Plant Science 169: 1210-1218.

LaDeau, S.L. and Clark, J.S. 2006a. Elevated CO2 and tree fecundity: the role of tree size, interannual variability, and population heterogeneity. Global Change Biology 12: 822-833.

LaDeau, S.L. and Clark, J.S. 2006b. Pollen production by Pinus taeda growing in elevated atmospheric CO2. Functional Ecology 20: 541-547.

Lake, J.C. and Hughes, L. 1999. Nectar production and floral characteristics of Tropaeolum majus L. grown in ambient and elevated carbon dioxide. Annals of Botany 84: 535-541.

Mortensen, L.M. 1986. Effect of intermittent as compared to continuous CO2 enrichment on growth and flowering of Chrysanthemum x morifolium Ramat. and Saintpaula ionantha H. Wentl. Scientia Horticulturae 29: 283-289.

Niu, G., Heins, R.D., Cameron, A.C. and Carlson, W.H. 2000. Day and night temperatures, daily light integral, and CO2 enrichment affect growth and flower development of pansy (Viola x wittrockiana). Journal of the American Society of Horticultural Science 125: 436-441.

Palacios, S.L. and Zimmerman, R.C. 2007. Response of eelgrass Zostera marina to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Marine Ecology Progress Series 344: 1-13.

Silberbush, M., Ephrath, J.E., Alekperov, Ch. and Ben-Asher, J. 2003. Nitrogen and potassium fertilization interactions with carbon dioxide enrichment in Hippeastrum bulb growth. Scientia Horticulturae 98: 85-90.

Springer, C.J. and Ward, J.K. 2007. Flowering time and elevated atmospheric CO2. New Phytologist 176: 243-255.

Zimmerman, R.C., Kohrs, D.G., Steller, D.L. and Alberte, R.S. 1997. Impacts of CO2-enrichment on productivity and light requirements of eelgrass. Plant Physiology 115: 599-607.