A Review of CO2 Enrichment Studies: Does Enhanced Photosynthesis Enhance Growth?

Plants typically only convert 2 to 4% of available energy into actual growth and this natural inefficiency provides a reason for scientists to attempt to increase the efficiency of the process by increasing photosynthesis. One of the most common methods, other than genetic modification, to increase photosynthesis is to increase ambient CO2. Elevated CO2 can lead to growth increases ranging from 10 to 50%, depending on the plant’s carbon sink capacity and nutrient availability. Previous studies show that elevated CO2inevitably leads to increased growth, but the magnitude of the growth varies with the photosynthetic capacity of the plant. Photosynthesis is an inefficient process with a maximum of 8 to 10% of the energy in sunlight being converted into chemical energy. Realistically, only 2 to 4% of energy in sunlight is converted. In this paper, Kirschbaum examines previous studies and conducts experiments of his own in order to summarize the current knowledge on CO2enrichment studies, focusing on the ability of increased photosynthesis to ultimately increase plant growth. Kirschbaum studies the factors that affect plant growth under elevated CO2 in an attempt to determine if photosynthesis is the main factor increasing growth or if other factors are relatively more important.—Taylor Jones
Kirschbaum, M.U.F., 2011. Does Enhanced Photosynthesis Enhance Growth? Lessons Learned from CO2 Enrichment Studies.  Plant Physiology 155, 117-124.

          Kirschbaum first examines the photosynthetic response to increasing CO2concentrations and distinguishes between Rubisco-limited photosynthetic rates and ribose 1,5-bisphosphate (RuBP) regeneration-limited rates. For both photosynthetic rates, the relative responsiveness of increases in CO2concentration decreases as atmospheric CO2 continues to increase. Photosynthesis is limited by Rubisco-limited rates at low CO2concentrations and RuBP regeneration-limited rates at high concentrations, and scientists argue that the amounts of Rubisco plants have today is in excess of what is needed, so most plants experience RuBP regeneration-limited photosynthesis. Changes in plant photosynthesis are supported by previous studies, as 30 to 40% enhancements in photosynthesis were recently found in free-air CO2 enrichment experiments and a 58% increase was found in a controlled plot experiment. Kirschbaum notes that there are important limitations to any photosynthesis study as plants that experience less light and increased self-shading may have less enhancement of photosynthesis, while plants grown in high temperature conditions may have more. On average, increases in ambient CO2 lead to a 30% enhancement of photosynthesis, but does this translate to a 30% enhancement of growth?
          Studies show that the relative growth rate for plants is often similar among species and enhanced photosynthesis often leads to only a 10% increase in the relative growth rate. Kirschbaum suggests that previous studies show an increases in photosynthesis leads to 20% enhanced leaf area, but also a 6.5% increase in leaf weight due to increase amounts of carbohydrates and this leads to an ineffective transformation of increased photosynthetic rates to new growth. Extra amounts of carbon produced from photosynthesis can only be of use if the plant can utilize it through root growth, new foliage, or other carbon sinks. Also, carbon cannot be used efficiently if other vital resources, such as nitrogen, are lacking. Studies have shown that many plants show strong photosynthetic enhancement during the growth stages, reduced enhancement during the flowering stages and then increased enhancement during the fruiting stages. During the flowering stages, plants lost much of their potential carbon sink that exists in the growth phase and is regained through seed production in the flowering stage. Most plants show some increased growth response to elevated CO2, but the degree of this growth is determined by other limiting factors, such as carbon sink and nitrogen availability.
          Kirschbaum also notes that a large number of papers use biomass enhancement ratios to determine the effects of elevated CO2 on plant growth. Biomass enhancement ratios are often much greater than relative growth rates and also greater for single-plant studies and fast-growing plants. Under elevated CO2, plants often experience exponential growth in early stages, followed by average growth rates in intermediate stages. Plants that experience an overall relative growth rate of 10% can experience a biomass enhancement ratio of 50% in intermediate stages which eventually decreases to about 10% in later stages. This concept explains why fast-growing plants can have higher biomass enhancement ratios compared to slower-growing plants, but the same relative growth rate. Therefore, the length of an experiment is very important and should be considered when examining the biomass enhancement ratio of a plant to determine if real growth increases exist. The biomass enhancement ratio can often be a misleading value as it can be manipulated by varying the length of an experiment.
          Kirschbaum identifies other issues that may affect photosynthetic enhancement rates that need to be considered, such as natural competition and growth response in mixed-species communities. Also, some studies have shown a decrease in protein concentrations under elevated CO2. Plant herbivore interactions might also change as elevated CO2 usually leads to lower nutrient concentrations which reduces the rate of herbivores feeding on the plant and as a result, herbivores may attempt to consume more of the plant. All of these factors are important complicating issues and should be addressed further.
          In conclusion, photosynthetic enhancement due to elevated CO2 increases the carbon available to plants and whether or not this translates to growth depends on other colimiting factors, such as nutrient availability and carbon sink. Increases in carbon will exacerbate any other limitations. Plants are also subjected to genetic constraints and will only respond to increases in photosynthesis to levels within their genetic capability. By examining several CO2 enrichment experiments, Kirschbaum found that growth enhancements are modest and a 10% increase in relative growth rate can translate to a much higher relative growth rate in the early exponential phases of plant growth. Kirschbaum suggests that genetic manipulation of photosynthesis should include appropriate crop management and close examination of plant attributes to maximize photosynthetic enhancement.

The Effects of Increased CO2 on Biomass and Exogenous-Toxin Quantity in Transgenic Bt Cotton and Rice Crops

Transgenic crops have become an increasingly important component of modern agroecosystems, ideally providing environmentally friendly, disease resistant crops with combinations of multiple genes that improve productivity and agricultural yield. One of the most common types of transgenic crop is Bacillus thuringiensis (“Bt”), which is produced worldwide and exhibits a strong resistance to lepidopteran pests in multiple cropping environments. With CO2 levels expected to increase in the future, scientists question the ability of Bt crops to adapt to changing atmospheric conditions and some hypothesize that increasing CO2 will pose new ecological risks for Bt crops and possibly reduce their effectiveness against target pests. In this study, a series of open-top chamber (OTC) experiments were conducted to asses whether measured exogenous-toxin quantity is reduced in transgenic Bt cotton and rice due to increased plant biomass under elevated atmospheric CO2. This study also examines the effectiveness of Bt cotton and rice transgenes against H. armigera and C. suppressalislarvae respectively. The study showed that there are significant differences between the exogenous-toxin levels of Bt cotton and rice under increased CO2and both showed differences in toxin quantity among developmental stages. Also, the new properties of Bt crops under elevated CO2 significantly affected the performance of H. armigeraand C. suppressalis larvae, despite the adverse effects of Bt gene expression in elevated CO2conditions.—Taylor Jones
Chen, F., Wu, G., Ge, F., Parajulee, M. N., 2011. Relationships between exogenous-toxin quantity and increased biomass of transgenic Bt crops under elevated carbon dioxide. Ecotoxicology and Environmental Safety 74, 1074–1080.

          Chen and colleagues performed a series of OTC experiments with ambient (375μl/L) and elevated (750μl/L) CO2  conditions that were maintained via a continuous automatic control system. Thirty-six pots of transgenic Bt cotton and twenty-six pots of transgenic Bt rice were planted and their positions were randomized each day to limit positional effects in the OTC chambers. In select plots, cotton bollworm (H. armigera) and rice stem borer C. suppressaliswere added to examine the effects of pest larvae on Bt cotton and rice. Biomass index was used to determine the increased amount of biomass under elevated CO2conditions and plant tissues were tested for exogenous-toxin quantity. Chen et al. recognize the potential “dilution effect” in which percent biomass increase exceeds the percent increase in exogenous-toxin increase, resulting in decreased levels of exogenous-toxin.
          The results show that increasing CO2levels significantly increased leaf, petiole, shoot and total plant biomass production of 45-DAS (“days after seedling”) Bt cotton as well as increases in shoot and total plant biomass production in 90-DAS cotton. Similar trends resulted for Bt rice as root, above-ground, and total stem biomass increased in 50-DAS rice and root tissues increased in 100-DAS rice. Overall, elevated levels of CO2 led to increased biomass in Bt cotton and rice, as predicted by previous studies showing increased photosynthesis and growth rates.
          Elevated CO2 conditions significantly reduced exogenous-toxin content in both Bt cotton and rice tissues. However, the effect of CO2 level on exogenous-toxin amount varied among crops and their respective plant tissues. For example, increased CO2 significantly reduced exogenous-toxin content per plant in 45-DAS and 90-DAS Bt cotton, while simultaneously increasing exogenous-toxin content in the stems of 50-DAS Bt rice. This shows that the responses of transgenic Bt cotton and rice (relating to exogenous-toxin content) to increased ambient CO2 are different. Also, each plant exhibited different responses in different phases of development. Chen and colleagues compared percent changes in biomass and exogenous-toxin levels and concluded that a dilution effect exists in shoot and petiole tissues of 45-DAS Bt cotton and in root, above-ground, and total stem tissues of 50-DAS Bt rice as well as leaf sheaths of 100-DAS rice. This is probably related to increased plant nitrogen-use efficiency and the authors predict that increased plant carbohydrate concentration diluted Bt proteins. For other increases in exogenous-toxin levels, the authors conclude that the dilution effect is only partly responsible and the reduction is due to reduced expression of the Bt gene under increased CO2 conditions.
          The results also suggest that most H. armigera larvae preferred to feed on transgenic Bt cotton squares and bolls, and most C. suppressalis larvae preferred to feed upon leaf sheaths of transgenic Bt rice. These areas of the Bt crops correlate with decreases in exogenous-toxin production, as expected. Although feeding increased in certain areas, the study found overall decreases in larval survival rate and pupal weight of H. armigera and C. suppressalis, suggesting that the Bt cotton and rice in this study to not face serious risks of reduced efficiency against pests in increased CO2 conditions.

Estimated Magnitude of Persistent Carbon Sink in World’s Forests

Forests are important in absorbing a significant amount of CO2 in the earth’s atmosphere. It is necessary to understand how much of an effect they have in order to set limitations on greenhouse gas emissions and better understand the effects of climate change. The Intergovernmental Panel on Climate Change (IPCC) reports a wide range of data on the C uptake by terrestrial ecosystems, stating that uptake could range from less than 1.0 to 2.6 Pg per year. More recent models on climate change report a C sink range of 2.0 to 3.4 Pg per year. Understanding and constraining these limitations is crucial in understanding the future effects of climate change. In this report, the authors carried out a bottom-up estimation of C stocks and changes based on recent data and long-term field observations coupled with statistical modeling. The C pools in forest include measurements from dead wood, harvested wood, living biomass, litter, and soil. Data from different countries, regions, and continents was compared to understand trends across geographic boundaries. The area examined contains 3.9 billion ha, which accounts for 95% of the world’s forests. —Taylor Jones
Pan, Y., Birdsey, R. A., Fang, J., Houghton, R., Kauppi, P. E., Kurz, W. A., Phillips, O. L., Shvidenko, A., Lewis, S. L., Canadell, J. G., Ciais, P., Jackson, R. B., Pacala, S. W., McGuire, A. D., Piao, S., Rautiainen, A., Sitch, S., Hayes, D., 2011. A Large and Persistent Carbon Sink in the World’s Forests. Science 333, 988-993.

          Yude Pan and colleagues report the estimated amount of carbon stock in the world’s forests at 861 ± 66 Pg C of which 44% resides in soil, 42% in live biomass, 8% in dead wood, and 5% in litter. Breaking down the C sink by types of forests, tropical forests account for 471 ± 93 Pg C, boreal forests 272 ± 23 Pg C, and temperate forests 119 ± 6 Pg C. Tropical and boreal forests store most of the earth’s carbon, however tropical forests have 56% in above ground biomass and boreal forests only have 20% in above ground biomass. This difference is crucial in determining what precautions should be taken to preserve certain parts of forests in different regions. The annual change in C stock shows an uptake of 2.5 ± 0.4 Pg C per year for 1990 to 1999 and 2.3 ± 0.5 Pg C per year from 2000 to 2007. Despite the overall C uptake in these two time periods, regional differences are apparent. For example, temperate forests increased C sink by 17% more from 2000 to 2007 compared to 1990 to 1999, while tropical forests decreased C sink by 23% during the same time period. By subtracting the C sink losses from forest degradation in tropical areas, the net forest C sink is estimated at 1.0 ± 0.8 and 1.2 Pg C per year from 1990 to 1999 and 2000 to 2007, respectively.
          Examining C sink by region and biome, boreal forests had an estimated C sink of 0.5 ± 0.1 Pg C per year for the past two decades. Some regions, such as Asian Russia, account for a significant portion of the total sink, but experienced no overall change. Other areas, like European Russia, experienced a 35% increase in C sink. The authors suggest this increase could be due to increased forest area after agricultural abandonment, reduced harvesting or several areas of forest progressing to later stages in the plant life cycle. The C sink in Canadian forests reduced by half during the same time period, largely due to wildfires and insect outbreaks. As a result of the increases and decreases mentioned above, the overall C sink did not experience a net change.
          Temperate forests contributed 0.7 ± 0.1 and 0.8 ± 0.1 Pg C per year for the past two decades. This increase in C sink is likely due to increases in density of forest biomass and an increase in forest area. The C sink in the U.S. on average increased by 33% during this time period due to the growth of forest area resulting from previous agriculture and harvesting. However, the western U.S. has experienced forest mortality due to drought stress, insects, and fires. The C sink in Europe remained constant, but the C sink in China increased by 34%, likely due to newly planted forest area and reforestation programs.
          Tropical forests account for about 70% of the world’s forests and in this study, the authors collected data from intensive monitoring of Africa and South America, and used these trends to estimate the data for Southeast Asia. The total C sink in tropical forests is estimated at 1.3 ± 0.3 and 1.0 ± 0.5 Pg C per year for the past two decades. The total C sink during this time period accounts for about half of the total C sink. Tropical land use, including clearing forests for agriculture, timber and pasture areas, accounts for a carbon release second to the amount produced by fossil fuels. Deforestation accounted for about 40% of global fossil fuel emissions in the past two decades, but this is often overlooked because it was offset by a large uptake in C due to forest regrowth. Pan and colleagues estimate that C uptake was stronger in regrowth forests compared to previously intact forests due to simultaneous rapid increases in biomass. The authors also suggest that the state tropical forests has a significant impact on total C sink and better monitoring techniques and increased understanding of C cycling in these areas should be a priority in the future.
          Dead wood, litter, soil, and harvested wood account for about 35% of the world’s forest C sink and are important factors that should not be overlooked, however they remain the most difficult to measure. This measurement could also be too low as it does not include deep soil beyond 1 meter and improved measuring techniques would be necessary to account for this. Dead wood is more vulnerable to fires than other sources of C and harvested wood in boreal areas experienced a decrease over the past two decades, mainly due to decreased Russian harvesting.
          Pan and colleagues recognize critical data gaps in their study including a substantial lack of data for North America (mainly Canadian unmanaged forests and Alaska), and for the C flux in tropical forests, which may account for a 10–20% error in estimates. The authors suggest that in order to attempt to combat these uncertainties, land monitoring should be increased, globally consistent land-sensing is necessary, and scientists need better tools to measure below ground, dead wood and litter sources of C.
          Forests have a crucial role in absorbing atmospheric C and will continue to maintain strong control over atmospheric CO2 levels. The factors that affect C levels in the atmosphere are complex and it is necessary to adopt better monitoring systems to separate their impacts and determine the effects of climate change. The authors note that although a large amount of CO2 humans place in the atmosphere is sequestered by forests, deforestation significantly contributes to C losses and relying on forests to absorb C is not without risk.

Negative Effects of Increased Temperature and O3 Offset Positive Effects of CO2 in Oilseed Rape (Brassica napus L.)

CO2 in the atmosphere is steadily increasing and is predicted to be 500–1000 ppm by the end of the century. Emissions of other greenhouse gases are also increasing and are expected to raise the surface temperature 1.8–4.0o C, along with increasing emissions of ozone (O3) from human activity. These forces, and many others, naturally act together and have an important effect on agricultural productivity and climate change. It is more useful and practical to study the effects of multiple, layered factors of climate change than to study one factor in isolation. For example, increased CO2 alone will increase the photosynthetic rate in plants, increasing biomass production, and result in positive growth for plants. However, this increase in biomass does not necessarily lead to an increase in crop yield. It is important to combine and test the effects of various factors of climate change on crops to determine potential crop yield because with a growing human population, maximizing crop yield is highly desirable. Plants do not have many natural adaptations for living in conditions with increased CO2, so it is important to study how they react in order to better breed and genetically prepare plants for climate change.—Taylor Jones
Frenk, G., Van der Linden, L., Mikkelsen, T. N., Brix, H., Jorgensen, R. B., 2011. Increased [CO2] does not compensate for negative effects on yield caused by higher temperature and [O3] in Brassica napus L. European Journal of Agronomy 35, 127–134.

          Frenk and colleagues controlled the ambient conditions of four cultivars of oilseed rape (Brassica napus L.) of different ages and origins and exposed each cultivar to a different combination of increased CO2 (700 ppm), increased temperature (+5oC), and increased O3 (60 ppb). The plants were raised in growth chambers and at the end of maturation, ten plants from each cultivar were selected at random to study. The pod, stem height, and stem width were recorded along with seed yield, stem weight, and biomass. The Thousand Seed Weight (TSW) and Harvest Index (HI) were determined for each sample.
          Increased temperature alone generally reduced the seed yield by 38–58%, the total number of seeds, and the mass of seeds and pods. Despite these general trends, variability among cultivars only produced a significant difference in seed yield for two of them. Stem biomass was not significantly different with increased temperature, and only one cultivar showed a difference in stem weight. The low total seed yield also reduced the HI. The authors predict the decrease in biomass typically associated with increased temperatures is due to reduced rates of photosynthesis, quick development, increased respiration, and decreased organ development. Plant breeding today is often focused on yield, so these new plants will likely be the most susceptible to climate change and the negative effects of increased temperature.
          Increased CO2 alone resulted in a general increase in total seed yield (only significant for one plot) and the total number of seeds. Stem height increased for all cultivars and biomass increased in general, but was only significant for one cultivar. Frenk et al. predict that the effects of increased CO2 can be offset over time because the plant does not have enough storage organs and has reduced carbon sink capacity.
          Increased O3 alone had no effect on plant yield or stem weight, but combined with temperature, O3further reduced the positive effects of increased CO2, and further decreased yield. When CO2 and temperature both increased, they equalized the effects of one another and the sample resembled the control in biomass growth and yield. According to Frenk and colleagues, no study to date has examined the combined effects of the three factors discussed above on agricultural productivity and the results show significant changes in agricultural productivity and should be combined with more abiotic and biotic factors in the future to determine the full effects of increased CO2.

Elevated CO2 Leads to Long-Term Forest Productivity and Increases in Carbon Flux

With rising levels of atmospheric CO2 due to climate change, the earth is becoming more dependent on changes in ambient air composition and its effect on plant growth and productivity. Recent studies have shown significant variety in ecosystem responses to enriched CO2 environments and only some studies demonstrated increased rates of NPP. In the following experiment, Drake et al. (2011) examine the physiological responses of loblolly pine (Pinus tadea) trees to increased CO2 and determine the effects on nutrient availability and uptake. The experiment was performed on the grounds of Duke’s FACE program and the authors collected data on a variety of physiological plant factors in ambient and enriched CO2 to determine if the information from this testing site can be applied to other ecosystems. It was predicted that increases in carbon flux, nitrogen-uptake and overall plant productivity would lead to long-term forest enrichment. —Taylor Jones
Drake, J. E., Gallet-Budynek, A., Hofmockel, K.S., Bernhardt, E. S., Billings, S. A., Jackson, R. B., Johnsen., K. S., Lichter, J., McCarthy, H. R., McCormack, M. L., Moore, D. J. P., Oren, R., Palmroth, S., Phillips, R. P., Pippen, J. S., Pritchard, S. G., Treseder, K. K., Schlesinger, W. H., DeLucia, E. H., Finzi, A. C., 2011. Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecology Letters 14, 348–357.

          John E. Drake and colleagues started the experiment with 3-year-old loblolly trees planted 2.4 by 2.4 meters apart. In 1994, they began collecting data on the paired reference plots and in 1996, began collecting data in all additional plots. Some data was taken from previous research at the FACE testing site and some data was new for this experiment. The standing pool of fine root biomass was measured every three months by collecting a 4.65 cm block of soil 15 cm deep and analyzing it for C content. The amount of C stored as CO2 in the soil air space was calculated and the microbial biomass of N was measured.
          The rate of CO2 diffusion out of the soil (soil CO2 efflux) was measured with the closed IKGA system and the data were plotted as a temperature response curve. The fine root production was measured monthly and the production of various fungi was measured using microscopic methods. The on-site litterfall was collected monthly January–September and biweekly October–December in 12 baskets per site, measuring 0.218m2 each. The authors also collected data on C-cycling, NPP and total belowground carbon flux (TBCF).
          The results showed that as CO2increased, the rate of C-cycling through the soil increased by 17%. Also, the TBCF increased 16% and the increased C entering the soil in an enriched CO2  environment led to increases in the net biomass. N also increased, supporting an increase in NPP, supplied by a 25% increase in soil uptake. TBCF and N-uptake demonstrated an inverse relationship. NPP positively correlated with canopy N content and supported an increase in photosynthetic N-use efficiency.
          Drake et al. suggest that the increase in productivity is due to an exchange of tree C with soil N belowground, allowing the N levels to meet the growth requirements of the plant. Also, the long-term NPP increases are likely enabled by increases in TBCF that stimulate N-uptake and  canopy leaf area. Despite increased productivity, the experiment did not result in a net accumulation of  C in the mineral soil pool. The authors suggest this could be a result of the fixed C being added to the experiment replacing some of the C initially present in the soil and increases in microbial activity could account for changes in the soil composition. This effect on C pools is likely to model the response of soil to a long-term rise in CO2. The authors recognize that this study provides an initial attempt to examine the physiological effects of increases CO2, but is by no means comprehensive and further experiments representing a diversity of effects are necessary to better understand the long-term effects of increased CO2. A simple experimental framework describing the most important processes that effect N availability and C uptake is necessary to understand the effects of CO2 enrichment in the future.

Increased Soil Emissions of Potent Greenhouse Gases under Increased Atmospheric CO2

 Burning fossil fuels and frequently changing land use contribute to rapidly increasing atmospheric CO2 levels. An increase in CO2 can alter both abiotic and biotic conditions of soil and affect the levels of other important greenhouse gases (GHG) such as nitrous oxide (N2O) and methane (CH4). Several previous studies have shown that increased CO2 levels could slow climate change by increasing plant efficiency and soil carbon input and storage, however CO2 should not be examined alone because other gases also have high global warming potentials. For example, N2O  and CH4 have global warming potentials 298 times higher and 25 times higher respectively than that of CO2. In this study, Van Groenigen et al. (2011) examined the effects of increased atmospheric CO2 on N2O levels in upland soil and CH4 levels in rice paddies and natural wetlands and concluded that changes in these greenhouse gases can greatly affect how ecosystems influence climate change.—Taylor Jones
Van Groenigen, K. J., Osenberg, C. W., Hungate, B. A., 2011. Increased soil emissions of potent greenhouse gases under increased atmospheric CO2. Nature 475, 214–216.

          Kees Jan van Groenigen and colleagues completed a meta-analysis on 152 observations from 49 published studies to examine fluxes of CH4 and N2O in the presence of increased CO2. GHG emissions span a variety of ecosystems and the compiled meta-analysis, compared to an individual experiment, provides a more comprehensive study. The increased CO2 stimulated N2O  emissions in uplands by 18.8% and stimulated CH4 in wetlands by 13.2% and in rice paddies by 43.4%. The authors also examined the effect of increased CO2 on the possible causes for these changes in GHG emissions, soil water content and root biomass. Combining all three types of terrain, soil water content increased 6% and root biomass increased 18%.
          The authors also investigated the importance of the changes in GHG levels on fertilized (agricultural) and non-fertilized (natural) land. The model was tested on current CO2levels to confirm the accuracy of the scaling approach. NO2 stimulation in agricultural uplands indicated an increased 0.33 Pg CO2equivalents per year and an increased 0.24 Pg CO2 equivalents per year in natural areas. CH4 stimulation in agricultural rice paddies indicated an increased 0.25 Pg CO2 equivalents per yearand an increased 0.31 Pg CO2 equivalents per year in natural wetlands. In addition, carbon sink was larger for fertilized areas and GHG emissions could cancel the expected increase in carbon sink by 16.6%, based on the authors’ calculations.
          Van Groenigen and colleagues present three reasons that suggest this increase of carbon sink could be an underestimate because first, the majority of data collected during the growing season and some terrains have higher N2O emissions during the winter that could add up to 7% more N2O. Second, N2O emissions increased in studies that included additional nitrogen, so as nitrogen increases along with CO2, N2O levels may also increases. Last, the authors noticed a weak correlation between experiment duration and so the effect of CO2 is likely to increase over time.
          Increased CO2 levels stimulate denitrification, a major contributor to N2O levels in upland soil and in wetlands and rice paddies of various geographic regions, methanogenic archaea rely heavily on carbon levels as a source of organic substrates and with increased CO2 levels, more CH4 is produced. This study shows that not only do increased CO2 levels amplify climate change, but the increase of N2O in uplands and CH4 in wetlands and rice paddies could negate carbon sink percentages and further studies should consider the indirect effects of these other greenhouse gases on climate change.

Interspecific Effects of Elevated CO2 on Seed Production in C3 Plants

Atmospheric CO2 was estimated to be 280µmol mol-1 before the industrial revolution era and is currently estimated at 390µmol mol-1with predictions to increase in the future. Several vital plant functions, such as photosynthesis, transpiration, and biomass are affected by increases in atmospheric CO2 levels. For wild plants, seed quantity and quality influence their fitness and seed production, and in the presence of elevated CO2, this varies considerably among species of C3 annual plants. In this study, Hikosaka et al. perform a meta-analysis to examine whether seed production is limited by nitrogen availability or concentration. In general, studies have shown that increased ambient CO2 leads to increased N per plant and increased seed production, as seed mass per plant has increased by 28–35%. However, this study shows that various species respond differently, and understanding these differences is important to maintaining C3 plant productivity in an enriched CO2 world. The authors predict that the N contained in reproductive organs accounts for the variation in the increased CO2 response of seed production.—Taylor Jones
Hikosaka, K., Kinugasa, T., Oikawa, S., Onoda, Y., Hirose, T., 2011. Effects of elevated CO2 concentration on seed production in C3 annual plants. Experimental Botany 62, 1523-1530.

          Kouki Hikosaka and colleagues performed a meta-analysis to examine the variation of seed production in annual C3 plants under increased CO2 concentrations. The enhancement ratio of seed mass per plant due to increased CO2 was 0.75–4.45 for rice, 0.93–1.87 for soybean, and 0.88–2.07 for wheat, but these differences could be attributed to different growth conditions. The authors also determined that seed production is not linked to change in total plant biomass. For example, a study cited by Jablonski et al. reported increases in fruit and seed yield of 12% and 25% respectively with a 31% increase in total plant mass. CO2 responses also differ between reproductive tissues in different species. The boll yield of cotton increased by 40% and lint increased by 54%. Studies also demonstrate an increase in pod wall mass of soybeans and greater increases in mass of reproductive structures of Xanthium canadense in low N environments compared to high N environments.
          Hikosaka and colleagues also examined N use in reproductive growth and CO2 response and hypothesized that the differences in response to increased CO2 are either a result of different limiting factors (such as CO2 or N) or a constant N limitation. Compilations of studies showed that the seed mass of C3plants grown at varying levels of CO2 was not correlated with N concentration, but rather demonstrated a 1:1 correlation between seed mass per plant and N per plant. This supports the second hypothesis that seed production is only enhanced when N is more readily available.
          Seed N levels experienced variation in some species more than others and may be enhanced in some plants by absorbing more during growth or retranslocating N from vegetative to reproductive organs. The N-fixing legumes showed the greatest N enhancement, but significant variation in other areas such as biomass, photosynthetic rates, and leaf-area index. In several studies, the N concentration in seeds remained the same while vegetative N concentrations decreased, showing that the vegetative organs are less conservative. The authors also examined seed N per plant and seed N concentration of three species: grass, legumes, and non-legume dicots. The studies showed increases in seed mass per plant in the presence of elevated CO2 and increases in seed N per plant for legume species.
          Three quarters of variation in seed-mass enhancement was attributed to increases in seed N per plant, while  one quarter was attributed to reductions in N concentration. The reduction of N concentration was noticed most in legumes, and not as much in the other species. Also, in several grass species, the presence of albumen allowed storage of high amounts of carbohydrates while N levels were low.
          Overall, N limitation is key to understanding seed production and responses in elevated CO2 environments. Plants experience increased seed production when they undergo increased N acquisition or decreased N concentration. Legumes are N-fixing and grasses often experience increases in seed production through increases in N acquisition and decreases in N concentration. Decreases in N concentration may not decrease the quality of the seeds if it results from increased albumen content without reduced N in embryos.

The Combined Effects of Increasing Temperature and CO2 on the Growth of C3 and C4 Annual Species

With CO2 levels predicted to rise in the future, several recent experiments have investigated the effects of increasing CO2 on plant growth and development. Studies on cool weather  C3 annual plants have demonstrated enhanced photosynthesis under elevated CO2 when other environmental factors remain constant. The ability to increase growth under elevated CO2 could be very beneficial for C3 crops, enhancing productivity and increasing yield. Warm weather C4 annual plants have generally been less responsive to increases in atmospheric CO2 levels, demonstrating similar levels for photosynthesis at various levels of CO2. However, studies have shown that increases in both temperature and CO2, a more realistic scenario, demonstrate an ecological advantage for C4 plants as the advantages of C3 plants decline with an increase in temperature. Rising CO2 is also expected to significantly affect the reproductive structures of both C3 and C4 plants, due to high temperature shocks during fertilization, inhibiting vital growth stages. Despite increasing literature on the effects of climate change on plants, few studies have examined the impacts of increased temperature and elevated CO2on weedy plants or grasses. In this study, Lee examined the effects of increased temperature, and increased temperature with elevated CO2on two annual species of C3 and C4 plants, Chenopodium album and Setaria viridis respectively. The author found that elevated temperature significantly                                                                                                                                                                                                                                                                                                                                                                                                                                                                              affects the biomass production in the reproductive stages and this effect may be enhanced for C3 plants. However, the disadvantages of warming are countered in the presence of elevated CO2 in C3 plants.—Taylor Jones
Lee, J.S., 2011. Combined effect of elevated CO2 and temperature on the growth and phenology of two annual C3 and C4 weedy species.  Agriculture, Ecosystems and Environment 140, 484-491.
          Lee assembled three experimental plots subjected to varying condition, the first being a control with ambient CO2and temperature. The second plot (T4) was subjected to a 4°C increase in temperature with ambient CO2 and the third plot (CT4) was subjected to a 4°C increase in temperature along with 1.8 times the ambient CO2level. The plots were rotated to minimize the effects of inadvertent variations in light, air temperature, and CO2 concentration. The biomass of the plants was estimated using the plant size index and was measured at two week intervals throughout the growing period. Leaf area and photosynthesis rates were also recorded. Emerging seedlings and flower number were counted after at least one seedling shoot extended 0.2 cm.
          Throughout this study, Lee found that seedling emergence and flowering times in C3 and C4plants were significantly advanced under T4 and CT4 conditions compared to the control, however the differences between these two conditions was relatively small. The date of emergence of C. albumseedlings was 27.0 and 24.3 days early in T4 and CT4 plots respectively, compared to the control. Also, the length of the flowering time increased significantly in T4 and CT4 scenarios compared to the control in S. viridis, but not in the C3plant. Lee concluded that since most of the differences were between the control and T4 or CT4 plots, plant phenology is likely affected more by the increase of temperature than the elevation of CO2. Also, the seedling emergence time of S. viridiswas more sensitive to increased temperature than that of C. album which could lead to serious implications for population establishment when seeds are competing for resources and space. The author concludes that C4 plants will have an advantage in this scenario due to the increased sensitivity to temperature.
          Throughout the growth stages, the mean temperatures in the plots subjected to elevated temperature remained approximately equal, indicating that the temperatures during critical growth stages were about the same for C3 and C4 plants. The changes in temperature were accounted for by advancing plant phenology. However, these conditions of ideal light and temperature are not realistic and changing plant phenology also affects the solar radiation intensity. Lee determined that accumulated solar radiation decreased by 19% and 16.1% in C3 and C4 plants respectively in T4 conditions and this decrease in solar radiation led to decreases in biomass production. It is likely that these decreases in biomass production would be compensated for in an increased temperature and CO2 environment.
          The effect of elevated CO2seemed to be greater when coupled with increases in temperature, which led to a significant increase in photosynthesis in C3 plants. In this study, elevated CO2 levels and temperature increased the rate of photosynthesis in C3 plants and increased biomass production when compared to ambient conditions. Increased temperature did not significantly affect the biomass production of C4 plants, maintaining their advantage in T4 and CT4 conditions as a result of resistance to increasing temperature and CO2. Based on this study, C3 plants are predicted to have an advantage under future global warming conditions as they can avoid the detrimental effects of high temperatures during the vegetative growth stage by flourishing under increased CO2

Increased Atmospheric CO2 Levels and Warmer Weather Prevent Desiccation in C4 Grassland

Grasslands and dry rangelands cover over 30% of the Earth’s terrestrial surface and increased population growth is limiting the natural soil water supply in these areas. Changes in soil water supply depend on precipitation, temperature, CO2 concentration, and various soil properties. Most of the world’s livestock depend on this supply of grasslands to eat and survive, and climate change, including increased temperatures and CO2 concentrations, may affect grass productivity. As CO2 concentration increases, stomatal closure also increases allowing plants to retain more water and increase water-use efficiency. However, this increased efficiency may be due to increase overall biomass of the canopy level that results from an increase in CO2. Most grasslands contain both C3 and C4 photosynthetic categories of plants and in the Prairie Heating and CO2 Enrichment (PHACE) experiment reported here, Morgan et al. (2011) examined changes in plant productivity and soil water content in response to increases in CO2. They concluded that increased CO2 concentrations offset deleterious effects of increased temperature, maintaining soil water content at levels that occur today and increasing productivity in C4 plants.—Taylor Jones
Morgan, J., LeCain, D., Pendall, E., Blumenthal, D., Kimball, B., Carrillo, Y., Williams, D., Heisler-White, J., Dijkstra, F., West., M., 2011. C4 grasses prosper as carbon dioxide eliminates desiccation in warm semi-arid grassland. Nature 476, 10274-10279.

          Jack A. Morgan and colleagues created the PHACE experiment to evaluate the responses of native mixed-grass prairie to one year of increased CO2 exposure and to a three year period of combined CO2  exposure and increased temperatures. In 2006, the ambient CO2 concentration was measured at the ambient level of 385 ppmv. It was experimentally increased to 600 ppmv. From 2007—2009, the temperature was increased by 1.3/3.0o C (day/night) in the canopy. The free-air CO2 enrichment (FACE) was used to alter air composition and the T-FACE system was used to alter the temperature. The authors found that increased temperature and increased CO2 concentration had opposite effects on soil water content (SWC). As CO2 increased, SWC also increased by 17.3%, as predicted by the increased water efficiency due to more closed stomata. However, as the temperature increased, SWC decreased by 13.1%. There was no difference between the control (15.5%) and the combined increased temperature and increased CO2 plot, suggesting that the water conservation effects of increased CO2 cancel out the drying effects of warmer temperatures.
          Using the same experimental design, the authors investigated the effects of increased CO2  concentration and increased temperature on above-ground biomass (AGB) and below-ground biomass (BGB), both estimates of a plant’s productivity and growth. As expected, the prairie exposed to increased levels of CO2 increased the amount of above-ground biomass by an average 33% over the first three years, supporting the benefits of CO2 enrichment on plant productivity and growth. The same positive effect of increased CO2 concentration appeared for the growth in roots composing the BGB. To continue the study of the effects of increased CO2 on SWC and plant productivity, Morgan et al. examined how these changes in AGB related to the soil matric potential (energy of soil water per unit volume) using the biomass enhancement ratio. A strong negative correlation between the soil matric potential and the biomass enhancement ratio resulted and is likely due to the increased water efficiency under conditions of high CO2 concentrations and shows that increased CO2 concentration will increase productivity when water is limited. Morgan et al. also compared the results of this portion of the experiment with results from other similar areas of the Great Plains.
          Through these experiments, the authors distinguished significant differences between C3 and C4grasses. C3 grasses showed 34% more growth during increased CO2conditions, but increases in temperature did not have an effect. C4 grasses showed 28% more growth during increased CO2 conditions but also increased growth during warming, suggesting that C4 grasses could be more productive in future atmospheric conditions of high CO2 and increased temperature. The results also suggest that increased CO2 concentration may counter the effects of extreme dryness due to increased temperatures in the future. The authors also created a model analysis that changed the canopy resistance to water loss (change in stomatal closure) through various temperatures and recorded the effects on the evapotranspiration rate (the combined rate of evaporation and transpiration of the prairie). The results showed that the temperature effect and the increased CO2 effect almost exactly offset one another. Despite this trend, the authors predict the efficiency advantages of increased CO2 will not be able to offset extreme drought conditions and regions like southwestern North America or the Mediterranean may not benefit from these effects. The results from this experiment only show one example of the benefits of increased CO2  in a semi-arid plant community, but it is clear that under certain circumstances, increased CO2 concentration can increase plant efficiency and water use. 

Increased Atmospheric CO2 Levels and Warmer Weather Prevent Desiccation in C4 Grassland

Grasslands and dry rangelands cover over 30% of the earth’s terrestrial surface and increased population growth is limiting the natural soil water supply in these areas. Changes in soil water supply depend on precipitation, temperature, CO2 concentration, and various soil properties. Most of the world’s livestock depend on this supply of grasslands to eat and survive, and climate change, including increased temperatures and CO2 concentrations, may affect grass productivity. As CO2 concentration increases, stomates need not open as long, allowing plants to retain more water and increase water-use efficiency. However, this increased efficiency may be due to increase overall biomass of the canopy level that results from an increase in CO2. Most grasslands contain both C4 and C3 photosynthetic categories of plants and in the Prairie Heating and CO2 Enrichment (PHACE) experiment reported here (2011), Morgan et al. examined changes in plant productivity and soil water content in response to increases in CO2. They concluded that increased CO2 concentrations offset deleterious effects of increased temperature, maintaining soil water content at levels that occur today and increasing productivity in C4 plants .—Taylor Jones
Morgan, J., LeCain, D., Pendall, E., Blumenthal, D., Kimball, B., Carrillo, Y., Williams, D., Heisler-White, J., Dijkstra, F., West., M., 2011. C4 grasses prosper as carbon dioxide eliminates desiccation in warm semi-arid grassland. Nature 476, 10274–10279.

          Jack A. Morgan and colleagues created the PHACE experiment to evaluate the responses of native mixed-grass prairie to one year of increased CO2  exposure and to a three year period of combined CO2  exposure and increased temperatures. In 2006, the ambient CO2 concentration was measured at the ambient level of 385 p.p.m.v. It was experimentally increased to 600 p.p.m.v. In 2007–2009, the temperature was increased by 1.3/3.0o C (day/night) in the canopy. The free-air CO2 enrichment (FACE) was used to alter air composition and the T-FACE system was used to alter the temperature. The authors found that increased temperature and increased CO2 concentration had opposite effects on soil water content (SWC). As CO2 increased, SWC also increased by 17.3%, as predicted by the increased water efficiency due to more closed stomata. However, as the temperature increased, SWC decreased by 13.1%. There was no difference between the control (15.5%) and the combined increased temperature and increased CO2 plot, suggesting that the water conservation effects of increased CO2 cancel out the drying effects of warmer temperatures.
          Using the same experimental design, the authors investigated the effects of increased CO2  concentration and increased temperature on above-ground biomass (AGB) and below-ground biomass (BGB), both estimates of a plant’s productivity and growth. As expected, the prairie exposed to increased levels of CO2 increased the amount of above-ground biomass by an average 33% over the first three years, supporting the benefits of CO2 enrichment on plant productivity and growth. The same positive effect of increased CO2  concentration appeared for the growth in  roots comprising the BGB. To continue the study of the effects of increased CO2 on SWC and plant productivity, Morgan et al. examined how these changes in AGB related to the soil matric potential (energy of soil water per unit volume) using the biomass enhancement ratio. A strong negative correlation between the soil matric potential and the biomass enhancement ratio resulted and is likely due to the increased water efficiency under conditions of high CO2 concentrations, showing that increased CO2 concentration will increase productivity when water is limited. Morgan et al. also compared the results of this portion of the experiment with results from other similar areas of the Great Plains.
          Through these experiments, the authors distinguished significant differences between C3 and C4grasses. C3 grasses showed 34% more growth during increased CO2conditions, but increases in temperature did not have an effect. C4 grasses showed 28% more growth during increased CO2 conditions but also increased growth during warming, suggesting that C4 grasses could be more productive in future atmospheric conditions of high CO2 and increased temperature. The results also suggest that increased CO2 concentration may counter the effects of extreme dryness due to increased temperatures in the future. The authors also created a model analysis that changed the canopy resistance to water loss (change in stomatal closure) through various temperatures, and recorded the effects on the evapotranspiration rate (the combined rate of evaporation and transpiration of the prairie). The results showed that the temperature effect and the increased CO2 effect almost exactly offset one another. Despite this trend, the authors predict the efficiency advantages of increased CO2 will not be able to offset extreme drought conditions and regions like southwestern North America or the Mediterranean may not benefit from these effects. The results from this experiment only show one example of the benefits of increased CO2  in a semi-arid plant community, but it is clear that under certain circumstances, increased CO2 concentration can increase plant efficiency and water use.