Other benefits of carbon dioxide
From ClimateWiki
From Climate Change Reconsidered, a work of the Nongovernmental International Panel on Climate Change
Other benefits to plants of CO2 enhancement documented in this section include superior nitrogen-use efficiency, increased nutrient acquisition, greater resistance to pathogens and parasitic plants, greater root development, greater seed and tannin production, and improved performance of transgenic plants. In addition to these benefits to plants, CO2 enrichment benefits all life on earth by reducing plant emissions of isoprene, a chemical responsible for the production of tropospheric ozone.
Contents |
Nitrogen-Use Efficiency
Long-term exposure to elevated atmospheric CO2 concentrations often, but not always, elicits photosynthetic acclimation or down regulation in plants, which is typically accompanied by reduced amounts of rubisco and/or other photosynthetic proteins that are typically present in excess amounts in plants grown in ambient air. As a consequence, foliar nitrogen concentrations often decrease with atmospheric CO2 enrichment, as nitrogen is mobilized out of leaves and into other areas of the plant to increase its availability for enhancing sink development or stimulating other nutrient-limited processes.
In reviewing the literature in this area, one quickly notices that in spite of the fact that photosynthetic acclimation has occurred, CO2-enriched plants nearly always display rates of photosynthesis that are greater than those of control plants exposed to ambient air. Consequently, photosynthetic nitrogen-use efficiency, i.e., the amount of carbon converted into sugars during the photosynthetic process per unit of leaf nitrogen, often increases dramatically in CO2-enriched plants.
In the study of Davey et al. (1999), for example, CO2-induced reductions in foliar nitrogen contents and concomitant increases in photosynthetic rates led to photosynthetic nitrogen-use efficiencies in the CO2-enriched (to 700 ppm CO2) grass Agrostis capillaris that were 27 and 62 percent greater than those observed in control plants grown at 360 ppm CO2 under moderate and low soil nutrient conditions, respectively. Similarly, elevated CO2 enhanced photosynthetic nitrogen-use efficiencies in Trifolium repens by 66 and 190 percent under moderate and low soil nutrient conditions, respectively, and in Lolium perenne by 50 percent, regardless of soil nutrient status. Other researchers have found comparable CO2-induced enhancements of photosynthetic nitrogen-use efficiency in wheat (Osborne et al., 1998) and in Leucadendron species (Midgley et al., 1999).
In some cases, researchers report nitrogen-use efficiency in terms of the amount of biomass produced per unit of plant nitrogen. Niklaus et al. (1998), for example, reported that intact swards of CO2-enriched calcareous grasslands grown at 600 ppm CO2 attained total biomass values that were 25 percent greater than those of control swards exposed to ambient air while extracting the same amount of nitrogen from the soil as ambiently grown swards. Similar results have been reported for strawberry by Deng and Woodward (1998), who noted that the growth nitrogen-use efficiencies of plants grown at 560 ppm CO2 were 23 and 17 percent greater than those of ambiently grown plants simultaneously subjected to high and low soil nitrogen availability, respectively.
In an additional study, McCalley et al. (2011) set out to determine wither changes in atmospheric CO2 enrichment would alter nitrogen gas emissions. Working at the Nevada Desert FACE Facility northwest of Las Vegas, Nevada (USA), McCalley et al. measured soil fluxes of reactive N gases (NO, NOy, NH3) and N2O in plots receiving long-term fumigation with ambient (380 ppm) and elevated (550 ppm) CO2. Begun in April 1997, nitrogen gas flux measurements were taken several times from 2005 to 2007, as well as after termination of CO2 fumigation in 2007 and 2008.
The researchers report that "long-term exposure to elevated CO2 decreased reactive N gas emissions from Mojave Desert soils," especially "in the spring and fall when recent precipitation, either natural or artificial, created soil conditions that are optimal for biological activity." Emissions of N2O, on the other hand, were "a very small component" of gaseous N loss and were "largely insensitive to elevated CO2."
The insensitivity of N2O emissions to elevated CO2 is a positive thing, in that McCalley et al. say that "nitrous oxide is a potent greenhouse gas with 180 times the global warming potential of CO2," citing Lashof and Ahuja (1990). In addition, the five researchers state that the greater-than-60% reductions in reactive N gas imply that elevated CO2 is "increasing the retention of biologically available N during critical growth periods," which is a major benefit for desert ecosystems.
In conclusion, the scientific literature indicates that as the air’s CO2 content continues to rise, earth’s plants will likely respond by reducing the amount of nitrogen invested in rubisco and other photosynthetic proteins, while still maintaining enhanced rates of photosynthesis, which consequently should increase their photosynthetic nitrogen-use efficiencies. As overall plant nitrogen-use efficiency increases, it is likely plants will grow ever better on soils containing less-than-optimal levels of nitrogen, a point addressed in more detail in Section 7.3.7 of this report.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenefficiency.php.
Nutrient Acquisition
Most species of plants respond to increases in the air’s CO2 content by displaying enhanced rates of photosynthesis and biomass production. Oftentimes, the resulting growth stimulation is preferentially expressed belowground, thereby causing significant increases in fine-root numbers and surface area. This phenomenon tends to increase total nutrient uptake under CO2-enriched conditions, which further stimulates plant growth and development. In this summary, we review how the acquisition of plant nutrients—primarily nitrate and phosphate—is affected by atmospheric CO2 enrichment. The effects of elevated CO2 on nitrogen fixation are addressed elsewhere (Sections 7.3.7 and 7.8.1) and more research on the effects of CO2 enhancement on roots appears in Section 7.8.5.
Smart et al. (1998) noted there were no differences on a per-unit-biomass basis in the total amounts of nitrogen within CO2-enriched and ambiently grown wheat seedlings after three weeks of exposure to atmospheric CO2 concentrations of 360 and 1,000 ppm. Nevertheless, the CO2-enriched seedlings exhibited greater rates of soil nitrate extraction than did the ambiently grown plants. Similarly, BassiriRad et al. (1998) reported that a doubling of the atmospheric CO2 concentration doubled the uptake rate of nitrate in the C4 grass Bouteloua eriopoda. However, they also reported that elevated CO2 had no effect on the rate of nitrate uptake in Prosopis, and that it decreased the rate of nitrate uptake by 55 percent in Larrea. Nonetheless, atmospheric CO2 enrichment increased total biomass in these two species by 55 and 69 percent, respectively. Thus, although the uptake rate of this nutrient was depressed under elevated CO2 conditions in the latter species, the much larger CO2-enriched plants likely still extracted more total nitrate from the soil than did the ambiently grown plants of the experiment.
Nasholm et al. (1998) determined that trees, grasses and shrubs can all absorb significant amounts of organic nitrogen from soils. Thus, plants do not have to wait for the mineralization of organic nitrogen before they extract the nitrogen they need from soils to support their growth and development. Hence, the forms of nitrogen removed from soils by plants (nitrate vs. ammonium) and their abilities to remove different forms may not be as important as was once thought.
With respect to the uptake of phosphate, Staddon et al. (1999) reported that Plantago lanceolata and Trifolium repens plants grown at 650 ppm CO2 for 2.5 months exhibited total plant phosphorus contents that were much greater than those displayed by plants grown at 400 ppm CO2, due to the fact that atmospheric CO2 enrichment significantly enhanced plant biomass. Similarly, Rouhier and Read (1998) reported that enriching the air around Plantago lanceolata plants with an extra 190 ppm of CO2 for a period of three months led to increased uptake of phosphorus and greater tissue phosphorus concentrations than were observed in plants growing in ambient air.
Greater uptake of phosphorus also can occur due to CO2-induced increases in root absorptive surface area or enhancements in specific enzyme activities. In addressing the first of these phenomena, BassiriRad et al. (1998) reported that a doubling of the atmospheric CO2 concentration significantly increased the belowground biomass of Bouteloua eriopoda and doubled its uptake rate of phosphate. However, elevated CO2 had no effect on uptake rates of phosphate in Larrea and Prosopis. Because the CO2-enriched plants grew so much bigger, they still removed more phosphate from the soil on a per-plant basis. With respect to the second phenomenon, phosphatase—the primary enzyme responsible for the conversion of organic phosphate into usable inorganic forms—had its activity increased by 30 to 40 percent in wheat seedlings growing at twice-ambient CO2 concentrations (Barrett et al., 1998).
In summary, as the CO2 content of the air increases, experimental data to date suggest that much of earth’s vegetation will likely extract enhanced amounts of mineral nutrients from the soils in which they are rooted.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nutrientacquis.php.
Pathogens
As the air’s CO2 content continues to rise, it is natural to wonder—and important to determine—how this phenomenon may impact plant-pathogen interactions. One thing we know about the subject is that atmospheric CO2 enrichment nearly always enhances photosynthesis, which commonly leads to increased plant production of carbon-based secondary compounds, including lignin and various phenolics, both of which substances tend to increase plant resistance to pathogen attack.
Enlarging upon this topic, Chakraborty and Datta (2003) report that “changes in plant physiology, anatomy and morphology that have been implicated in increased resistance or [that] can potentially enhance host resistance at elevated CO2 include: increased net photosynthesis allowing mobilization of resources into host resistance (Hibberd et al., 1996a.); reduced stomatal density and conductance (Hibberd et al., 1996b); greater accumulation of carbohydrates in leaves; more waxes, extra layers of epidermal cells and increased fibre content (Owensby, 1994); production of papillae and accumulation of silicon at penetration sites (Hibberd et al., 1996a); greater number of mesophyll cells (Bowes, 1993); and increased biosynthesis of phenolics (Hartley et al., 2000), among others.”
Chakraborty and Datta found another way atmospheric CO2 enrichment may tip the scales in favor of plants in a study of the aggressiveness of the fungal anthracnose pathogen Colletotrichum gloeosporioides. They inoculated two isolates of the pathogen onto two cultivars of the tropical pasture legume Stylosanthes scabra (Fitzroy, which is susceptible to the fungal pathogen, and Seca, which is more resistant) over the course of 25 sequential infection cycles at ambient (350 ppm) and elevated (700 ppm) atmospheric CO2 concentrations in controlled environment chambers. This protocol revealed that “at twice-ambient CO2 the overall level of aggressiveness of the two [pathogen] isolates was significantly reduced on both [host] cultivars.” In addition, they say that “as shown previously (Chakraborty et al., 2000), the susceptible Fitzroy develops a level of resistance to anthracnose at elevated CO2, but resistance in Seca remains largely unchanged.” Simultaneously, however, pathogen fecundity was found to increase at twice-ambient CO2. Of this finding, they report that their results “concur with the handful of studies that have demonstrated increased pathogen fecundity at elevated CO2 (Hibberd et al., 1996a; Klironomos et al., 1997; Chakraborty et al., 2000).” How this happened in the situation they investigated, as they describe it, is that the overall increase in fecundity at high CO2 “is a reflection of the altered canopy environment,” wherein “the 30 percent larger S. scabra plants at high CO2 (Chakraborty et al., 2000) makes the canopy microclimate more conducive to anthracnose development.”
In view of the opposing changes induced in pathogen behavior by elevated levels of atmospheric CO2 in this specific study—reduced aggressiveness but increased fecundity—it is difficult to know the outcome of atmospheric CO2 enrichment for the pathogen-host relationship. More research, especially under realistic field conditions, will be needed to clarify the situation; and, of course, different results are likely to be observed for different pathogen-host associations. Results also could differ under different climatic conditions. Nevertheless, the large number of ways in which elevated CO2 has been demonstrated to increase plant resistance to pathogen attack suggests that plants may well gain the advantage over pathogens as the air’s CO2 content continues to climb in the years ahead.
McElrone et al. (2005) “assessed how elevated CO2 affects a foliar fungal pathogen, Phyllosticta minima, of Acer rubrum [red maple] growing in the understory at the Duke Forest free-air CO2 enrichment experiment in Durham, North Carolina, USA … in the 6th, 7th, and 8th years of the CO2 exposure.” Surveys conducted in those years, in their words, “revealed that elevated CO2 [to 200 ppm above ambient] significantly reduced disease incidence, with 22%, 27% and 8% fewer saplings and 14%, 4%, and 5% fewer leaves infected per plant in the three consecutive years, respectively.” In addition, they report that the elevated CO2 “also significantly reduced disease severity in infected plants in all years (e.g. mean lesion area reduced 35%, 50%, and 10% in 2002, 2003, and 2004, respectively).”
With respect to identifying the underlying mechanism or mechanisms that produced these beneficent consequences, thinking it could have been a direct deleterious effect of elevated CO2 on the fungal pathogen, McElrone et al. performed some side experiments in controlled environment chambers. However, they found that the elevated CO2 benefited the fungal pathogen as well as the red maple saplings, observing that “exponential growth rates of P. minima were 17% greater under elevated CO2.” And they obtained similar results when they repeated the in vitro growth analysis two additional times in different growth chambers.
Taking another tack when “scanning electron micrographs verified that conidia germ tubes of P. minima infect A. rubrum leaves by entering through the stomata,” the researchers turned their attention to the pathogen’s mode of entry into the saplings’ foliage. In this investigation they found that both stomatal size and density were unaffected by atmospheric CO2 enrichment, but that “stomatal conductance was reduced by 21-36% under elevated CO2, providing smaller openings for infecting germ tubes.” They concluded that reduced disease severity under elevated CO2 was likely due to altered leaf chemistry, as elevated CO2 increased total leaf phenolic concentrations by 15 percent and tannin concentrations by 14 percent.
Because the phenomena they found to be important in reducing the amount and severity of fungal pathogen infection (leaf spot disease) of red maple have been demonstrated to be operative in most other plants as well, McElrone et al. say these CO2-enhanced leaf defensive mechanisms “may be prevalent in many plant pathosystems where the pathogen targets the stomata.” They state their results “provide concrete evidence for a potentially generalizable mechanism to predict disease outcomes in other pathosystems under future climatic conditions.”
Malmstrom and Field (1997) grew individual oat plants for two months in pots within phytocells maintained at CO2 concentrations of 350 and 700 ppm, while a third of each CO2 treatment’s plants were infected with the barley yellow dwarf virus (BYDV), which plagues more than 150 plant species worldwide, including all major cereal crops. They found that the elevated CO2 stimulated net photosynthesis rates in all plants, but with the greatest increase occurring in diseased individuals (48 percent vs. 34 percent). In addition, atmospheric CO2 enrichment decreased stomatal conductance by 34 percent in healthy plants, but by 50 percent in infected ones, thus reducing transpirational water losses more in infected plants. Together, these two phenomena contributed to a CO2-induced doubling of the instantaneous water-use efficiency of healthy control plants, but to a much larger 2.7-fold increase in diseased plants. Thus, although BYDV infection did indeed reduce overall plant biomass production, the growth response to elevated CO2 was greatest in the diseased plants. After 60 days of CO2 enrichment, for example, total plant biomass increased by 36 percent in infected plants, while it increased by only 12 percent in healthy plants. In addition, while elevated CO2 had little effect on root growth in healthy plants, it increased root biomass in infected plants by up to 60 percent. In their concluding remarks, therefore, Malmstrom and Field say that CO2 enrichment “may reduce losses of infected plants to drought” and “may enable diseased plants to compete better with healthy neighbors.”
Tiedemann and Firsching (2000) grew spring wheat from germination to maturity in controlled environment chambers maintained at either ambient (377 ppm) or enriched (612 ppm) atmospheric CO2 concentrations and either ambient (20 ppb) or enriched (61 ppb) atmospheric ozone (O3) concentrations, while half of the plants in each of the four resulting treatments were inoculated with a leaf rust-causing pathogen. These procedures revealed that the percent of leaf area infected by rust in inoculated plants was largely unaffected by atmospheric CO2 enrichment but strongly reduced by elevated O3. With respect to photosynthesis, elevated CO2 increased rates in inoculated plants by 20 and 42 percent at ambient and elevated O3 concentrations, respectively. Although inoculated plants produced lower yields than non-inoculated plants, atmospheric CO2 enrichment still stimulated yield in infected plants, increasing it by fully 57 percent at high O3. Consequently, the beneficial effects of elevated CO2 on wheat photosynthesis and yield continued to be expressed in the presence of both O3 and pathogenic stresses.
In another joint CO2/O3 study, Percy et al. (2002) grew the most widely distributed North American tree species—trembling aspen—in twelve 30-m-diameter free-air CO2 enrichment (FACE) rings near Rhinelander, Wisconsin, USA in air maintained at ambient CO2 and O3 concentrations, ambient O3 and elevated CO2 (560 ppm during daylight hours), ambient CO2 and elevated O3 (46.4-55.5 ppb during daylight hours), and elevated CO2 and O3 over the period of each growing season from 1998 through 2001. Throughout this experiment they assessed a number of the young trees’ growth characteristics, as well as their responses to poplar leaf rust (Melampsora medusae), which they say “is common on aspen and belongs to the most widely occurring group of foliage diseases.” Their work revealed that elevated CO2 alone did not alter rust occurrence, but that elevated O3 alone increased it by nearly fourfold. When applied together, however, elevated CO2 reduced the enhancement of rust development caused by elevated O3 from nearly fourfold to just over twofold.
Jwa and Walling (2001) grew tomato plants in hydroponic culture for eight weeks in controlled environment chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm. At week five of their study, half of the plants growing in each CO2 concentration were infected with the fungal pathogen Phytophthora parasitica, which attacks plant roots and induces water stress that decreases plant growth and yield. This infection procedure reduced total plant biomass by nearly 30 percent at both atmospheric CO2 concentrations. However, the elevated CO2 treatment increased the total biomass of healthy and infected plants by the same percentage, so that infected tomato plants grown at 700 ppm CO2 exhibited biomass values similar to those of healthy tomato plants grown at 350 ppm CO2. Consequently, atmospheric CO2 enrichment completely counterbalanced the negative effects of Phytophthora parasitica infection on tomato productivity.
Pangga et al. (2004) grew well-watered and fertilized pencilflower (cultivar Fitzroy) seedlings—an important legume crop susceptible to anthracnose disease caused by Colletotrichum gloeosporioides—within a controlled environment facility maintained at atmospheric CO2 concentrations of either 350 or 700 ppm, where they inoculated six-, nine- and twelve-week-old plants with conidia of C. gloeosporioides. Then, ten days after inoculation, they counted the anthracnose lesions on the plants and classified them as either resistant or susceptible. In doing so, they found that “the mean number of susceptible, resistant, and total lesions per leaf averaged over the three plant ages was significantly (P<0.05) greater at 350 ppm than at 700 ppm CO2, reflecting the development of a level of resistance in susceptible cv. Fitzroy at high CO2.” With respect to plants inoculated at twelve weeks of age, they say that those grown “at 350 ppm had 60 and 75 percent more susceptible and resistant lesions per leaf, respectively, than those [grown] at 700 ppm CO2.” The Australian scientists say their work “clearly shows that at 350 ppm overall susceptibility of the canopy increases with increasing age because more young leaves are produced on secondary and tertiary branches of the more advanced plants.” However, “at 700 ppm CO2, infection efficiency did not increase with increasing plant age despite the presence of many more young leaves in the enlarged canopy,” which finding, in their words, “points to reduced pathogen efficiency or an induced partial resistance to anthracnose in Fitzroy at 700 ppm CO2.”
Finally, according to Plessl et al. (2007), “potato late blight caused by the oomycete Phytophthora infestans (Mont.) de Bary is the most devastating disease of potato worldwide,” adding that “infection occurs through leaves and tubers followed by a rapid spread of the pathogen finally causing destructive necrosis.” In an effort to ascertain the effects of atmospheric CO2 enrichment on this pathogen, Plessl et al. grew individual well watered and fertilized plants of the potato cultivar Indira in 3.5-liter pots filled with a 1:2 mixture of soil and “Fruhstorfer T-Erde” in controlled-environment chambers maintained at atmospheric CO2 concentrations of either 400 or 700 ppm. Four weeks after the start of the experiment, the first three fully developed pinnate leaves were cut from the plants and inoculated with zoospores of P. infestans in Petri dishes containing water-agar, after which their symptoms were evaluated daily via comparison with control leaves that were similarly treated but unexposed to the pathogen.
Results of the German researchers analysis revealed that the 300 ppm increase in CO2 “dramatically reduced symptom development,” including extent of necrosis (down by 44 percent four days after inoculation and 65 percent five days after inoculation), area of sporulation (down by 100 percent four days after inoculation and 61 percent five days after inoculation), and sporulation intensity (down by 73 percent four days after inoculation and 17 percent five days after inoculation). Plessl et al. conclude that their results “clearly demonstrated that the potato cultivar Indira, which under normal conditions shows a high susceptibility to P. infestans, develops resistance against this pathogen after exposure to 700 ppm CO2,” noting that “this finding agrees with results from Ywa et al. (1995), who reported an increased tolerance of tomato plants to Phytophthora root rot when grown at elevated CO2.” These similar observations bode well for both potato and tomato cultivation in a CO2-enriched world of the future.
In conclusion, the balance of evidence obtained to date demonstrates an enhanced ability of plants to withstand pathogen attacks in CO2-enriched as opposed to ambient-CO2 air. As the atmosphere’s CO2 concentration continues to rise in the years to come, earth’s vegetation should fare ever better in its battle against myriad debilitating plant diseases.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/p/pathogens.php.
Parasitic Plants
Parasitic plants obtain energy, water and nutrients from their host plants and cause widespread reductions in harvestable crop yields around the globe. Hence, it is important to understand how rising atmospheric CO2 levels may impact the growth of parasitic plants and the relationships between them and their hosts.
Matthies and Egli (1999) grew Rhinanthus alectorolophus (a widely distributed parasitic plant of Central Europe) for a period of two months on the grass Lolium perenne and the legume Medicago sativa in pots placed within open-top chambers maintained at atmospheric CO2 concentrations of 375 and 590 ppm, half of which pots were fertilized to produce an optimal soil nutrient regime and half of which were unfertilized. At low nutrient supply, they found that atmospheric CO2 enrichment decreased mean parasite biomass by an average of 16 percent, while at high nutrient supply it increased parasite biomass by an average of 123 percent. Nevertheless, the extra 215 ppm of CO2 increased host plant biomass in both situations: by 29 percent under high soil nutrition and by 18 percent under low soil nutrition.
Dale and Press (1999) infected white clover (Trifolium repens) plants with Orobanche minor (a parasitic weed that primarily infects leguminous crops in the United Kingdom and the Middle East) and exposed them to atmospheric CO2 concentrations of either 360 or 550 ppm for 75 days in controlled-environment growth cabinets. The elevated CO2 in this study had no effect on the total biomass of parasite per host plant, nor did it impact the number of parasites per host plant or the time to parasitic attachment to host roots. On the other hand, whereas infected host plants growing in ambient air produced 47 percent less biomass than uninfected plants growing in ambient air, infected plants growing at 550 ppm CO2 exhibited final dry weights that were only 20 percent less than those displayed by uninfected plants growing in the CO2-enriched air, indicative of a significant CO2-induced partial alleviation of parasite-induced biomass reductions in the white clover host plants.
Watling and Press (1997) infected several C4 sorghum plants with Striga hermonthica and Striga asiatica (parasitic C3 weeds of the semi-arid tropics that infest many grain crops) and grew them, along with uninfected control plants, for approximately two months in controlled-environment cabinets maintained at atmospheric CO2 concentrations of 350 and 700 ppm. In the absence of parasite infection, the extra 350 ppm of CO2 increased sorghum biomass by approximately 36 percent. When infected with S. hermonthica, however, the sorghum plants grown at ambient and elevated CO2 concentrations only produced 32 and 43 percent of the biomass displayed by their respective uninfected controls. Infection with S. asiatica was somewhat less stressful and led to host biomass production that was about half that of uninfected controls in both ambient and CO2-enriched air. The end result was that the doubling of the air’s CO2 content employed in this study increased sorghum biomass by 79 percent and 35 percent in the C4 sorghum plants infected with S. hermonthica and S. asiatica, respectively.
Hwangbo et al. (2003) grew Kentucky Bluegrass (Poa pratensis L.) with and without infection by the C3 chlorophyllous parasitic angiosperm Rhinanthus minor L. (a facultative hemiparasite found in natural and semi-natural grasslands throughout Europe) for eight weeks in open-top chambers maintained at ambient and elevated (650 ppm) CO2 concentrations. At the end of the study, the parasite’s biomass (when growing on its host) was 47 percent greater in the CO2-enriched chambers, while its host exhibited only a 10 percent CO2-induced increase in biomass in the parasite’s absence but a nearly doubled 19 percent increase when infected by it.
Watling and Press (2000) grew upland rice (Oryza sativa L.) in pots in controlled-environment chambers maintained at 350 and 700 ppm CO2 in either the presence or absence of the root parasite S. hermonthica for a period of 80 days after sowing, after which time the plants were harvested and weighed. In ambient air, the presence of the parasite reduced the biomass of the rice to only 35 percent of what it was in the absence of the parasite; whereas in air enriched with CO2 the presence of the parasite reduced the biomass of infected plants to but 73 percent of what it was in the absence of the parasite.
In summary, these several observations suggest that the rising CO2 content of the air can have wide and variable effects on parasitic plants, ranging from negative to positive growth responses, depending upon soil nutrition and host plant specificity. With respect to the infected host plants, elevated CO2 generally tends to reduce the negative effects of parasitic infection, so that infected host plants continue to exhibit positive growth responses to elevated CO2. It is likely that whatever the scenario with regard to parasitic infection, host plants will fare better under higher atmospheric CO2 conditions than they do currently.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/p/parasites.php.
Roots
In reviewing the scientific literature pertaining to atmospheric CO2 enrichment effects on belowground plant growth and development, Weihong et al. (2000) briefly summarize what is known about this subject. They report that atmospheric CO2 enrichment typically enhances the growth rates of roots, especially those of fine roots, and that CO2-induced increases in root production eventually lead to increased carbon inputs to soils, due to enhanced root turnover and exudation of various organic carbon compounds, which can potentially lead to greater soil carbon sequestration. In addition, they note that increased soil carbon inputs stimulate the growth and activities of soil microorganisms that utilize plant-derived carbon as their primary energy source; and they report that subsequently enhanced activities of fungal and bacterial plant symbionts often lead to increased plant nutrient acquisition.
In a much more narrowly focused study, Crookshanks et al. (1998) sprouted seeds of the small and fast-growing Arabidopsis thaliana plant on agar medium in Petri dishes and grew the resulting immature plants in controlled environment chambers maintained at atmospheric CO2 concentrations of either 355 or 700 ppm. Visual assessments of root growth were made after emergence of the roots from the seeds, while microscopic investigations of root cell properties were also conducted. The scientists learned that the CO2-enriched plants directed a greater proportion of their newly produced biomass into root, as opposed to shoot, growth. In addition, the young plants produced longer primary roots and more and longer lateral roots. These effects were found to be related to the CO2-induced stimulation of mitotic activity, accelerated cortical cell expansion, and increased cell wall plasticity.
Gouk et al. (1999) grew an orchid plantlet, Mokara Yellow, in plastic bags flushed with 350 and 10,000 ppm CO2 for three months to study the effects of elevated CO2 on this epiphytic CAM species. They determined that the super-elevated CO2 of their experiment enhanced the total dry weight of the orchid plantlets by more than two-fold, while increasing the growth of existing roots and stimulating the induction of new roots from internodes located on the orchid stems. Total chlorophyll content was also increased by elevated CO2—by 64 percent in young leaves and by 118 percent in young roots. This phenomenon permitted greater light harvesting during photosynthesis and likely led to the tissue starch contents of the CO2-enriched plantlets rising nearly 20-fold higher than those of the control-plantlets. In spite of this large CO2-induced accumulation of starch, however, no damage or disruption of chloroplasts was evident in the leaves and roots of the CO2-enriched plants.
A final question that has periodically intrigued researchers is whether plants take up carbon through their roots in addition to through their leaves. Although a definitive answer eludes us, various aspects of the issue have been described by Idso (1989), who we quote as follows.
“Although several investigators have claimed that plants should receive little direct benefit from dissolved CO2 (Stolwijk et al., 1957; Skok et al., 1962; Splittstoesser, 1966), a number of experiments have produced significant increases in root growth (Erickson, 1946; Leonard and Pinckard, 1946; Geisler, 1963; Yorgalevitch and Janes, 1988), as well as yield itself (Kursanov et al., 1951; Grinfeld, 1954; Nakayama and Bucks, 1980; Baron and Gorski, 1986), with CO2-enriched irrigation water. Early on, Misra (1951) suggested that this beneficent effect may be related to CO2-induced changes in soil nutrient availability; and this hypothesis may well be correct. Arteca et al. (1979), for example, have observed K, Ca and Mg to be better absorbed by potato roots when the concentration of CO2 in the soil solution is increased; while Mauney and Hendrix (1988) found Zn and Mn to be better absorbed by cotton under such conditions, and Yurgalevitch and Janes (1988) found an enhancement of the absorption of Rb by tomato roots. In all cases, large increases in either total plant growth or yield accompanied the enhanced uptake of nutrients. Consequently, as it has been suggested that CO2 concentration plays a major role in determining the porosity, plasticity and charge of cell membranes (Jackson and Coleman, 1959; Mitz, 1979), which could thereby alter ion uptake and organic acid production (Yorgalevitch and Janes, 1988), it is possible that some such suite of mechanisms may well be responsible for the plant productivity increases often observed to result from enhanced concentrations of CO2 in the soil solution.”
In the next two sections we survey the scientific literature on root responses to atmospheric CO2 enrichment for crops and then trees.
Additional information on this topic, including reviews on roots not discussed here, can be found at http://www.co2science.org/subject/r/subject_r.php under the heading Roots.
Crops
Hodge and Millard (1998) grew narrowleaf plantain (Plantago lanceolata) seedlings for a period of six weeks in controlled environment growth rooms maintained at atmospheric CO2 concentrations of either 400 or 800 ppm. By the end of this period, the plants in the 800-ppm air exhibited increases in shoot and root dry matter production that were 159 percent and 180 percent greater, respectively, than the corresponding dry matter increases experienced by the plants growing in 400-ppm air, while the amount of plant carbon recovered from the potting medium (sand) was 3.2 times greater in the elevated-CO2 treatment. Thus, these investigators found that the belowground growth stimulation provided by atmospheric CO2 enrichment was greater than that experienced above-ground.
Wechsung et al. (1999) grew spring wheat (Triticum aestivum) in rows in a FACE study employing atmospheric CO2 concentrations of 370 and 550 ppm and irrigation treatments that periodically replaced either 50 percent or 100 percent of prior potential evapotranspiration in an effort to determine the effects of elevated CO2 and water stress on root growth. They found that elevated CO2 increased in-row root dry weight by an average of 22 percent during the growing season under both the wet and dry irrigation regimes. In addition, during the vegetative growth phase, atmospheric CO2 enrichment increased inter-row root dry weight by 70 percent, indicating that plants grown in elevated CO2 developed greater lateral root systems than plants grown at ambient CO2. During the reproductive growth phase, elevated CO2 stimulated the branching of lateral roots into inter-row areas, but only when water was limiting to growth. In addition, the CO2-enriched plants tended to display greater root dry weights at a given depth than did ambiently grown plants.
In a comprehensive review of all prior FACE experiments conducted on agricultural crops, Kimball et al. (2002) determined that for a 300-ppm increase in atmospheric CO2 concentration, the root biomass of wheat, ryegrass and rice experienced an average increase of 70 percent at ample water and nitrogen, 58 percent at low nitrogen and 34 percent at low water, while clover experienced a 38 percent increase at ample water and nitrogen, plus a 32 percent increase at low nitrogen. Outdoing all of the other crops was cotton, which exhibited a 96 percent increase in root biomass at ample water and nitrogen.
Zhao et al. (2000) germinated pea (Pisum sativum) seeds and exposed the young plants to various atmospheric CO2 concentrations in controlled environment chambers to determine if elevated CO2 impacts root border cells, which are major contributors of root exudates in this and most other agronomic plants. They found that elevated CO2 increased the production of root border cells in pea seedlings. In going from ambient air to air enriched to 3,000 and 6,000 ppm CO2, border-cell numbers increased by over 50 percent and 100 percent, respectively. Hence, as the CO2 content of the air continues to rise, peas (and possibly many other crop plants) will likely produce greater numbers of root border cells, which should increase the amounts of root exudations occurring in their rhizospheres, which further suggests that associated soil microbial and fungal activities will be stimulated as a result of the increases in plant-derived carbon inputs that these organisms require to meet their energy needs.
Van Ginkel et al. (1996) grew perennial ryegrass (Lolium perenne) plants from seed in two growth chambers for 71 days under continuous 14CO2-labeling of the atmosphere at CO2 concentrations of 350 and 700 ppm at two different soil nitrogen levels. At the conclusion of this part of the experiment, the plants were harvested and their roots dried, pulverized and mixed with soil in a number of one-liter pots that were placed within two wind tunnels in an open field, one of which had ambient air of 361 ppm CO2 flowing through it, and one of which had air of 706 ppm CO2 flowing through it. Several of the containers were then seeded with more Lolium perenne, others were similarly seeded the following year, and still others were kept bare for two years. Then, at the ends of the first and second years, the different degrees of decomposition of the original plant roots were assessed.
It was determined, first, that shoot and root growth were enhanced by 13 and 92 percent, respectively, by the extra CO2 in the initial 71-day portion of the experiment, once again demonstrating the significant benefits that are often conferred upon plant roots by atmospheric CO2 enrichment. Secondly, it was found that the decomposition of the high-CO2-grown roots in the high-CO2 wind tunnel was 19 percent lower than that of the low-CO2-grown roots in the low-CO2 wind tunnel at the end of the first year, and that it was 14 percent lower at the end of the second year in the low-nitrogen-grown plants but equivalent in the high-nitrogen-grown plants. It was also determined that the presence of living roots reduced the decomposition rate of dead roots below the dead-root-only decomposition rate observed in the bare soil treatment. Based on these findings, van Ginkel et al. conclude that “the combination of higher root yields at elevated CO2 combined with a decrease in root decomposition will lead to a longer residence time of C in the soil and probably to a higher C storage.”
In conclusion, as the CO2 content of the air continues to rise, many crops will likely develop larger and more extensively branching root systems that may help them to better cope with periods of reduced soil moisture availability. This chain of events should make the soil environment even more favorable for plant growth and development in a high-CO2 world of the future.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/r/rootscrops.php.
Trees
Janssens et al. (1998) grew three-year-old Scots pine seedlings for a period of six months in open-top chambers maintained at ambient and 700 ppm atmospheric CO2, finding that the extra CO2 increased total root length by 122 percent and total root dry mass by 135 percent. In a similar study that employed close to the same degree of enhancement of the air’s CO2 content, Pritchard et al. (2001a) grew idealized ecosystems representative of regenerating longleaf pine forests of the southeastern USA for a period of 18 months in large soil bins located within open-top chambers. The above-ground parts of these seedlings experienced a growth enhancement of 20 percent. The root biomass of the trees, however, was increased by more than three times as much (62 percent).
Working with FACE technology, Pritchard et al. (2001b) studied 14-year-old loblolly pine trees after a year of exposure to an extra 200 ppm of CO2, finding that total standing root length and root numbers were 16 and 34 percent greater, respectively, in the CO2-enriched plots than in the ambient-air plots. In addition, the elevated CO2 increased the diameter of living and dead roots by 8 and 6 percent, respectively, while annual root production was found to be 26 percent greater in the CO2-enriched plots. For the degree of CO2 enrichment employed in the prior two studies, this latter enhancement corresponds to a root biomass increase of approximately 45 percent.
In an open-top chamber study of a model ecosystem composed of a mixture of spruce and beech seedlings, Wiemken et al. (2001) investigated the effects of a 200 ppm increase in the air’s CO2 concentration that prevailed for a period of four years. On nutrient-poor soils, the extra CO2 led to a 30 percent increase in fine-root biomass, while on nutrient-rich soils it led to a 75 percent increase. These numbers correspond to increases of about 52 percent and 130 percent, respectively, for atmospheric CO2 enhancements on the order of those employed by Janssens et al. (1998) and Pritchard et al. (2001a).
Another interesting aspect of the Wiemken et al. study was their finding that the extra CO2 increased the amount of symbiotic fungal biomass associated with the trees’ fine roots by 31 percent on nutrient-poor soils and by 100 percent on nutrient-rich soils, which for the degree of atmospheric CO2 enrichment used in the studies of Janssens et al. (1998) and Pritchard et al. (2001a) translate into increases of about 52 percent and 175 percent, respectively.
Berntsen and Bazzaz (1998) removed intact chunks of soil from the Hardwood-White Pine-Hemlock forest region of New England and placed them in plastic containers within controlled environment glasshouses maintained at either 375 or 700 ppm CO2 for a period of two years in order to study the effects of elevated CO2 on the regeneration of plants from seeds and rhizomes present in the soil. At the conclusion of the study, total mesocosm plant biomass (more than 95 percent of which was supplied by yellow and white birch tree seedlings) was found to be 31 percent higher in the elevated CO2 treatment than in ambient air, with a mean enhancement of 23 percent above-ground and 62 percent belowground. The extra CO2 also increased the mycorrhizal colonization of root tips by 45 percent in white birch and 71 percent in yellow birch; and the CO2-enriched yellow birch seedlings exhibited 322 percent greater root length and 305 percent more root surface area than did the yellow birch seedlings growing in ambient air.
Kubiske et al. (1998) grew cuttings of four quaking aspen genotypes in open-top chambers for five months at atmospheric CO2 concentrations of either 380 or 720 ppm and low or high soil nitrogen concentrations. They found, surprisingly, that the cuttings grown in elevated CO2 displayed no discernible increases in above-ground growth. However, the extra CO2 significantly increased fine-root length and root turnover rates at high soil nitrogen by increasing fine-root production, which would logically be expected to produce benefits (not the least of which would be a larger belowground water- and nutrient-gathering system) that would eventually lead to enhanced above-ground growth as well.
Expanding on this study, Pregitzer et al. (2000) grew six quaking aspen genotypes for 2.5 growing seasons in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm with both adequate and inadequate supplies of soil nitrogen. This work demonstrated that the trees exposed to elevated CO2 developed thicker and longer roots than the trees growing in ambient air, and that the fine-root biomass of the CO2-enriched trees was enhanced by 17 percent in the nitrogen-poor soils and by 65 percent in the nitrogen-rich soils.
Yet another study of quaking aspen conducted by King et al. (2001) demonstrated that trees exposed to an atmospheric CO2 concentration 560 ppm in a FACE experiment produced 133 percent more fine-root biomass than trees grown in ambient air of 360 ppm, which roughly equates to 233 percent more fine-root biomass for the degree of CO2 enrichment employed in the prior study of Pregitzer et al. And when simultaneously exposed to air of 1.5 times the normal ozone concentration, the degree of fine-root biomass stimulation produced by the extra CO2 was still as great as 66 percent, or roughly 115 percent when extrapolated to the greater CO2 enrichment employed by Pregitzer et al.
In a final quaking aspen study, King et al. (1999) grew four clones at two different temperature regimes (separated by 5°C) and two levels of soil nitrogen (N) availability (high and low) for 98 days, while measuring photosynthesis, growth, biomass allocation, and root production and mortality. They found that the higher of the two temperature regimes increased rates of photosynthesis by 65 percent and rates of whole-plant growth by 37 percent, while it simultaneously enhanced root production and turnover. It was thus their conclusion that “trembling aspen has the potential for substantially greater growth and root turnover under conditions of warmer soil at sites of both high and low N-availability” and that “an immediate consequence of this will be greater inputs of C and nutrients to forest soils.”
In light of these several findings pertaining to quaking aspen trees, it is evident that increases in atmospheric CO2 concentration, air temperature and soil nitrogen content all enhance their belowground growth, which positively impacts their above-ground growth.
Turning our attention to other deciduous trees, Gleadow et al. (1998) grew eucalyptus seedlings for six months in glasshouses maintained at atmospheric CO2 concentrations of either 400 or 800 ppm, fertilizing them twice daily with low or high nitrogen solutions. The elevated CO2 of their experiment increased total plant biomass by 98 and 134 percent relative to plants grown at ambient CO2 in the high and low nitrogen treatments, respectively. In addition, in the low nitrogen treatment, elevated CO2 stimulated greater root growth, as indicated by a 33 percent higher root:shoot ratio.
In a more complex study, Day et al. (1996) studied the effects of elevated CO2 on fine-root production in open-top chambers erected over a regenerating oak-palmetto scrub ecosystem in Florida, USA, determining that a 350-ppm increase in the atmosphere’s CO2 concentration increased fine-root length densities by 63 percent while enhancing the distribution of fine roots at both the soil surface (0-12 cm) and at a depth of 50-60 cm. These findings suggest that the ongoing rise in the atmosphere’s CO2 concentration will likely increase the distribution of fine roots near the soil surface, where the greatest concentrations of nutrients are located, and at a depth that coincides with the upper level of the site’s water table, both of which phenomena should increase the trees’ ability to acquire the nutrients and water they will need to support CO2-enhanced biomass production in the years ahead.
In another study that employed CO2, temperature and nitrogen as treatments, Uselman et al. (2000) grew seedlings of the nitrogen-fixing black locust tree for 100 days in controlled environments maintained at atmospheric CO2 concentrations of 350 and 700 ppm and air temperatures of 26°C (ambient) and 30°C, with either some or no additional nitrogen fertilization, finding that the extra CO2 increased total seedling biomass by 14 percent, the elevated temperature increased it by 55 percent, and nitrogen fertilization increased it by 157 percent. With respect to root exudation, a similar pattern was seen. Plants grown in elevated CO2 exuded 20 percent more organic carbon compounds than plants grown in ambient air, while elevated temperature and fertilization increased root exudation by 71 and 55 percent, respectively. Hence, as the air’s CO2 content continues to rise, black locust trees will likely exhibit enhanced rates of biomass production and exudation of dissolved organic compounds from their roots. Moreover, if air temperature also rises, even by as much as 4°C, its positive effect on biomass production and root exudation will likely be even greater than that resulting from the increasing atmospheric CO2 concentration. The same would appear to hold true for anthropogenic nitrogen deposition, reinforcing what was learned about the impacts of these three environmental factors on the growth of quaking aspen trees.
In light of these several experimental findings, it can confidently be concluded that the ongoing rise in the air’s CO2 content, together with possible concurrent increases in air temperature and nitrogen deposition, will likely help earth’s woody plants increase their root mass and surface area to become ever more robust and productive.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/r/rootsconifers.php and http://www.co2 science.org/subject/r/rootsdeciduous.php.
Seeds
Elevated CO2 levels are known to have effects on seeds that are different from their effects on total biomass, roots, and other dimensions examined so far. In this section we survey the scientific literature on this topic regarding crops, grasslands, and trees.
Additional information on this topic, including reviews on seeds not discussed here, can be found at http://www.co2science.org/subject/s/subject_s.php under the heading Seeds.
Crops
In a greenhouse study of the various components of seed biomass production, Palta and Ludwig (2000) grew narrow-leafed lupin in pots filled with soil within Mylar-film tunnels maintained at either 355 or 700 ppm CO2. They found that the extra CO2 increased (1) the final number of pods and (2) the number of pods that filled large seeds, while it (3) reduced to zero the number of pods that had small seeds, (4) reduced the number of pods with unfilled seeds from 16 to 1 pod per plant, and increased (5) pod set and (6) dry matter accumulation on the developing branches. These several CO2-induced improvements to key physiological processes resulted in 47 to 56 percent increases in dry matter per plant, which led to increases of 44 to 66 percent in seed yield per plant.
Sanhewe et al. (1996) grew winter wheat in polyethylene tunnels maintained at atmospheric CO2 concentrations of 380 and 680 ppm from the time of seed germination to the time of plant maturity, while maintaining a temperature gradient of approximately 4°C in each tunnel. In addition to the elevated CO2 increasing seed yield per unit area, they found it also increased seed weight, but not seed survival or germination. Increasing air temperature, on the other hand, increased seed longevity across the entire range of temperatures investigated (14 to 19°C).
Thomas et al. (2003) grew soybean plants to maturity in sunlit controlled-environment chambers under sinusoidally varying day/night-max/min temperatures of 28/18, 32/22, 36/26, 40/30 and 44/34°C and two levels of atmospheric CO2 concentration (350 and 700 ppm). They determined, in their words, that the effect of temperature on seed composition and gene expression was “pronounced,” but that “there was no effect of CO2.” In this regard, however, they note that “Heagle et al. (1998) observed a positive significant effect of CO2 enrichment on soybean seed oil and oleic acid concentration,” the latter of which parameters Thomas et al. found to increase with rising temperature all the way from 28/18 to 44/34°C.
In another soybean study, Ziska et al. (2001) grew one modern and eight ancestral genotypes in glasshouses maintained at atmospheric CO2 concentrations of 400 and 710 ppm, finding that the extra CO2 increased photosynthetic rates by an average of 75 percent. This enhancement in photosynthetic sugar production led to increases in seed yield that averaged 40 percent for all cultivars, except for one ancestral variety that exhibited an 80 percent increase in seed yield. Hence, if plant breeders were to utilize the highly CO2-responsive ancestral cultivar identified in this study in their breeding programs, it is possible that soybean seed yields could be made to rise even faster and higher in the days and years ahead.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/s/seedscrops.php.
Grasslands
Steinger et al. (2000) collected seeds from Bromus erectus plants that had been grown at atmospheric CO2 concentrations of 360 and 650 ppm and germinated some of both groups of seeds under those same two sets of conditions. They found the elevated CO2 treatment increased individual seed mass by about 9 percent and increased seed carbon-to-nitrogen ratio by almost 10 percent. However, they also learned that these changes in seed properties had little impact on subsequent seedling growth. In fact, when the seeds produced by ambient or CO2-enriched plants were germinated and grown in ambient air, there was no significant size difference between the two groups of resultant seedlings after a period of 19 days. Likewise, when the seeds produced from ambient or CO2-enriched plants were germinated and grown in the high CO2 treatment, there was also no significant difference between the sizes of the seedlings derived from the two groups of seeds. However, the CO2-enriched seedlings produced from both groups of seeds were almost 20 percent larger than the seedlings produced from both groups of seeds grown in ambient air, demonstrating that the direct effects of elevated atmospheric CO2 concentration on seedling growth and development were more important than the differences in seed characteristics produced by the elevated atmospheric CO2 concentration in which their parent plants grew.
In another study conducted about the same time, Edwards et al. (2001) utilized a FACE experiment where daytime atmospheric CO2 concentrations above a sheep-grazed pasture in New Zealand were increased by 115 ppm to study the effects of elevated CO2 on seed production, seedling recruitment and species compositional changes. In the two years of their study, the extra daytime CO2 increased seed production and dispersal in seven of the eight most abundant species, including the grasses Anthoxanthum odoratum, Lolium perenne and Poa pratensis, the legumes Trifolium repens and T. subterranean, and the herbs Hypochaeris radicata and Leontodon saxatilis. In some of these plants, elevated CO2 increased the number of seeds per reproductive structure, while all of them exhibited CO2-induced increases in the number of reproductive structures per unit of ground area. In addition, they determined that the CO2-induced increases in seed production contributed in a major way to the increase in the numbers of species found within the CO2-enriched plots.
In a five-year study of a nutrient-poor calcareous grassland in Switzerland, Thurig et al. (2003) used screen-aided CO2 control (SACC) technology (Leadley et al., 1997) to enrich the air over half of their experimental plots with an extra 300 ppm of CO2, finding that “the effect of elevated CO2 on the number of flowering shoots (+24%) and seeds (+29%) at the community level was similar to above ground biomass response.” In terms of species functional groups, there was a 42 percent increase in the mean seed number of graminoids and a 33 percent increase in the mean seed number of forbs, but no change in legume seed numbers. In most species, mean seed weight also tended to be greater in plants grown in CO2-enriched air (+12 percent); and Thurig et al. say it is known from many studies that heavier seeds result in seedlings that “are more robust than seedlings from lighter seeds (Baskin and Baskin, 1998).”
Wang and Griffin (2003) grew dioecious white cockle plants from seed to maturity in sand-filled pots maintained at optimum moisture and fertility conditions in environmentally controlled growth chambers in which the air was continuously maintained at CO2 concentrations of either 365 or 730 ppm. In response to this doubling of the air’s CO2 content, the vegetative mass of both male and female plants rose by approximately 39 percent. Reproductive mass, on the other hand, rose by 82 percent in male plants and by 97 percent in females. In the female plants, this feat was accomplished, in part, by increases of 36 percent and 44 percent in the number and mass of seeds per plant, and by a 15 percent increase in the mass of individual seeds, in harmony with the findings of Jablonski et al. (2002), which they derived from a meta-analysis of the results of 159 CO2 enrichment experiments conducted on 79 species of agricultural and wild plants. Because dioecious plants comprise nearly half of all angiosperm families, we may expect to see a greater proportion of plant biomass allocated to reproduction in a high-CO2 world of the future, which result should bode well for the biodiversity of earth’s many ecosystems.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/s/seedsgrasslands.php.
Trees
How does enriching the air with carbon dioxide impact the reproductive capacity of trees? LaDeau and Clark (2001) determined the reproductive response of loblolly pine trees to atmospheric CO2 enrichment at Duke Forest in the Piedmont region of North Carolina, USA, where in August of 1996 three 30-m-diameter FACE rings began to enrich the air around the 13-year-old trees they encircled to 200 ppm above the atmosphere’s normal background concentration, while three other FACE rings served as control plots. Because the trees were not mature at the start of the experiment they did not produce any cones until a few rare ones appeared in 1998. By the fall of 1999, however, the two scientists found that, compared to the trees growing in ambient air, the CO2-enriched trees were twice as likely to be reproductively mature, and they produced three times more cones per tree. Similarly, the trees growing in the CO2-enriched air produced 2.4 times more cones in the fall of 2000; and from August 1999 through July 2000, they collected three times as many seeds in the CO2-fertilized FACE rings as in the control rings.
Also working on this aspect of the Duke Forest FACE study were Hussain et al. (2001), who report that (1) seeds collected from the CO2-enriched trees were 91 percent heavier than those collected from the trees growing in ambient air, (2) the CO2-enriched seeds had a lipid content that was 265 percent greater than that of the seeds produced on the ambient-treatment trees, (3) the germination success for seeds developed under atmospheric CO2 enrichment was more than three times greater than that observed for control seeds developed at ambient CO2, regardless of germination CO2 concentration, (4) seeds from the CO2-enriched trees germinated approximately five days earlier than their ambiently produced counterparts, again regardless of germination CO2 concentration, and (5) seedlings developing from seeds collected from CO2-enriched trees displayed significantly greater root lengths and needle numbers than seedlings developing from trees exposed to ambient air, also regardless of growth CO2 concentration.
The propensity for elevated levels of atmospheric CO2 to hasten the production of more plentiful seeds on the trees of this valuable timber species bodes well for naturally regenerating loblolly pine stands of the southeastern United States, where LaDeau and Clark report the trees “are profoundly seed-limited for at least 25 years.” As the air’s CO2 content continues to climb, they conclude that “this period of seed limitation may be reduced.” In addition, the observations of Hussain et al. suggest that loblolly pine trees in a CO2-enriched world of the future will likely display significant increases in their photosynthetic rates. Enhanced carbohydrate supplies resulting from this phenomenon will likely be used to increase seed weight and lipid content. Such seeds should consequently exhibit significant increases in germination success, and their enhanced lipid supplies will likely lead to greater root lengths and needle numbers in developing seedlings. Consequently, when CO2-enriched loblolly pine seedlings become photosynthetically active, they will likely produce biomass at greater rates than those exhibited by seedlings growing under current CO2 concentrations.
Five years later, LaDeau and Clark (2006a) conducted a follow-up study that revealed “carbon dioxide enrichment affected mean cone production both through early maturation and increased fecundity,” so that “trees in the elevated CO2 plots produced twice as many cones between 1998 and 2004 as trees in the ambient plots.” They also determined that the trees grown in elevated CO2 “made the transition to reproductive maturation at smaller [trunk] diameters,” and that they “not only reached reproductive maturation at smaller diameters, but also at younger ages.” By 2004, for example, they say that “roughly 50% of ambient trees and 75% of fumigated trees [had] produced cones.” In addition, they observed that “22% of the trees in high CO2 produced between 40 and 100 cones during the study, compared with only 9% of ambient trees.”
“In this 8-year study,” in the words of the two researchers, “we find that previous short-term responses indeed persist.” In addition, they note that “P. taeda trees that produce large seed crops early in their life span tend to continue to be prolific producers (Schutlz, 1997),” and they conclude that this fact, together with their findings, suggests that “individual responses seen in this young forest may be sustained over their life span.”
In a concurrent report, LaDeau and Clark (2006b) analyzed the seed and pollen responses of the loblolly pines to atmospheric CO2 enrichment, finding that the “trees grown in high-CO2 plots first began producing pollen while younger and at smaller sizes relative to ambient-grown trees,” and that cone pollen and airborne pollen grain abundances were significantly greater in the CO2-enriched stands. More specifically, they found that “by spring 2005, 63% of all trees growing in high CO2 had produced both pollen and seeds vs. only 36% of trees in the ambient plots.” The researchers say precocious pollen production “could enhance the production of viable seeds by increasing the percentage of fertilized ovules,” and that “more pollen disseminated from multiple-source trees may also increase rates of gene flow among stands, and could further reduce rates of self-pollination, indirectly enhancing the production of viable seeds.” They also say “pine pollen is not a dangerous allergen for the public at large.”
Another major study of the reproductive responses of trees to elevated levels of atmospheric CO2 was conducted at the Kennedy Space Center, Florida, USA, where in 1996 three species of scrub-oak (Quercus myrtifolia, Q. chapmanii, and Q. geminata) were enclosed within sixteen open-top chambers, half of which were maintained at 379 ppm CO2 and half at 704 ppm. Five years later—in August, September and October of 2001—Stiling et al. (2004) counted the numbers of acorns on randomly selected twigs of each species, while in November of that year they counted the numbers of fallen acorns of each species within equal-size quadrates of ground area, additionally evaluating mean acorn weight, acorn germination rate, and degree of acorn infestation by weevils. They found acorn germination rate and degree of predation by weevils were unaffected by elevated CO2, while acorn size was enhanced by a small amount: 3.6 percent for Q. myrtifolia, 7.0 percent for Q. chapmanii, and 7.7 percent for Q. geminata. Acorn number responses, on the other hand, were enormous, but for only two of the three species, as Q. geminata did not register any CO2-induced increase in reproductive output, in harmony with its unresponsive overall growth rate. For Q. myrtifolia, however, Stiling et al. report “there were four times as many acorns per 100 twigs in elevated CO2 as in ambient CO2 and for Q. chapmanii the increase was over threefold.” On the ground, the enhancement was greater still, with the researchers reporting that “the number of Q. myrtifolia acorns per meter squared in elevated CO2 was over seven times greater than in ambient CO2 and for Q. chapmanii, the increase was nearly sixfold.”
Stiling et al. say these results lead them to believe “there will be large increases in seedling production in scrub-oak forests in an atmosphere of elevated CO2,” noting that “this is important because many forest systems are ‘recruitment-limited’ (Ribbens et al., 1994; Hubbell et al., 1999),” which conclusion echoes that of LaDeau and Clark with respect to loblolly pines.
A third major study of CO2 effects on seed production in trees has been conducted at the FACE facility near Rhinelander, Wisconsin (USA), where young paper birch (Betula papyrifera Marsh.) seedlings were planted in 1997 and have been growing since 1998 in open-top chambers maintained at atmospheric CO2 concentrations of either 360 or 560 ppm, as well as at atmospheric ozone (O3) concentrations of either ambient or 1.5 times ambient. There, Darbah et al. (2007) collected many types of data pertaining to flowering, seed production, seed germination and new seedling growth and development over the 2004-2006 growing seasons; and as they describe it, “elevated CO2 had significant positive effect[s] on birch catkin size, weight, and germination success rate.” More specifically, they note that “elevated CO2 increased germination rate of birch by 110%, compared to ambient CO2 concentrations, decreased seedling mortality by 73%, increased seed weight by 17% [and] increased [new seedling] root length by 59%.”
In conclusion, research on a variety of tree species finds that CO2 enhancement increases the production of viable seeds and seedlings, meaning these species should flourish as CO2 levels conntinue to rise. Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/s/seedstrees.php.
Tannins
Condensed tannins are naturally occurring secondary carbon compounds produced in the leaves of a number of different plants that often act to deter herbivorous insects. How do condensed tannin concentrations in the leaves and roots of trees respond to atmospheric CO2 enrichment?
Additional information on this topic, including reviews on tannins not discussed here, can be found at http://www.co2science.org/subject/t/subject_t.php under the heading Tannins.
Aspen Trees
King et al. (2001) grew aspen seedlings for five months in open-top chambers maintained at atmospheric CO2 concentrations of either 350 or 700 ppm. At the end of this period, naturally senesced leaf litter was collected and analyzed; and it was found that the elevated CO2 of this particular study had no effect on leaf litter tannin concentration.
A substantially different result was obtained in an earlier study of aspen leaves that was conducted by McDonald et al. (1999), who grew aspen seedlings in controlled environment greenhouses that were maintained at either ambient (387 ppm) or elevated (696 ppm) CO2 concentrations under conditions of either low or high light availability (half and full sunlight, respectively) for 31 days after the mean date of bud break. In this case it was determined that under low light conditions, the CO2-enriched seedlings exhibited an increase of approximately 15 percent in leaf condensed tannin concentration, while under high light conditions the CO2-induced increase in leaf condensed tannin concentration was 175 percent.
In a much more complex study than either of the two preceding ones, Agrell et al. (2005) examined the effects of ambient and elevated concentrations of atmospheric CO2 (360 ppm and 560 ppm, respectively) and O3 (35-60 ppb and 52-90 ppb, respectively) on the foliar chemistry of more mature aspen trees of two different genotypes (216 and 259) growing out-of-doors at the Aspen Free Air CO2 Enrichment (FACE) facility near Rhinelander, Wisconsin, USA, as well as the impacts of these effects on the host plant preferences of forest tent caterpillar larvae.
In reporting the results of the study, Agrell et al. say that “the only chemical component showing a somewhat consistent covariation with larval preferences was condensed tannins,” noting that “the tree becoming relatively less preferred as a result of CO2 or O3 treatment was in general also the one for which average levels of condensed tannins were most positively (or least negatively) affected by that treatment.” The mean condensed tannin concen-trations of the aspen 216 and 259 genotypes were 25 percent and 57 percent higher, respectively, under the elevated CO2 and O3 combination treatment compared to the ambient CO2 and O3 combination treatment.
In light of these findings, it is logical to presume that as atmospheric concentrations of CO2 and O3 continue to rise, the increase in condensed tannin concentration likely to occur in the foliage of aspen trees should lead to their leaves becoming less preferred for consumption by the forest tent caterpillar.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/t/tanninsaspen.php.
Birch Trees
How do condensed tannin concentrations in the leaves and roots of paper birch (Betula papyrifera Marsh.) and silver birch (Betula pendula Roth) trees respond to atmospheric CO2 enrichment with and without concomitant increases in atmospheric temperature and ozone concentrations? We here briefly summarize the findings of several studies that have broached one or more parts of this question.
McDonald et al. (1999) grew paper birch seedlings in controlled environment greenhouses that were maintained at either ambient (387 ppm) or elevated (696 ppm) CO2 concentrations under conditions of either low or high light availability (half and full sunlight, respectively) for 31 days after the mean date of bud break. In doing so, they determined that under low light conditions the CO2-enriched seedlings exhibited an increase of approximately 15 percent in leaf condensed tannin concentration, while under high light conditions the CO2-induced tannin increase was a whopping 175 percent.
Peltonen et al. (2005) studied the impacts of doubled atmospheric CO2 and O3 concentrations on the accumulation of 27 phenolic compounds, including soluble condensed tannins, in the leaves of two European silver birch clones in seven-year-old soil-grown trees that were exposed in open-top chambers for three growing seasons to ambient and twice-ambient atmospheric CO2 and O3 concentrations singly and in combination. This work, which was carried out in central Finland, revealed that elevated CO2 increased the concentration of soluble condensed tannins in the leaves of the trees by 19 percent. In addition, they found that the elevated CO2 protected the leaves from elevated O3 because, as they describe it, “all the O3-derived effects on the leaf phenolics and traits were prevented by elevated CO2.”
Kuokkanen et al. (2003) grew two-year-old silver birch seedlings in ambient air of 350 ppm CO2 or air enriched to a CO2 concentration of 700 ppm under conditions of either ambient temperature or ambient temperature plus 3°C for one full growing season in the field in closed-top chambers at the Mekrijarvi Research Station of the University of Joensuu in eastern Finland. Then, during the middle of the summer, when carbon-based secondary compounds of birch leaves are fairly stable, they picked several leaves from each tree and determined their condensed tannin concentrations, along with the concentrations of a number of other physiologically important substances. This work revealed that the concentration of total phenolics, condensed tannins and their derivatives significantly increased in the leaves produced in the CO2-enriched air, as has also been observed by Lavola and Julkunen-Titto (1994), Williams et al. (1994), Kinney et al. (1997), Bezemer and Jones (1998) and Kuokkanen et al. (2001). In fact, the extra 350 ppm of CO2 nearly tripled condensed tannin concentrations in the ambient-temperature air, while it increased their concentrations in the elevated-temperature air by a factor in excess of 3.5.
In a study of roots, Parsons et al. (2003) grew two-year-old paper birch saplings in well-watered and fertilized 16-L pots from early May until late August in glasshouse rooms maintained at either 400 or 700 ppm CO2. This procedure revealed that the concentration of condensed tannins in the fine roots of the saplings was increased by 27 percent in the CO2-enriched treatment; and in regard to this finding, the researchers say “the higher condensed tannin concentrations that were present in the birch fine roots may offer these tissues greater protection against soil-borne pathogens and herbivores.”
Parsons et al. (2004) collected leaf litter samples from early September to mid-October beneath paper birch trees growing in ambient and CO2-enriched (to 200 ppm above ambient) FACE plots in northern Wisconsin, USA, which were also maintained under ambient and O3-enriched (to 19 ppb above ambient) conditions, after which the leaf mass produced in each treatment was determined, sub-samples of the leaves were assessed for a number of chemical constituents. The researchers learned that condensed tannin concentrations were 64 percent greater in the CO2-enriched plots. Under CO2- and O3-enriched conditions, condensed tannin concentrations were 99 percent greater.
In conclusion, it appears that elevated concentrations of atmospheric CO2 tend to increase leaf and fine-root tannin concentrations of birch trees, and that this phenomenon tends to protect the trees’ foliage from predation by voracious insect herbivores and protect the trees’ roots from soil-borne pathogens and herbivores.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/t/tanninsbirch.php.
Oak Trees
Dury et al. (1998) grew four-year-old pedunculate oak trees (Quercus robur L.) in pots within greenhouses maintained at ambient and twice-ambient atmospheric CO2 concentrations in combination with ambient and elevated (ambient plus 3°C) air temperatures for approximately one year. This work revealed that elevated CO2 had only minor and contrasting direct effects on leaf palatability: a temporary increase in foliar phenolic concentrations and decreases in leaf toughness and nitrogen content. The elevated temperature treatment, on the other hand, significantly reduced leaf palatability, because oak leaf toughness increased as a consequence of temperature-induced increases in condensed tannin concentrations. As a result, the researchers concluded that “a 3°C rise in temperature might be expected to result in prolonged larval development, increased food consumption, and reduced growth” for herbivores feeding on oak leaves in a CO2-enriched and warmer world of the future.
Cornelissen et al. (2003) studied fluctuating asymmetry in the leaves of two species of schlerophyllous oaks—myrtle oak (Quercus myrtifolia) and sand live oak (Quercus geminata)—that dominate a native scrub-oak community at the Kennedy Space Center, Titusville, Florida (USA). Fluctuating asymmetry is the term used to describe small variations from perfect symmetry in otherwise bilaterally symmetrical characters in an organism (Moller and Swaddle, 1997), which asymmetry is believed to arise as a consequence of developmental instabilities experienced during ontogeny that may be caused by various stresses, including both genetic and environmental factors (Moller and Shykoff, 1999).
Based on measurements of (1) distances from the leaf midrib to the left and right edges of the leaf at its widest point and (2) leaf areas on the left and right sides of the leaf midrib, Cornelissen et al. determined that “asymmetric leaves were less frequent in elevated CO2, and, when encountered, they were less asymmetric than leaves growing under ambient CO2.” In addition, they found that “Q. myrtifolia leaves under elevated CO2 were 15.0% larger than in ambient CO2 and Q. geminata leaves were 38.0 percent larger in elevated CO2 conditions.” They also determined that “elevated CO2 significantly increased tannin concentration for both Q. myrtifolia and Q. geminata leaves” and that “asymmetric leaves contained significantly lower concentrations of tannins than symmetric leaves for both Q. geminata and Q. myrtifolia.” Specifically, they found induced incfreases in tanning concentrations of approximately 35 percent for Q. myrtifolia and 43 percent for Q. geminata. In commenting on their primary findings of reduced percentages of leaves experiencing asymmetry in the presence of elevated levels of atmospheric CO2 and the lesser degree of asymmetry exhibited by affected leaves in the elevated CO2 treatment, Cornelissen et al. say that “a possible explanation for this pattern is the fact that, by contrast to other environmental stresses, which can cause negative effects on plant growth, the predominant effect of elevated CO2 on plants is to promote growth with consequent reallocation of resources (Docherty et al., 1996).” Another possibility they discuss “is the fact that CO2 acts as a plant fertilizer,” and, as a result, that “elevated CO2 ameliorates plant stress compared with ambient levels of CO2.”
In a subsequent study conducted at the Kennedy Space Center’s scrub-oak community, Hall et al. (2005b) evaluated foliar quality and herbivore damage in three oaks (Q. myrtifolia, Q. chapmanii and Q. geminata) plus the nitrogen-fixing legume Galactia elliottii at three-month intervals from May 2001 to May 2003, at which times samples of undamaged leaves were removed from each of the four species in all chambers and analyzed for various chemical constituents, while 200 randomly selected leaves of each species in each chamber were scored for the presence of six types of herbivore damage. Analyses of the data thereby obtained indicated that for condensed tannins, hydrolyzable tannins, total phenolics and lignin, in all four species there were always greater concentrations of all four leaf constituents in the CO2-enriched leaves, with across-species mean increases of 6.8 percent for condensed tannins, 6.1 percent for hydrolyzable tannins, 5.1 percent for total phenolics and 4.3 percent for lignin. In addition, there were large CO2-induced decreases in all leaf damage categories among all species: chewing (-48 percent), mines (-37 percent), eye spot gall (-45 percent), leaf tier (-52 percent), leaf mite (-23 percent) and leaf gall (-16 percent). Hall et al. thus concluded that the changes they observed in leaf chemical constituents and herbivore damage “suggest that damage to plants may decline as atmospheric CO2 levels continue to rise.”
Last, and largely overlapping the investigation of Hall et al. (2005b), was the study of Hall et al. (2005a), who evaluated the effects of the Kennedy Space Center experiment’s extra 350 ppm of CO2 on litter quality, herbivore activity, and their interactions, over the three-year-period 2000-2002. This endeavor indicated, in their words, that “changes in litter chemistry from year to year were far larger than effects of CO2 or insect damage, suggesting that these may have only minor effects on litter decomposition.” The one exception to this finding was that “condensed tannin concentrations increased under elevated CO2 regardless of species, herbivore damage, or growing season,” rising by 11 percent in 2000, 18 percent in 2001 and 41 percent in 2002 as a result of atmospheric CO2 enrichment, as best we can determine from the researchers’ bar graphs. Also, the five scientists report that “lepidopteran larvae can exhibit slower growth rates when feeding on elevated CO2 plants (Fajer et al., 1991) and become more susceptible to pathogens, parasitoids, and predators (Lindroth, 1996; Stiling et al., 1999),” noting further that at their field site, “which hosts the longest continuous study of the effects of elevated CO2 on insects, herbivore populations decline markedly under elevated CO2 (Stiling et al., 1999, 2002, 2003; Hall et al., 2005b).”
In conclusion, it would appear CO2-enriched air produces a large and continuous enhancement of condensed tannin concentrations in oak tree foliage, which causes marked declines in herbivore populations observed in CO2-enriched open-top-chamber studies.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/t/tanninsoak.php.
Transgenic Plants
Toxins produced by Bacillus thuringiensis (Bt) supplied to crops via foliar application have been used as a means of combating crop pests for well over half a century. More recently, the Bt gene for producing the toxin has been artificially inserted in some species of plants, producing transgenic plants that are pest resistant. The effectiveness of this management technique depends primarily upon the amount of Bt-produced toxins that are ingested by targeted insects. Another kind of transgenic plant is wheat that has been made heat resistant by the introduction into its gene code of heat shock protein (HSP) or plastidial EF-Tu (protein synthesis elongation factor). How does atmospheric CO2 enrichment affect transgenic plants?
If soil nitrogen levels are low, foliar nitrogen concentrations in plants grown in enhanced CO2 environments are generally reduced from what they are at the current atmospheric CO2 concentration, which suggests that insects would have to eat more foliage to get their normal requirement of nitrogen for proper growth and development in CO2-enriched air. But by eating more foliage, the insects would also ingest more Bt-produced toxins, and they would be more severely impacted by those substances.
To test this hypothesis, Coviella and Trumble (2000) grew cotton plants in each of six Teflon-film chambers in a temperature-controlled greenhouse, where three of the chambers were maintained at an atmospheric CO2 concentration of 370 ppm, and three were maintained at 900 ppm CO2. In addition, half of the plants in each chamber received high levels of nitrogen (N) fertilization, while half received low levels (30 vs. 130 mg N/kg soil/week). After 45 days of growth under these conditions, leaves were removed from the plants and dipped in a Bt solution, after which known amounts of treated leaf material were fed to Spodoptera exigua larvae and their responses measured and analyzed.
By these means, the two researchers determined that the plants grown in the elevated CO2 chambers did indeed have significantly lower foliar nitrogen concentrations than the plants grown in the ambient CO2 chambers under the low N fertilization regime; but this was not the case under the high N regime. They also discovered that older larvae fed with foliage grown in elevated CO2 with low N fertilization consumed significantly more plant material than insects fed with foliage grown in ambient CO2; but, again, no differences were observed with high N fertilization. Last, and “consistent with the effect of higher Bt toxin intake due to enhanced consumption,” they found that “insects fed on low N plants had significantly higher mortality in elevated CO2.” Yet, again, no such effect was evident in the high N treatment. Consequently, with respect to pest management using Bt-produced toxins supplied to crops via foliar application, Coviella and Trumble concluded that “increasing atmospheric CO2 is making the foliar applications more efficacious.”
Coviella et al. (2000), in an analogous experiment to that of Coviella and Trumble, grew cotton plants in 12 Teflon-film chambers in a temperature-controlled greenhouse, where six chambers were maintained at an atmospheric CO2 concentration of 370 ppm and six were maintained at 900 ppm CO2. Half of the cotton plants in each of these chambers were of a transgenic line containing the Bt gene for the production of the Cry1Ac toxin, which is mildly toxic for Spodoptera exigua, while the other half were of a near isogenic line without the Bt gene. In addition, and as before, half of the plants in each chamber received the same low and high levels of N fertilization; and between 40 and 45 days after emergence, leaves were removed from the plants and fed to the S. exigua larvae, after which a number of larval responses were measured and analyzed, along with various leaf properties.
This work revealed that the low-N plants in the elevated CO2 treatment had lower foliar N concentrations than did the low-N plants in the ambient CO2 treatment, and that the transgenic plants from the low-N, high CO2 treatment produced lower levels of Bt toxin than did the transgenic plants from the low-N, ambient CO2 treatment. In addition, the high level of N fertilization only partially compensated for this latter high-CO2 effect. In the ambient CO2 treatment there was also a significant increase in days to pupation for insects fed transgenic plants; but this difference was not evident in elevated CO2. In addition, pupal weight in ambient CO2 was significantly higher in non-transgenic plants; and, again, this difference was not observed in elevated CO2.
In discussing their findings, the three researchers wrote that “these results support the hypothesis that the lower N content per unit of plant tissue caused by the elevated CO2 will result in lower toxin production by transgenic plants when nitrogen supply to the plants is a limiting factor.” They also note that “elevated CO2 appears to eliminate differences between transgenic and non-transgenic plants for some key insect developmental/fitness variables including length of the larval stage and pupal weight.”
These findings suggest that in the case of inadvertent Bt gene transference to wild relatives of transgenic crop lines, elevated levels of atmospheric CO2 will tend to negate certain of the negative effects the wayward genes might otherwise inflict on the natural world. Hence, the ongoing rise in the air’s CO2 content could be said to constitute an “insurance policy” against this potential outcome.
On the other hand, Coviella et al.’s results also suggest that transgenic crops designed to produce Bt-type toxins may become less effective in carrying out the objectives of their design as the air’s CO2 content continues to rise. Coupling this possibility with the fact that the foliar application of Bacillus thuringiensis to crops should become even more effective in a higher-CO2 world, as found by Coviella and Trumble, one could argue that the implantation of toxin-producing genes in crops is not the way to go in the face of the ongoing rise in the air’s CO2 content, which reduces that technique’s effectiveness at the same time that it increases the effectiveness of direct foliar applications.
In a study of three different types of rice—a wild type (WT) and two transgenic varieties, one with 65 percent wild-type Rubisco (AS-77) and one with 40 percent wild-type Rubisco (AS-71)—Makino et al. (2000) grew plants from seed for 70 days in growth chambers maintained at 360 and 1000 ppm CO2, after which they harvested the plants and determined their biomass. In doing so, they found that the mean dry weights of the WT, AS-77 and AS-71 varieties grown in air of 360 ppm were, respectively, 5.75, 3.02 and 0.83 g, while in air of 1000 ppm CO2, corresponding mean dry weights were 7.90, 7.40 and 5.65 g. Consequently, although the growth rates of the genetically engineered rice plants were inferior to that of the wild type when grown in normal air of 360 ppm CO2 (with AS-71 producing less than 15 percent as much biomass as the wild type), when grown in air of 1000 ppm CO2 they experienced greater CO2-induced increases in growth: a 145 percent increase in the case of AS-77 and a 581 percent increase in the case of AS-71. Hence, whereas the transgenic plants were highly disadvantaged in normal air of 360 ppm CO2 (with AS-71 plants attaining a mean dry weight of only 0.83 g while the WT plants attained a mean dry weight of 5.75 g), they were found to be pretty much on an equal footing in highly CO2-enriched air (with AS-71 plants attaining a mean dry weight of 5.65 g while the WT plants attained a mean dry weight of 7.90 g). This finding bodes well for the application of this type of technology to rice crops in a future world of higher atmospheric CO2 content.
Returning to cotton, Chen et al. (2005) grew well watered and fertilized plants of two varieties—one expressing Cry1A (c) genes from Bacillus thurigiensis and a non-transgenic cultivar from the same recurrent parent—in pots placed within open-top chambers maintained at either 375 or 750 ppm CO2 in Sanhe County, Hebei Province, China, from planting in mid-May to harvest in October, throughout which period several immature bolls were collected and analyzed for various chemical characteristics, while others were stored under refrigerated conditions for later feeding to cotton bollworm larvae, whose growth characteristics were closely were monitored. In pursuing this protocol, the five researchers found that the elevated CO2 treatment increased immature boll concentrations of condensed tannins by approximately 22 percent and 26 percent in transgenic and non-transgenetic cotton, respectively (see Tannins in Section 7.8.7. for a discussion of the significance of this observation). In addition, they found that elevated CO2 slightly decreased the body biomass of the cotton bollworms and reduced moth fecundity. The Bt treatment was even more effective in this regard, and in the combined Bt-high-CO2 treatment, the negative cotton bollworm responses were expressed most strongly of all. Chen et al. concluded that the expected higher atmospheric CO2 concentrations of the future will “either not change or only slightly enhance the efficacy of Bt technology against cotton bollworms.”
Two years later, Chen et al. (2007) reported growing the same two cultivars under the same conditions from the time of planting on 10 May 2004 until the plants were harvested in October, after which egg masses of the cotton bollworms were reared in a growth chamber under ambient-CO2 conditions, while three successive generations of them were fed either transgenic or non-transgenic cotton bolls from plants grown in either ambient or twice-ambient atmospheric CO2 concentrations, during which time a number of physiological characteristics of the cotton bollworms were periodically assessed. This work revealed, in the words of Chen et al., that “both elevated CO2 and transgenic Bt cotton increased larval lifespan,” but that they decreased “pupal weight, survival rate, fecundity, frass output, relative and mean relative growth rates, and the efficiency of conversion of ingested and digested food.” As a result, they say that “transgenic Bt cotton significantly decreased the population-trend index compared to non-transgenic cotton for the three successive bollworm generations, especially at elevated CO2 [our italics].”
Based on these findings, the four researchers concluded that the negative effects of elevated CO2 on cotton bollworm physiology and population dynamics “may intensify through successive generations,” in agreement with the findings of Brooks and Whittaker (1998, 1999) and Wu et al. (2006). They additionally concluded that “both elevated CO2 and transgenic Bt cotton are adverse environmental factors for cotton bollworm long-term population growth,” and that the combination of the two factors may intensify their adverse impact on the population performance of the cotton bollworm, which would be good news for cotton growers.
Fu et al. (2008) note that “heat stress is a major constraint to wheat production and negatively impacts grain quality, causing tremendous economic losses, and may become a more troublesome factor due to global warming.” Consequently, as they describe it, they “introduced into wheat the maize gene coding for plastidal EF-Tu [protein synthesis elongation factor],” in order to assess “the expression of the transgene, and its effect on thermal aggregation of leaf proteins in transgenic plants,” as well as “the heat stability of photosynthetic membranes (thylakoids) and the rate of CO2 fixation in young transgenic plants following exposure to heat stress.” These operations led, in their words, “to improved protection of leaf proteins against thermal aggregation, reduced damage to thylakoid membranes and enhanced photosynthetic capability following exposure to heat stress,” which results “support the concept that EF-Tu ameliorates negative effects of heat stress by acting as a molecular chaperone.”
Fu et al. describe their work as “the first demonstration that a gene other than HSP [heat shock protein] gene can be used for improvement of heat tolerance,” noting it also indicates that the improvement is possible in a species that has a complex genome, such as hexaploid wheat. They conclude by stating their results “strongly suggest that heat tolerance of wheat, and possibly other crop plants, can be improved by modulating expression of plastidal EF-Tu and/or by selection of genotypes with increased endogenous levels of this protein.”
In summary, genetic alterations to crop plants enable them to better withstand the assaults of insects pests or increases in seasonal maximum air temperates. Elevated CO2 either improves or does not change the effectiveness of genetic alternatives to achieve these objectives, while it simultaneously reduces the severity of possible negative effects that could arise from the escape of transplanted genes into the natural environment.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/t/summaries/transgenicplants.php.
Isoprene
Isoprene (C5H8 or 2-methyl-1,3-butadiene) is a highly reactive non-methane hydrocarbon (NMHC) that is emitted in copious quantities by vegetation and is responsible for the production of vast amounts of tropospheric ozone (Chameides et al., 1988; Harley et al., 1999), which is a debilitating scourge of plant and animal life alike. Poisson et al. (2000) calculate that current levels of NMHC emissions—the vast majority of which are isoprene, accounting for more than twice as much as all other NMHCs combined—may increase surface ozone concentrations by up to 40 percent in the marine boundary-layer and 50-60 percent over land. They further estimate that the current tropospheric ozone content extends the atmospheric lifetime of methane—one of the world’s most powerful greenhouse gases—by approximately 14 percent. Consequently, it can be appreciated that reducing isoprene emissions from vegetation is to be desired.
Although a few experiments conducted on certain plant species have suggested that elevated concentrations of atmospheric CO2 have little to no effect on their emissions of isoprene (Buckley, 2001; Baraldi et al., 2004; Rapparini et al., 2004), a much larger number of other experiments are suggestive of substantial CO2-induced reductions in isoprene emissions, as demonstrated by the work of Monson and Fall (1989), Loreto and Sharkey (1990), Sharkey et al. (1991) and Loreto et al. (2001).
Rosentiel et al. (2003) studied three 50-tree cottonwood plantations growing in separate mesocosms within the forestry section of the Biosphere 2 facility near Oracle, Arizona, USA, one of which mesocosms was maintained at an atmospheric CO2 concentration of 430 ppm, while the other two were enriched to concentrations of 800 and 1200 ppm for one entire growing season. Integrated over that period, the total above-ground biomass of the trees in the latter two mesocosms was increased by 60 percent and 82 percent, respectively, while their production of isoprene was decreased by 21 percent and 41 percent, respectively.
Scholefield et al. (2004) measured isoprene emissions from Phragmites australis plants (one of the world’s most important natural grasses) growing at different distances from a natural CO2 spring in central Italy. At the specific locations they chose to make their measurements, atmospheric CO2 concentrations of approximately 350, 400, 550 and 800 ppm had likely prevailed for the entire lifetimes of the plants. Across this CO2 gradient, plant isoprene emissions dropped ever lower as the air’s CO2 concentration rose ever higher. Over the first 50-ppm CO2 increase, isoprene emissions were reduced to approximately 65 percent of what they were at ambient CO2, while for CO2 increases of 200 and 450 ppm, they were reduced to only about 30 percent and 7 percent of what they were in the 350-ppm-CO2 air. The researchers note that these reductions were likely caused by reductions in leaf isoprene synthase, which was observed to be highly correlated with isoprene emissions, leading them to conclude that “elevated CO2 generally inhibits the expression of isoprenoid synthesis genes and isoprene synthase activity which may, in turn, limit formation of every chloroplast-derived isoprenoid.” They state that the “basal emission rate of isoprene is likely to be reduced under future elevated CO2 levels.”
Centritto et al. (2004) grew hybrid poplar saplings for one full growing season in a FACE facility located at Rapolano, Italy, where the air’s CO2 concentration was increased by approximately 200 ppm. Their study demonstrated that “isoprene emission is reduced in elevated CO2, in terms of both maximum values of isoprene emission rate and isoprene emission per unit of leaf area averaged across the total number of leaves per plant,” which in their case amounted to a reduction of approximately 34 percent. When isoprene emission was summed over the entire plant profile, however, the reduction was not nearly so great (only 6 percent), because of the greater number of leaves on the CO2-enriched saplings. “However,” as they state, “Centritto et al. (1999), in a study with potted cherry seedlings grown in open-top chambers, and Gielen et al. (2001), in a study with poplar saplings exposed to FACE, showed that the stimulation of total leaf area in response to elevated CO2 was a transient effect, because it occurred only during the first year of growth.” Hence, they concluded “it may be expected that with similar levels of leaf area, the integrated emission of isoprene would have been much lower in elevated CO2.” Indeed, they say that their data, “as well as that reported by Scholefield et al. (2004), in a companion experiment on Phragmites growing in a nearby CO2 spring, mostly confirm that isoprene emission is inversely dependent on CO2 [concentration] when this is above ambient, and suggests that a lower fraction of C will be re-emitted in the atmosphere as isoprene by single leaves in the future.”
Working at another FACE facility, the Aspen FACE facility near Rhinelander, Wisconsin, USA, Calfapietra et al. (2008) measured emissions of isoprene from sun-exposed upper-canopy leaves of an O3-tolerant clone and an O3-sensitive clone of trembling aspen (Populus tremuloides Michx.) trees that were growing in either normal ambient air, air enriched with an extra 190-200 ppm CO2, air with 1.5 times the normal ozone concentration, or air simultaneously enriched with the identical concentrations of both of these atmospheric trace gases. Results of their analysis showed that for the trees growing in air of ambient ozone concentration, the extra 190 ppm of CO2 decreased the mean isoprene emission rate by 11.7 percent in the O3-tolerant aspen clone and by 22.7 percent in the O3-sensitive clone, while for the trees growing in air with 1.5 times the ambient ozone concentration, the extra CO2 also decreased the mean isoprene emission rate by 10.4 percent in the O3-tolerant clone and by 32.7 percent in the O3-sensitive clone. At the same time, and in the same order, net photosynthesis rates were increased by 34.9 percent, 47.4 percent, 31.6 percent and 18.9 percent.
Possell et al. (2004) grew seedlings of English oak (Quercus robur), one to a mesocosm (16 cm diameter, 60 cm deep), in either fertilized or unfertilized soil in solardomes maintained at atmospheric CO2 concentrations of either ambient or ambient plus 300 ppm for one full year, at the conclusion of which period they measured rates of isoprene emissions from the trees’ foliage together with their rates of photosynthesis. In the unfertilized trees, this work revealed that the 300-ppm increase in the air’s CO2 concentration reduced isoprene emissions by 63 percent on a leaf area basis and 64 percent on a biomass basis, while in the fertilized trees the extra CO2 reduced isoprene emissions by 70 percent on a leaf area basis and 74 percent on a biomass basis. In addition, the extra CO2 boosted leaf photosynthesis rates by 17 percent in the unfertilized trees and 13 percent in the fertilized trees.
Possell et al. (2005) performed multiple three-week-long experiments with two known isoprene-emitting herbaceous species (Mucuna pruriens and Arundo donax), which they grew in controlled environment chambers that were maintained at two different sets of day/night temperatures (29/24°C and 24/18°C) and atmospheric CO2 concentrations characteristic of glacial (180 ppm), pre-industrial (280 ppm) and current (366 ppm) conditions, where canopy isoprene emission rates were measured on the final day of each experiment. They obtained what they describe as “the first empirical evidence for the enhancement of isoprene production, on a unit leaf area basis, by plants that grew and developed in [a] CO2-depleted atmosphere,” which results, in their words, “support earlier findings from short-term studies with woody species (Monson and Fall, 1989; Loreto and Sharkey, 1990).” Then, combining their emission rate data with those of Rosenstiel et al. (2003) for Populus deltoides, Centritto et al. (2004) for Populus x euroamericana and Scholefield et al. (2004) for Phragmites australis, they developed a single downward-trending isoprene emissions curve that stretches all the way from 180 to 1200 ppm CO2, where it asymptotically approaches a value that is an order of magnitude less than what it is at 180 ppm.
Working at the Biosphere 2 facility near Oracle, Arizona, USA, in enclosed ultraviolet light-depleted mesocosms (to minimize isoprene depletion by atmospheric oxidative reactions such as those involving OH), Pegoraro et al. (2005) studied the effects of atmospheric CO2 enrichment (1200 ppm compared to an ambient concentration of 430 ppm) and drought on the emission of isoprene from cottonwood (Populus deltoides Bartr.) foliage and its absorption by the underlying soil for both well-watered and drought conditions. In doing so, they found that “under well-watered conditions in the agriforest stands, gross isoprene production (i.e., the total production flux minus the soil uptake) was inhibited by elevated CO2 and the highest emission fluxes of isoprene were attained in the lowest CO2 treatment.” In more quantitative terms, it was determined that the elevated CO2 treatment resulted in a 46 percent reduction in gross isoprene production. In addition, it was found that drought suppressed the isoprene sink capacity of the soil beneath the trees, but that “the full sink capacity of dry soil was recovered within a few hours upon rewetting.”
Putting a slightly negative slant on their findings, Pegoraro et al. suggested that “in future, potentially hotter, drier environments, higher CO2 may not mitigate isoprene emission as much as previously suggested.” However, we note that climate models generally predict an intensification of the hydrologic cycle in response to rising atmospheric CO2 concentrations, and that the anti-transpirant effect of atmospheric CO2 enrichment typically leads to increases in the moisture contents of soils beneath vegetation. Also, we note that over the latter decades of the twentieth century, when the IPCC claims the earth warmed at a rate and to a level that were unprecedented over the past two millennia, soil moisture data from all around the world tended to display upward trends. Robock et al. (2000), for example, developed a massive collection of soil moisture data from over 600 stations spread across a variety of climatic regimes, including the former Soviet Union, China, Mongolia, India and the United States, determining that “In contrast to predictions of summer desiccation with increasing temperatures, for the stations with the longest records, summer soil moisture in the top 1 m has increased while temperatures have risen.” And in a subsequent study of “45 years of gravimetrically observed plant available soil moisture for the top 1 m of soil, observed every 10 days for April-October for 141 stations from fields with either winter or spring cereals from the Ukraine for 1958-2002,” Robock et al. (2005) discovered that these real-world observations “show a positive soil moisture trend for the entire period of observation,” noting that “even though for the entire period there is a small upward trend in temperature and a downward trend in summer precipitation, the soil moisture still has an upward trend for both winter and summer cereals.” Consequently, in a CO2-enriched world of the future, we likely will have the best of both aspects of isoprene activity: less production by vegetation and more consumption by soils.
Finally, we address the issue of how well models predict the response of isoprene emission to future global change. According to Monson et al. (2007) such predictions “probably contain large errors,” which clearly need to be corrected. The reason for the errors, write the twelve researchers who conducted the study, is that “the fundamental logic of such models is that changes in NPP [net primary production] will produce more or less biomass capable of emitting isoprene, and changes in climate will stimulate or inhibit emissions per unit of biomass.” They continue, “these models tend to ignore the discovery that there are direct effects of changes in the atmospheric CO2 concentration on isoprene emission that tend to work in the opposite direction to that of stimulated NPP,” as has been indicated in the research studies described above. Their results showed, in their words, “that growth in an atmosphere of elevated CO2 inhibited the emission of isoprene at levels that completely compensate for possible increases in emission due to increases in aboveground NPP.”
In lamenting this sorry state of global-change modeling, Monson et al. say that, “to a large extent, the modeling has ‘raced ahead’ of our mechanistic understanding of how isoprene emissions will respond to the fundamental drivers of global change,” and that “without inclusion of these effects in the current array of models being used to predict changes in atmospheric chemistry due to global change, one has to question the relevance of the predictions.”
A year later, Arneth et al. (2008) used a mechanistic isoprene-dynamic vegetation model of European woody vegetation to “investigate the interactive effects of climate and CO2 concentration on forest productivity, species composition, and isoprene emissions for the periods 1981-2000 and 2081-2100,” which included a parameterization of the now-well-established direct CO2-isoprene inhibition phenomenon we have described in the papers above. The study found that “across the model domain,” the CO2-isoprene inhibition effect “has the potential to offset the stimulation of [isoprene] emissions that could be expected from warmer temperatures and from the increased productivity and leaf area of emitting vegetation.”
In view of these findings, it appears the ongoing rise in the atmosphere’s CO2 concentration will lead to ever greater reductions in atmospheric isoprene concentrations. As noted in the introductory paragraph of this section, such a consequence would be welcome news for man and nature.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/i/isoprene.php.
Microorganisms
Plants grown in CO2-enriched atmospheres nearly always exhibit increased photosynthetic rates and biomass production. Due to this productivity enhancement, more plant material is typically added to soils from root growth, turnover and exudation, as well as from leaves and stems following their abscission and falling to the ground during senescence. Such additions of carbon onto and into soils often serve as the only carbon source for supporting the development and growth of microorganisms in terrestrial habitats. Thus, it is important to understand how CO2-induced increases in plant growth affect microorganisms, a topic omitted from discussion by the IPCC.
Several studies have shown that atmospheric CO2 enrichment does not significantly impact soil microorganisms. Zak et al. (2000), for example, observed no significant differences in soil microbial biomass beneath aspen seedlings grown at 350 and 700 ppm CO2 after 2.5 years of differential treatment. Likewise, in the cases of Griffiths et al. (1998) and Insam et al. (1999), neither research team reported any changes in microbial community structure beneath ryegrass and artificial tropical ecosystems, respectively, after subjecting them to atmospheric CO2 enrichment.
Other studies, however, have found that elevated CO2 can significantly affect soil microorganisms. Van Ginkel and Gorissen (1998) observed that three months of elevated CO2 exposure (700 ppm) increased soil microbial biomass beneath ryegrass plants by 42 percent relative to that produced under ambient CO2 conditions, as did Van Ginkel et al. (2000). Likewise, soil microbial biomass was reported to increase by 15 percent beneath agricultural fields subjected to a two-year wheat-soybean crop rotation (Islam et al., 2000). In a study by Marilley et al. (1999), atmospheric CO2 enrichment significantly increased bacterial numbers in the rhizospheres beneath ryegrass and white clover monocultures. Similarly, Lussenhop et al. (1998) reported CO2-induced increases in the amounts of bacteria, protozoa, and microarthropods in soils that had supported regenerating poplar tree cuttings for five months. In addition, Hungate et al. (2000) reported that twice-ambient CO2 concentrations significantly increased the biomass of active fungal organisms and flagellated protozoa beneath serpentine and sandstone grasslands after four years of treatment exposure.
In taking a closer look at the study of Marilley et al. (1999), it is evident that elevated CO2 caused shifts in soil microbial populations. In soils beneath their leguminous white clover, for example, elevated CO2 favored shifts towards Rhizobium bacterial species, which likely increased nitrogen availability—via nitrogen fixation—to support enhanced plant growth. However, in soils beneath non-leguminous ryegrass monocultures, which do not form symbiotic relationships with Rhizobium species, elevated CO2 favored shifts towards Pseudomonas species, which likely acquired nutrients to support enhanced plant growth through mechanisms other than nitrogen fixation. Nonetheless, in both situations, the authors observed CO2-induced shifts in bacterial populations that would likely optimize nutrient acquisition for specific host plant species.
In an unrelated study, Montealegre et al. (2000) reported that elevated CO2 acted as a selective agent among 120 different isolates of Rhizobium growing beneath white clover plants. Specifically, when bacterial strains favored by ambient and elevated CO2 concentrations were mixed together and grown with white clover at an atmospheric CO2 concentration of 600 ppm, 17 percent more root nodules were formed by isolates previously determined to be favored by elevated CO2.
Hu et al. (2001) subjected fertile sandstone grasslands to five years of twice-ambient CO2 concentrations and found they exhibited increased soil microbial biomass while simultaneously enhancing plant nitrogen uptake. The net effect of these phenomena reduced nitrogen availability for microbial use, which consequently decreased microbial respiration and, hence, microbial decomposition. Consequently, these ecosystems displayed CO2-induced increases in net carbon accumulation. Similarly, Williams et al. (2000) reported that microbial biomass carbon increased by 4 percent in a tallgrass prairie after five years exposure to twice-ambient CO2 concentrations, which contributed to a total soil carbon enhancement of 8 percent.
In summation, as the CO2 content of the air continues to rise, earth’s vegetation will likely respond with increasing photosynthetic rates and biomass production, returning more organic carbon to the soil where it will be utilized by microbial organisms to maintain or increase their population numbers, biomass and heterotrophic activities (Weihong et al., 2000; Arnone and Bohlen, 1998). Shifts in microbial community structure may occur that will favor the intricate relationships that currently exist between leguminous and non-leguminous plants and the specific microorganisms upon which they depend.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/m/microorganisms.php.
Worms
Perhaps the best known worm in the world is the common earthworm. How will it be affected as the air’s CO2 content continues to climb, and how will its various responses affect the biosphere? What about other worms? How will they fare in a CO2-enriched world of the future, and what will be the results of their responses?
“Earthworms,” in the words of Edwards (1988), “play a major role in improving and maintaining the fertility, structure, aeration and drainage of agricultural soils.” As noted by Sharpley et al. (1988), “by ingestion and digestion of plant residue and subsequent egestion of cast material, earthworms can redistribute nutrients in a soil and enhance enzyme activity, thereby increasing plant availability of both soil and plant residue nutrients,” as others have also demonstrated (Bertsch et al., 1988; McCabe et al., 1988; Zachmann and Molina, 1988). Kemper (1988) describes how “burrows opened to the surface by surface-feeding worms provide drainage for water accumulating on the surface during intense rainfall,” noting that “the highly compacted soil surrounding the expanded burrows has low permeability to water which often allows water to flow through these holes for a meter or so before it is sorbed into the surrounding soil.”
Hall and Dudas (1988) report that the presence of earthworms appears to mitigate the deleterious effects of certain soil toxins. Logsdon and Linden (1988) describe a number of other beneficial effects of earthworms, including (1) enhancement of soil aeration, since under wet conditions earthworm channels do not swell shut as many soil cracks do, (2) enhancement of soil water uptake, since roots can explore deeper soil layers by following earthworm channels, and (3) enhancement of nutrient uptake, since earthworm casts and channel walls have a more neutral pH and higher available nutrient level than bulk soil. Hence, we should care about what happens to earthworms as the air’s CO2 content rises because of the many important services they provide for earth’s plant life.
Edwards (1988) says “the most important factor in maintaining good earthworm populations in agricultural soils is that there be adequate availability of organic matter,” while Hendrix et al. (1988) and Kladivko (1988) report that greater levels of plant productivity promote greater levels of earthworm activity. Consequently, since the most ubiquitous and powerful effect of atmospheric CO2 enrichment is its stimulation of plant productivity, which leads to enhanced organic matter delivery to soils, it logically follows that this aerial fertilization effect of the ongoing rise in the air’s CO2 content should increase earthworm populations and amplify the many beneficial services they provide for plants.
The second most significant and common effect of atmospheric CO2 enrichment on plants is its antitranspirant effect, whereby elevated levels of atmospheric CO2 reduce leaf stomatal apertures and slow the rate of evaporative water loss from the vast bulk of earth’s vegetation. Both growth chamber studies and field experiments that have studied this phenomenon provide voluminous evidence that it often leads to increased soil water contents in many terrestrial ecosystems, which also benefits earthworm populations.
Zaller and Arnone (1997) fumigated open-top and -bottom chambers in a calcareous grassland near Basal, Switzerland with air of either 350 or 600 ppm CO2 for an entire growing season. They found that the mean annual soil moisture content in the CO2-enriched chambers was 10 percent greater than that observed in the ambient-air chambers, and because rates of surface cast production by earthworms are typically positively correlated with soil moisture content, they found that cumulative surface cast production after only one year was 35 percent greater in the CO2-enriched chambers than in the control chambers. In addition, because earthworm casts are rich in organic carbon and nitrogen, the cumulative amount of these important nutrients on a per-land-area basis was found to be 28 percent greater in the CO2-enriched chambers than it was in the ambient-air chambers. In a subsequent study of the same grassland, Zaller and Arnone (1999) found that plants growing in close proximity to the earthworm casts produced more biomass than similar plants growing further away from them. They also found that the CO2-induced growth stimulation experienced by the various grasses was also greater for those plants growing nearer the earthworm casts.
These various observations suggest that atmospheric CO2 enrichment sets in motion a self-enhancing cycle of positive biological phenomena, whereby increases in the air’s CO2 content (1) stimulate plant productivity and (2) reduce plant evaporative water loss, which results in (3) more organic matter entering the soil and (4) a longer soil moisture retention time and/or greater soil water contents, all of which factors lead to (5) the development of larger and more active earthworm populations, which (6) enhance many important soil properties, including fertility, structure, aeration and drainage, which improved properties (7) further enhance the growth of the plants whose CO2-induced increase in productivity was the factor that started the whole series of processes in the first place.
More earthworms also can increase soil’s ability to sequester carbon. As Jongmans et al. (2003) point out, “the rate of organic matter decomposition can be decreased in worm casts compared to bulk soil aggregates (Martin, 1991; Haynes and Fraser, 1998).” On the basis of these studies and their own micro-morphological investigation of structural development and organic matter distribution in two calcareous marine loam soils on which pear trees had been grown for 45 years (one of which soils exhibited little to no earthworm activity and one of which exhibited high earthworm activity, due to different levels of heavy metal contamination of the soils as a consequence of the prior use of different amounts of fungicides), they concluded that “earthworms play an important role in the intimate mixing of organic residues and fine mineral soil particles and the formation of organic matter-rich micro-aggregates and can, therefore, contribute to physical protection of organic matter, thereby slowing down organic matter turnover and increasing the soil’s potential for carbon sequestration.” Put more simply, atmospheric CO2 enrichment that stimulates the activity of earthworms also leads to more—and more secure—sequestration of carbon in earth’s soils.
Don et al. (2008) studied the effects of anecic earthworms—which generally inhabit a single vertical burrow throughout their entire lives that can be as much as five meters in depth, but is generally in the range of one to two meters—on soil carbon stocks and turnover via analyses of enzyme activity, stable isotopes, nuclear magnetic resonance spectroscopy, and the 14C age of their burrow linings. The results of their study indicated that “the carbon distribution in soils is changed by anecic earthworms’ activity with more carbon stored in the subsoil where earthworms slightly increase the carbon stocks.” In this regard they also state that “the translocation of carbon from [the] organic layer to the subsoil will decrease the carbon vulnerability to mineralization,” since “carbon in the organic layer and the surface soil is much more prone to disturbances with rapid carbon loss than subsoil carbon.”
Bossuyt et al. (2005) conducted a pair of experiments designed to investigate “at what scale and how quickly earthworms manage to protect SOM [soil organic matter].” In the first experiment, soil aggregate size distribution together with total C and 13C were measured in three treatments—control soil, soil + 13C-labeled sorghum leaf residue, and soil + 13C-labeled residue + earthworms—after a period of 20 days incubation, where earthworms were added after the eighth day. In the second experiment, they determined the protected C and 13C pools inside the newly formed casts and macro- and micro-soil-aggregates. Results indicated that the proportion of large water-stable macroaggregates was on average 3.6 times greater in the soil-residue samples that contained earthworms than in those that lacked earthworms, and that the macroaggregates in the earthworm treatment contained approximately three times more sequestered carbon. What is more, the earthworms were found to form “a significant pool of protected C in microaggregates within large macroaggregates after 12 days of incubation,” thereby demonstrating the rapidity with which earthworms perform their vital function of sequestering carbon in soils when plant residues become available to them.
Cole et al. (2002) report that “in the peatlands of northern England, which are classified as blanket peat, it has been suggested that the potential effects of global warming on carbon and nutrient dynamics will be related to the activities of dominant soil fauna, and especially enchytraeid worms.” In harmony with these ideas, Cole et al. say they “hypothesized” that warming would lead to increased enchytraeid worm activity, which would lead to higher grazing pressure on microbes in the soil; and since enchytraeid grazing has been observed to enhance microbial activity (Cole et al., 2000), they further hypothesized that more carbon would be liberated in dissolved organic form, “supporting the view that global warming will increase carbon loss from blanket peat ecosystems.”
The scientists next describe how they constructed small microcosms from soil and litter they collected near the summit of Great Dun Fell, Cumbria, England. Subsequent to “defaunating” this material by reducing its temperature to -80°C for 24 hours, they thawed and inoculated it with native soil microbes, after which half of the microcosms were incubated in the dark at 12°C and half at 18°C, the former of which temperatures was approximately equal to mean August soil temperature at a depth of 10 cm at the site of soil collection, while the latter was said by them to be “close to model predictions for soil warming that might result from a doubling of CO2 in blanket peat environments.”
Ten seedlings of an indigenous grass of blanket peat were then transplanted into each of the microcosms, while 100 enchytraeid worms were added to each of half of the mini-ecosystems. These procedures resulted in the creation of four experimental treatments: ambient temperature, ambient temperature + enchytraeid worms, elevated temperature, and elevated temperature + enchytraeid worms. The resulting 48 microcosms—sufficient to destructively harvest three replicates of each treatment four different times throughout the course of the 64-day experiment—were arranged in a fully randomized design and maintained at either 12 or 18°C with alternating 12-hour light and dark periods. In addition, throughout the entire course of the study, the microcosms were given distilled water every two days to maintain their original weights.
So what did the researchers find? First, and contrary to their hypothesis, elevated temperature reduced the ability of the enchytraeid worms to enhance the loss of carbon from the microcosms. At the normal ambient temperature, for example, the presence of the worms enhanced dissolved organic carbon (DOC) loss by 16 percent, while at the elevated temperature expected for a doubling of the air’s CO2 content, the worms had no effect at all on DOC. In addition, Cole et al. note that “warming may cause drying at the soil surface, forcing enchytraeids to burrow to deeper subsurface horizons.” Hence, since the worms are known to have little influence on soil carbon dynamics below a depth of 4 cm (Cole et al., 2000), they concluded that this additional consequence of warming would further reduce the ability of enchytraeids to enhance carbon loss from blanket peatlands.
In summarizing their findings, Cole et al. say that “the soil biotic response to warming in this study was negative.” That is, it was of such a nature that it resulted in a reduced loss of carbon to the atmosphere, which would tend to slow the rate of rise of the air’s CO2 content, just as was suggested by the results of the study of Jongmans et al.
Yeates et al. (2003) report results from a season-long FACE study of a 30-year-old New Zealand pasture, where three experimental plots had been maintained at the ambient atmospheric CO2 concentration of 360 ppm and three others at a concentration of 475 ppm (a CO2 enhancement of only 32 percent) for a period of four to five years. The pasture contained about twenty species of plants, including C3 and C4 grasses, legumes and forbs. Nematode, or “roundworm,” populations increased significantly in response to the 32 percent increase in the air’s CO2 concentration. Of the various feeding groups studied, Yeates et al. report that the relative increase “was lowest in bacterial-feeders (27%), slightly higher in plant (root) feeders (32%), while those with delicate stylets (or narrow lumens; plant-associated, fungal-feeding) increased more (52% and 57%, respectively).” The greatest nematode increases were recorded among omnivores (97 percent) and predators (105 percent). Most dramatic of all, root-feeding populations of the Longidorus nematode taxon rose by 330 percent. Also increasing in abundance were earthworms: Aporrectodea caliginosa by 25 percent and Lumbricus rubellus by 58 percent. Enchytraeids, on the other hand, decreased in abundance, by approximately 30 percent.
With respect to earthworms, Yeates et al. note that just as was found in the studies cited in the first part of this review, the introduction of lumbricids has been demonstrated to improve soil conditions in New Zealand pastures (Stockdill, 1982), which benefits pasture plants. Hence, the CO2-induced increase in earthworm numbers observed in Yeates et al.’s study would be expected to do more of the same, while the reduced abundance of enchytraeids they documented in the CO2-enriched pasture would supposedly lead to less carbon being released to the air from the soil, as per the known ability of enchytraeids to promote carbon loss from British peat lands under current temperatures.
In summary, the lowly earthworm and still lowlier soil nematodes respond to increases in the air’s CO2 content via a number of plant-mediated phenomena in ways that further enhance the positive effects of atmospheric CO2 enrichment on plant growth and development, while at the same time helping to sequester more carbon more securely in the soil.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/e/earthworms.php.
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