Amelioration of Environmental Stresses
From ClimateWiki
From Climate Change Reconsidered, a work of the Nongovernmental International Panel on Climate Change
Atmospheric CO2 enrichment has been shown to help ameliorate the detrimental effects of several environmental stresses on plant growth and development, including disease, herbivory (predation by insects), shade (caused by increased cloudiness), ozone (a common air pollutant), low temperatures, nitrogen deficiency, UV-B radiation, and water stress. In this section we survey research on each of these types of stress.
Additional information on this topic, including reviews on stresses not discussed here, can be found at http://www.co2science.org/subject/g/subject_g.php under the heading Growth Response to CO2 with Other Variables.
Contents |
Disease
According to the IPCC, CO2-induced global warming will increase the risk of plant disease outbreaks, resulting in negative consequences for food, fiber, and forestry across all world regions (IPCC, 2007-II). But it appears the IPCC has omitted the results of real-world observations that contradict this forecast.
Chakraborty and Datta (2003) note there are a number of CO2-induced changes in plant physiology, anatomy and morphology that have been implicated in increased plant resistance to disease and that “can potentially enhance host resistance at elevated CO2.” Among these phenomena they list “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.”
Malmstrom and Field (1997) grew individual oat plants for two months in pots placed within phytocells maintained at atmospheric CO2 concentrations of 350 and 700 ppm, while they infected one-third of the plants with the barley yellow dwarf virus (BYDV), which plagues more than 150 plant species worldwide, including all major cereal crops. Over the course of their study, they found that elevated CO2 stimulated rates of net photosynthesis in all plants, regardless of pathogen infection. However, the greatest percentage increase occurred in diseased individuals (48 percent vs. 34 percent). Moreover, atmospheric CO2 enrichment decreased stomatal conductance by 50 percent in infected plants but by only 34 percent in healthy ones, which led to a CO2-induced doubling of the instantaneous water-use efficiency of the healthy plants, but an increase of fully 2.7-fold in the diseased plants. Last, after 60 days of growth under these conditions, they determined that the extra CO2 increased total plant biomass by 36 percent in infected plants, but by only 12 percent in healthy plants. In addition, while elevated CO2 had little effect on root growth in the healthy plants, it increased root biomass in the infected plants by up to 60 percent. Consequently, it can be appreciated that as the CO2 content of the air continues to rise, its many positive effects will likely offset some, if not most, of the negative effects of the destructive BYDV. Quoting Malmstrom and Field with respect to two specific examples, they say in their concluding remarks 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 plants from germination to maturity in controlled-environment chambers maintained at ambient (377 ppm) and elevated (612 ppm) concentrations of atmospheric CO2 and at ambient (20 ppb) and elevated (61 ppb) concentrations of ozone (and combinations thereof), the latter of which gases is typically toxic to most plants. In addition, half of the plants in each treatment were inoculated with a leaf rust-causing fungus. Under these conditions, the elevated CO2 increased the photosynthetic rates of the diseased plants by 20 and 42 percent at the ambient and elevated ozone concentrations, respectively. It also enhanced the yield of the infected plants, increasing it by 57 percent, even in the presence of high ozone concentrations.
Jwa and Walling (2001) grew tomato plants hydroponically for eight weeks in controlled-environment chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm. In addition, at week five of the study, half of all plants growing in each CO2 concentration were infected with a fungal pathogen that attacks plant roots and induces a water stress that decreases growth and yield. At the end of the study, they found that the pathogenic infection had reduced total plant biomass by nearly 30 percent at both atmospheric CO2 concentrations. However, the elevated CO2 had increased the total biomass of the healthy and diseased plants by the same amount (+30 percent), with the result that the infected tomato plants grown at 700 ppm CO2 had biomass values that were essentially identical to those of the healthy tomato plants grown at 350 ppm CO2. Thus, the extra CO2 completely counterbalanced the negative effect of the pathogenic infection on overall plant productivity.
Chakraborty and Datta (2003) studied the aggressiveness of the fungal anthracnose pathogen Colletotrichum gloeosporioides by inoculating 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 25 sequential infection cycles in controlled-environment chambers filled with air of either 350 or 700 ppm CO2. By these means they determined that the aggressiveness of the pathogen was reduced at the twice-ambient level of atmospheric CO2, where aggressiveness is defined as “a property of the pathogen reflecting the relative amount of damage caused to the host without regard to resistance genes (Shaner et al., 1992).” As they describe it, “at twice-ambient CO2 the overall level of aggressiveness of the two [pathogen] isolates was significantly reduced on both cultivars.”
Simultaneously, however, pathogen fecundity was found to increase at twice-ambient CO2. Of this finding, Chakraborty and Datta 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, according to Chakraborty and Datta, is that the overall increase in fecundity at high CO2 “is a reflection of the altered canopy environment,” wherein “the 30% larger S. scabra plants at high CO2 (Chakraborty et al., 2000) makes the canopy microclimate more conducive to anthracnose development.”
In view of these opposing changes in pathogen behavior at elevated levels of atmospheric CO2, it is difficult to know the outcome of atmospheric CO2 enrichment for this specific 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. What is more, results could also 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 gives us reason to believe that plants will gain the advantage as the air’s CO2 content continues to climb in the years ahead.
Another study that fuels this optimism was conducted by Parsons et al. (2003), who grew two-year-old saplings of paper birch and three-year-old saplings of sugar maple in well-watered and fertilized pots from early May until late August in glasshouse rooms maintained at either 400 or 700 ppm CO2. In these circumstances, the whole-plant biomass of paper birch was increased by 55 percent in the CO2-enriched portions of the glasshouse, while that of sugar maple was increased by 30 percent. Also, concentrations of condensed tannins were increased by 27 percent in the paper birch (but not the sugar maple) saplings grown in the CO2-enriched air; in light of this finding, Parsons et al. conclude that “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.”
Within this context, it is interesting to note that Parsons et al. report that CO2-induced increases in fine root concentrations of total phenolics and condensed tannins have also been observed in warm temperate conifers by King et al. (1997), Entry et al. (1998), Gebauer et al. (1998), and Runion et al. (1999), as well as in cotton by Booker (2000).
In another intriguing study, Gamper et al. (2004) begin by noting that arbuscular mycorrhizal fungi (AMF) are expected to modulate plant responses to elevated CO2 by “increasing resistance/tolerance of plants against an array of environmental stressors (Smith and Read, 1997).” In investigating this subject in a set of experiments conducted over a seven-year period of free-air CO2-enrichment on two of the world’s most extensively grown cool-season forage crops (Lolium perenne and Trifolium repens) at the Swiss free-air CO2 enrichment (FACE) facility near Zurich, they determined that “at elevated CO2 and under [two] N treatments, AMF root colonization of both host plant species was increased,” and that “colonization levels of all three measured intraradical AMF structures (hyphae, arbuscules and vesicles) tended to be higher.” Hence, they concluded that these CO2-induced benefits may lead to “increased protection against pathogens and/or herbivores.”
Pangga et al. (2004) grew well-watered and fertilized seedlings of a cultivar (Fitzroy) of the pencilflower (Stylosanthes scabra)—an important legume crop that is susceptible to anthracnose disease caused by Colletotrichum gloeosporioides (Penz.) Penz. & Sacc.—within a controlled-environment facility maintained at atmospheric CO2 concentrations of either 350 or 700 ppm, where they inoculated six-, nine- and 12-week-old plants with conidia of C. gloeosporioides. Then, 10 days after inoculation, they counted the anthracnose lesions on the plants and classified them as either resistant or susceptible.
Adherence to this protocol revealed, in their words, 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.” In fact, with respect to the plants inoculated at 12 weeks of age, they say that those grown “at 350 ppm had 60 and 75% more susceptible and resistant lesions per leaf, respectively, than those [grown] at 700 ppm CO2.”
In terms of infection efficiency (IE), 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, they report that “at 700 ppm CO2, IE 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.” Consequently, as the air’s CO2 content continues to rise, it would appear that the Fitzroy cultivar of the pasture legume Stylosanthes scabra will acquire a greater intrinsic resistance to the devastating anthracnose disease.
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).”
What underlying mechanism or mechanisms 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.” In addition, they concluded that reduced disease severity under elevated CO2 was also 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.” Indeed, they state that their results “provide concrete evidence for a potentially generalizable mechanism to predict disease outcomes in other pathosystems under future climatic conditions.”
Matros et al. (2006) grew tobacco plants (Nicotiana tabacum L.) in 16-cm-diameter pots filled with quartz sand in controlled-climate chambers maintained at either 350 or 1,000 ppm CO2 for a period of eight weeks, where they were irrigated daily with a complete nutrient solution containing either 5 or 8 mM NH4NO3. In addition, some of the plants in each treatment were mechanically infected with the potato virus Y (PVY) when they were six weeks old. Then, at the end of the study, the plants were harvested and a number of their chemical constitutes identified and quantified.
This work revealed, in the researchers words, that “plants grown at elevated CO2 and 5 mM NH4NO3 showed a marked and significant decrease in content of nicotine in leaves as well as in roots,” while at 8 mM NH4NO3 the same was found to be true of upper leaves but not of lower leaves and roots. With respect to the PVY part of the study, they further report that the “plants grown at high CO2 showed a markedly decreased spread of virus.” Both of these findings would likely be considered beneficial by most people, as potato virus Y is an economically important virus that infects many crops and ornamental plants throughout the world, while nicotine is nearly universally acknowledged to have significant negative impacts on human health (Topliss et al., 2002).
Braga et al. (2006) conducted three independent experiments where they grew well-watered soybean (Glycine max (L.) Merr) plants of two cultivars (IAC-14, susceptible to stem canker disease, and IAC-18, resistant to stem canker disease) from seed through the cotyledon stage in five-liter pots placed within open-top chambers maintained at atmospheric CO2 concentrations of either 360 or 720 ppm in a glasshouse, while they measured various plant properties and processes, concentrating on the production of glyceollins (the major phytoalexins, or anti-microbial compounds, produced in soybeans) in response to the application of ß-glucan elicitor (derived from mycelial walls of Phythophthora sojae) to carefully created and replicated wounds in the surfaces of several soybean cotyledons. In doing so, they found that the IAC-14 cultivar did not exhibit a CO2-induced change in glyceollin production in response to elicitation—as Braga et al. had hypothesized would be the case, since this cultivar is susceptible to stem canker disease—but they found that the IAC-18 cultivar (which has the potential to resist the disease to varying degrees) experienced a 100 percent CO2-induced increase in the amount of glyceollins produced after elicitation, a response the researchers described as remarkable. As for its significance, Braga et al. say the CO2-induced response they observed “may increase the potential of the soybean defense since infection at early stages of plant development, followed by a long incubation period before symptoms appear, is characteristic of the stem canker disease cycle caused by Dpm [Diaporthe phaseolorum (Cooke & Ellis) Sacc. f. sp. meridionalis Morgan-Jones].” They say the response they observed “indicates that raised CO2 levels forecasted for next decades may have a real impact on the defensive chemistry of the cultivars.”
Last, in a study conducted within the BioCON (Biodiversity, Carbon dioxide, and Nitrogen effects on ecosystem functioning) FACE facility located at the Cedar Creek Natural History Area in east-central Minnesota, USA, Strengbom and Reich (2006) evaluated the effects of an approximate 190-ppm increase in the air’s daytime CO2 concentration on leaf photosynthetic rates of stiff goldenrod (Solidago rigida) growing in monoculture for two full seasons, together with its concomitant effects on the incidence and severity of leaf spot disease. Although they found that elevated CO2 had no significant effect on plant photosynthetic rate in their study, they report that “both disease incidence and severity were lower on plants grown under elevated CO2.” More specifically, they found that “disease incidence was on average more than twice as high [our italics] under ambient as under elevated CO2,” and that “disease severity (proportion of leaf area with lesions) was on average 67% lower under elevated CO2 compared to ambient conditions.”
In discussing their results, Strengbom and Reich say the “indirect effects from elevated CO2, i.e., lower disease incidence, had a stronger effect on realized photosynthetic rate than the direct effect of higher CO2,” which as noted above was negligible in their study. They conclude “it may be necessary to consider potential changes in susceptibility to foliar diseases to correctly estimate the effects on plant photosynthetic rates of elevated CO2.” In addition, they note that the plants grown in CO2-enriched air had lower leaf nitrogen concentrations than the plants grown in ambient air, as is often observed in studies of this type; and they say that their results “are, thus, also in accordance with other studies that have found reduced pathogen performance following reduced nitrogen concentration in plants grown under elevated CO2 (Thompson and Drake, 1994).” What is more, they conclude that their results are “also in accordance with studies that have found increased [disease] susceptibility following increased nitrogen concentration of host plants (Huber and Watson, 1974; Nordin et al., 1998; Strengbom et al., 2002).” It is possible, therefore, that the ongoing rise in the air’s CO2 content may help many plants of the future reduce the deleterious impacts of various pathogenic fungal diseases that currently beset them, thereby enabling them to increase their productivities above and beyond what is typically provided by the more direct growth stimulation resulting from the aerial fertilization effect of elevated atmospheric CO2 concentrations.
In summation, the bulk of the available data shows atmospheric CO2 enrichment asserts its greatest positive influence on infected as opposed to healthy plants. Moreover, it would appear that elevated CO2 has the ability to significantly ameliorate the deleterious effects of various stresses imposed upon plants by numerous pathogenic invaders. Consequently, as the atmosphere’s CO2 concentration continues its upward climb, earth’s vegetation should be increasingly better equipped to successfully deal with pathogenic organisms and the damage they have traditionally done to mankind’s crops, as well as to the plants that sustain the rest of the planet’s animal life.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/disease.php
Herbivory
Insect pests have greatly vexed earth’s plants in the past and will likely continue to do so in the future. It is possible, however, that the ongoing rise in the atmosphere’s CO2 content may affect this phenomenon, for better or for worse. In this section we review the results of several studies that have addressed this subject as it applies to herbaceous and woody plants.
Additional information on this topic, including reviews on herbivory not discussed here, can be found at http://www.co2science.org/subject/h/subject_h.php under the heading Herbivory.
Herbaceous Plants
Kerslake et al. (1998) grew five-year-old heather (Calluna vulgaris) plants collected from a Scottish moor in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 600 ppm. At two different times during the study, larvae of the destructive winter moth Operophtera brumata—whose outbreaks periodically cause extensive damage to heather moorland—were allowed to feed upon current-year shoots. Feeding upon the high-CO2-grown foliage did not affect larval growth rates, development, or final pupal weights; neither was moth survivorship significantly altered. The authors concluded that their study “provides no evidence that increasing atmospheric CO2 concentrations will affect the potential for outbreak of Operophtera brumata on this host.” What it did show, however, was a significant CO2-induced increase in heather water use efficiency.
Newman et al. (1999) inoculated tall fescue (Festuca arundinacea) plants growing in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm with bird cherry-oat aphids (Rhopalosiphum padi). After nine weeks, the plants growing in the CO2-enriched air had experienced a 37 percent increase in productivity and were covered with many fewer aphids than the plants growing in ambient air.
Goverde et al. (1999) collected four genotypes of Lotus corniculatus near Paris and grew them in controlled environment chambers kept at atmospheric CO2 concentrations of 350 and 700 ppm. Larvae of the Common Blue Butterfly (Polyommatus icarus) that were allowed to feed upon the foliage produced in the CO2-enriched air ate more, grew larger, and experienced shorter development times than larvae feeding on the foliage produced in the ambient-air treatment, suggesting that this butterfly species will likely become more robust and plentiful as the air’s CO2 content continues to rise.
Brooks and Whittaker (1999) removed grassland monoliths containing eggs of the xylem-feeding spittlebug Neophilaenus lineatus from the UK’s Great Dun Fell in Cumbria and placed them in glasshouses maintained at atmospheric CO2 concentrations of 350 and 600 ppm for two years. Survival of the spittlebug’s nymphal states was reduced by 24 percent in both of the generations produced in their experiment, suggesting that this particular insect will likely cause less tissue damage to the plants of this species-poor grassland in a CO2-enriched world of the future.
Joutei et al. (2000) grew bean (Phaseolus vulgaris) plants in controlled environments kept at atmospheric CO2 concentrations of 350 and 700 ppm, to which they introduced the destructive agricultural mite Tetranychus urticae, observing that female mites produced 34 percent and 49 percent less offspring in the CO2-enriched chambers in their first and second generations, respectively. This CO2-induced reduction in the reproductive success of this invasive insect, which negatively affects more than 150 crop species worldwide, bodes well for mankind’s ability to grow the food we will need to feed our growing numbers in the years ahead.
Peters et al. (2000) fed foliage derived from FACE plots of calcareous grasslands of Switzerland (maintained at 350 and 650 ppm CO2) to terrestrial slugs, finding they exhibited no preference with respect to the CO2 treatment from which the foliage was derived. Also, in a study that targeted no specific insect pest, Castells et al. (2002) found that a doubling of the air’s CO2 content enhanced the total phenolic concentrations of two Mediterranean perennial grasses (Dactylis glomerata and Bromus erectus) by 15 percent and 87 percent, respectively, which compounds tend to enhance plant defensive and resistance mechanisms to attacks by both herbivores and pathogens.
Coviella and Trumbel (2000) determined that toxins produced by Bacillus thuringiensis (Bt), which are applied to crop plants by spraying as a means of combating various crop pests, were “more efficacious” in cotton grown in an elevated CO2 environment than in ambient air, which is a big plus for modern agriculture. In addition, Coviella et al. (2000) determined that “elevated CO2 appears to eliminate differences between transgenic [Bt-containing] and nontransgenic plants for some key insect developmental/fitness variables including length of the larval stage and pupal weight.”
In summary, the majority of evidence that has been accumulated to date suggests that rising atmospheric CO2 concentrations may reduce the frequency and severity of pest outbreaks that are detrimental to agriculture, while not seriously impacting herbivorous organisms found in natural ecosystems that are normally viewed in a more favorable light.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/h/herbivoresherbplants.php.
Woody Plants
Maple
Working with Acer rubrum saplings beginning their fourth year of growth in open-top chambers maintained at four different atmospheric CO2/temperature conditions—(1) ambient temperature, ambient CO2, (2) ambient temperature, elevated CO2 (ambient + 300 ppm), (3) elevated temperature (ambient + 3.5°C), ambient CO2, and (4) elevated temperature, elevated CO2—Williams et al. (2003) bagged first instar gypsy moth larvae on various branches of the trees and observed their behavior. The data they obtained demonstrated, in their words, “that larvae feeding on CO2-enriched foliage ate a comparably poorer food source than those feeding on ambient CO2-grown plants, irrespective of temperature,” and that there was a minor reduction in leaf water content due to CO2 enrichment. Nevertheless, they found the “CO2-induced reductions in foliage quality (e.g. nitrogen and water) were unrelated [our italics] to insect mortality, development rate and pupal weight,” and that these and any other phytochemical changes that may have occurred “resulted in no negative effects on gypsy moth performance.” They also found that “irrespective of CO2 concentration, on average, male larvae pupated 7.5 days earlier and female larvae 8 days earlier at elevated temperature,” and noting that anything that prolongs the various development stages of insects potentially exposes them to greater predation and parasitism risk, they concluded that the observed temperature-induced hastening of the insects’ development would likely expose them to less predation and parasitism risk.
One year later, Hamilton et al. (2004) began the report of their study of this important subject by noting that many single-species investigations have suggested that increases in atmospheric CO2 will increase herbivory (Bezemer and Jones, 1998; Cannon, 1998; Coviella and Trumble, 1999; Hunter, 2001; Lincoln et al., 1993; Whittaker, 1999). However, because there are so many feedbacks and complex interactions among the numerous components of real-world ecosystems, they warned that one ought not put too much faith in these predictions until relevant real-world ecosystem-level experiments have been completed.
In one such study they conducted at the Duke Forest FACE facility near Chapel Hill, North Carolina, USA, Hamilton et al. “measured the amount of leaf tissue damaged by insects and other herbivorous arthropods during two growing seasons in a deciduous forest understory continuously exposed to ambient (360 ppm) and elevated (560 ppm) CO2 conditions.” This forest is dominated by loblolly pine trees that account for fully 92 percent of the ecosystem’s total woody biomass. In addition, it contains 48 species of other woody plants (trees, shrubs, and vines) that have naturally established themselves in the forest’s understory. In their study of this ecosystem, Hamilton et al. quantified the loss of foliage due to herbivory that was experienced by three deciduous tree species, one of which was Acer rubrum.
As Hamilton et al. describe it, “we found that elevated CO2 led to a trend toward reduced herbivory [our italics] in [the] deciduous understory in a situation that included the full complement of naturally occurring plant and insect species.” In 1999, for example, they determined that “elevated CO2 reduced overall herbivory by more than 40 percent,” while in 2000 they say they observed “the same pattern and magnitude of reduction.”
With respect to changes in foliage properties that might have been expected to lead to increases in herbivory, Hamilton et al. report they “found no evidence for significant changes in leaf nitrogen, C/N ratio, sugar, starch or total leaf phenolics in either year of [the] study,” noting that these findings agree with those of “another study performed at the Duke Forest FACE site that also found no effect of elevated CO2 on the chemical composition of leaves of understory trees (Finzi and Schlesinger, 2002).”
Hamilton et al. thus concluded their landmark paper by emphasizing that “despite the large number of studies that predict increased herbivory, particularly from leaf chewers, under elevated CO2, our study found a trend toward reduced herbivory two years in a row.” In addition, they note that their real-world results “agree with the only other large-scale field experiment that quantified herbivory for a community exposed to elevated CO2 (Stiling et al., 2003).”
Consequently, and in spite of the predictions of increased destruction of natural ecosystems by insects and other herbivorous arthropods in a CO2-enriched world of the future, just the opposite would appear to be the more likely outcome; i.e., greater plant productivity plus less foliage consumption by herbivores, “whether expressed on an absolute or a percent basis,” as Hamilton et al. found to be the case in their study.
In another study conducted at the same site, Knepp et al. (2005) quantified leaf damage by chewing insects on saplings of seven species (including Acer rubrum) in 2001, 2002, and 2003, while five additional species (including Acer barbatum) were included in 2001 and 2003. This work revealed, in their words, that “across the seven species that were measured in each of the three years, elevated CO2 caused a reduction in the percentage of leaf area removed by chewing insects,” which was such that “the percentage of leaf tissue damaged by insect herbivores was 3.8 percent per leaf under ambient CO2 and 3.3 percent per leaf under elevated CO2.” Greatest effects were observed in 2001, when they report that “across 12 species the average damage per leaf under ambient CO2 was 3.1 percent compared with 1.7 percent for plants under elevated CO2,” which was “indicative of a 46 percent decrease in the total area and total mass of leaf tissue damaged by chewing insects in the elevated CO2 plots.”
What was responsible for these welcome results? Knepp et al. say that “given the consistent reduction in herbivory under high CO2 across species in 2001, it appears that some universal feature of chemistry or structure that affected leaf suitability was altered by the treatment.” Another possibility they discuss is that “forest herbivory may decrease under elevated CO2 because of a decline in the abundance of chewing insects,” citing the observations of Stiling et al. (2002) to this effect and noting that “slower rates of development under elevated CO2 prolongs the time that insect herbivores are susceptible to natural enemies, which may be abundant in open-top chambers and FACE experiments but absent from greenhouse experiments.” In addition, they suggest that “decreased foliar quality and increased per capita consumption under elevated CO2 may increase exposure to toxins and insect mortality,” also noting that “CO2-induced changes in host plant quality directly decrease insect fecundity,” citing the work of Coviella and Trumble (1999) and Awmack and Leather (2002).
So what’s the bottom line with respect to the outlook for earth’s forests, and especially its maple trees, in a high-CO2 world of the future? In their concluding paragraph, Knepp et al. say that “By contrast to the view that herbivore damage will increase under elevated CO2 as a result of compensatory feeding on lower quality foliage, our results and those of Stiling et al. (2002) and Hamilton et al. (2004) in open experimental systems suggest that damage to trees may decrease.”
But what if herbivore-induced damage in fact increases in a future CO2-enriched world? The likely answer is provided by the work of Kruger et al. (1998), who grew well-watered and fertilized one-year-old Acer saccharum saplings in glasshouses maintained at atmospheric CO2 concentrations of either 356 or 645 ppm for 70 days to determine the effects of elevated CO2 on photosynthesis and growth. In addition, on the 49th day of differential CO2 exposure, 50 percent of the saplings’ leaf area was removed from half of the trees in order to study the impact of simulated herbivory. This protocol revealed that the 70-day CO2 enrichment treatment increased the total dry weight of the non-defoliated seedlings by about 10 percent. When the trees were stressed by simulated herbivory, however, the CO2-enriched maples produced 28 percent more dry weight over the final phase of the study than the maples in the ambient-air treatment did. This result thus led Kruger et al. to conclude that in a high-CO2 world of the future “sugar maple might be more capable of tolerating severe defoliation events which in the past have been implicated in widespread maple declines.”
It appears that earth’s maple trees—and probably many, if not most, other trees—will fare much better in the future with respect to the periodic assaults of leaf-damaging herbivores, as the air’s CO2 content continues its upward climb.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/h/herbivoresmaple.php.
Oak
Dury et al. (1998) grew four-year-old Quercus robur seedlings in pots in 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 to study the interactive effects of elevated CO2 and temperature on leaf nutritional quality. In doing so, they found that the elevated air temperature treatment significantly reduced leaf palatability, and that leaf toughness increased as a consequence of temperature-induced increases in condensed tannin concentrations. In addition, the higher temperatures significantly reduced leaf nitrogen content, while elevated CO2 caused a temporary increase in leaf phenolic concentrations and a decrease in leaf nitrogen content.
In one of the first attempts to move outside the laboratory/greenhouse and study the effects of atmospheric CO2 enrichment on trophic food webs in a natural ecosystem, Stiling et al. (1999) enclosed portions of a native scrub-oak community in Florida (USA) within 3.6-m-diameter open-top chambers and fumigated them with air having CO2 concentrations of either 350 or 700 ppm for approximately one year, in order to see if elevated CO2 would impact leaf miner densities, feeding rates, and mortality in this nutrient-poor ecosystem.
Adherence to this protocol led to the finding that total leaf miner densities were 38 percent less on the foliage of trees growing in CO2-enriched air than on the foliage of trees growing in ambient air. In addition, atmospheric CO2 enrichment consistently reduced the absolute numbers of the study’s six leaf miner species. At the same time, however, the elevated CO2 treatment increased the leaf area consumed by the less abundant herbivore miners by approximately 40 percent relative to the areas mined by the more abundant herbivores present on the foliage exposed to ambient air; but in spite of this increase in feeding, the leaf miners in the CO2-enriched chambers experienced significantly greater mortality than those in the ambient-air chambers. Although CO2-induced reductions in leaf nitrogen content played a role in this phenomenon, the greatest factor contributing to increased herbivore mortality was a four-fold increase in parasitization by various wasps, which could more readily detect the more-exposed leaf miners on the CO2-enriched foliage.
If extended to agricultural ecosystems, these findings suggest that crops may experience less damage from such herbivores in a high-CO2 world of the future, thus increasing potential harvest and economic gains. In addition, with reduced numbers of leaf miners in CO2-enriched air, farmers could reduce their dependency upon chemical pesticides to control them.
In another study conducted on five scrub-oak forest species at the same experimental facility, Stiling et al. (2003) investigated the effects of an approximate doubling of the air’s CO2 concentration on a number of characteristics of several insect herbivores. As before, they found that the “relative levels of damage by the two most common herbivore guilds, leaf-mining moths and leaf-chewers (primarily larval lepidopterans and grasshoppers), were significantly lower in elevated CO2 than in ambient CO2, for all five plant species,” and they found that “the response to elevated CO2 was the same across all plant species.” In addition, they report that “more host-plant induced mortality was found for all miners on all plants in elevated CO2 than in ambient CO2.” These effects were so powerful that in addition to the relative densities of insect herbivores being reduced in the CO2-enriched chambers, and “even though there were more leaves of most plant species in the elevated CO2 chambers,” the total densities of leaf miners in the high-CO2 chambers were also lower for all plant species. Consequently, it would appear that in a high-CO2 world of the future, many of earth’s plants may be able to better withstand the onslaughts of various insect pests that have plagued them in the past. Another intriguing implication of this finding, as Stiling et al. note, is that “reductions in herbivore loads in elevated CO2 could boost plant growth beyond what might be expected based on pure plant responses to elevated CO2.”
Continuing to investigate the same ecosystem, which is dominated by two species of scrub oak (Quercus geminata and Q. myrtifolia) that account for more than 90 percent of the ecosystem’s biomass, and focusing on the abundance of a guild of lepidopteran leafminers that attack the leaves of Q. myrtifolia, as well as various leaf chewers that also like to munch on this species, Rossi et al. (2004) followed 100 marked leaves in each of 16 open-top chambers (half exposed to ambient air and half exposed to air containing an extra 350 ppm of CO2) for a total of nine months, after which, in their words, “differences in mean percent of leaves with leafminers and chewed leaves on trees from ambient and elevated chambers were assessed using paired t-tests.”
In reporting their findings the researchers wrote that “both the abundance of the guild of leafmining lepidopterans and damage caused by leaf chewing insects attacking myrtle oak were depressed in elevated CO2.” Specifically, they found that leafminer abundance was 44 percent lower (P = 0.096) in the CO2-enriched chambers compared to the ambient-air chambers, and that the abundance of leaves suffering chewing damage was 37 percent lower (P = 0.072) in the CO2-enriched air. The implications of these findings are obvious: Myrtle oak trees growing in their natural habitat will likely suffer less damage from both leaf miners and leaf chewers as the air’s CO2 concentration continues to rise in the years and decades ahead.
Still concentrating on the same ecosystem, where atmospheric enrichment with an extra 350 ppm of CO2 was begun in May 1996, Hall et al. (2005b) studied the four species that dominate the community and are present in every experimental chamber: the three oaks (Quercus myrtifolia, Q. chapmanii and Q. geminata) plus the nitrogen-fixing legume Galactia elliottii. At three-month intervals from May 2001 to May 2003, undamaged leaves were removed from each of these 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.
Throughout the study there were no significant differences between the CO2-enriched and ambient-treatment leaves of any single species in terms of either condensed tannins, hydrolyzable tannins, total phenolics, or lignin. However, in all four species together there were always greater concentrations of all four leaf constituents in the CO2-enriched leaves, with accross-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 and often significant CO2-induced decreases in all leaf damage categories among all species: chewing (-48 percent, P < 0.001), mines (-37 percent, P = 0.001), eye spot gall (-45 percent, P < 0.001), leaf tier (-52 percent, P = 0.012), leaf mite (-23 percent, P = 0.477), and leaf gall (-16 percent, P = 0.480). 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.”
In one additional study to come out of the Florida scrub-oak ecosystem, Hall et al. (2005a) studied the effects of an extra 350 ppm of CO2 on litter quality, herbivore activity and their interactions. Over the three years of this experiment (2000, 2001, 2002), they determined 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, in their words, 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 their bar graphs. Also, the five researchers 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[d] markedly under elevated CO2 (Stiling et al., 1999, 2002, 2003; Hall et al., 2005b).”
In conclusion, from the evidence accumulated to date with respect to herbivory in oak trees, it would appear that ever less damage will be done to such trees by various insect pests as the air’s CO2 concentration continues to climb ever higher.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/h/herbivoreswoodoak.php.
Other
Stiling et al. (1999) enclosed portions of a Florida scrub-oak community in open-top chambers and maintained them at atmospheric CO2 concentrations of 350 and 700 ppm for approximately one year, while they studied the effects of this treatment on destructive leaf miners. Among their many findings, the researchers noted that the individual areas consumed by leaf miners munching on leaves in the CO2-enriched chambers were larger than those created by leaf miners dining on leaves in the ambient-air chambers. As a result, there was a four-fold increase in parasitization by various wasps that could more readily detect the more-exposed leaf miners on the CO2-enriched foliage. Consequently, leaf miners in the elevated CO2 chambers suffered significantly greater mortality than those in the control chambers.
In a subsequent and much expanded study of the same ecosystem, Stiling et al. (2002) investigated several characteristics of a number of insect herbivores found on the five species of plants that accounted for more than 98 percent of the total plant biomass within the chambers. As they describe their results, the “relative levels of damage by the two most common herbivore guilds, leaf-mining moths and leaf-chewers (primarily larval lepidopterans and grasshoppers), were significantly lower in elevated CO2 than in ambient CO2, for all five plant species.”
In another study that did not involve herbivores, Gleadow et al. (1998) grew eucalyptus seedlings in glasshouses maintained at 400 and 800 ppm CO2 for a period of six months, observing biomass increases of 98 percent and 134 percent in high and low nitrogen treatments, respectively. They also studied a sugar-based compound called prunasin, which produces cyanide in response to tissue damage caused by foraging herbivores. Although elevated CO2 caused no significant change in leaf prunasin content, it was determined that the proportion of nitrogen allocated to prunasin increased by approximately 20 percent in the CO2-enriched saplings, suggestive of a potential for increased prunasin production had the saplings been under attack by herbivores.
Lovelock et al. (1999) grew seedlings of the tropical tree Copaifera aromatica for 50 days in pots placed within open-top chambers maintained at atmospheric CO2 concentrations of 390 and 860 ppm. At the 14-day point of the experiment, half of the seedlings in each treatment had about 40 percent of their total leaf area removed. In this case, none of the defoliated trees of either CO2 treatment fully recovered from this manipulation, but at the end of the experiment, the total plant biomass of the defoliated trees in the CO2-enriched treatment was 15 percent greater than that of the defoliated trees in the ambient-CO2 treatment, again attesting to the benefits of atmospheric CO2 enrichment in helping trees to deal with herbivory.
Docherty et al. (1997) grew beech and sycamore saplings in glasshouses maintained at atmospheric CO2 concentrations of 350 and 600 ppm, while groups of three sap-feeding aphid species and two sap-feeding leafhopper species were allowed to feed on them. Overall, elevated CO2 had few significant effects on the performance of the insects, although there was a non-significant tendency for elevated CO2 to reduce the individual weights and population sizes of the aphids.
Finally, Hattenschwiler and Schafellner (1999) grew seven-year-old spruce (Picea abies) trees at atmospheric CO2 concentrations of 280, 420, and 560 ppm and various nitrogen deposition treatments for three years, allowing nun moth larvae to feed on current-year needles for a period of 12 days. Larvae placed upon the CO2-enriched foliage consumed less needle biomass than larvae placed upon the ambiently grown foliage, regardless of nitrogen treatment. This effect was so pronounced that the larvae feeding on needles produced by the CO2-enriched trees attained an average final biomass that was only two-thirds of that attained by the larvae that fed on needles produced at 280 ppm CO2. Since the nun moth is a deadly defoliator that resides in most parts of Europe and East Asia between 40° and 60°N latitude and is commonly regarded as the coniferous counterpart of its close relative the gypsy moth, which feeds primarily on deciduous trees, the results of this study suggest that the ongoing rise in the air’s CO2 content will likely lead to significant reductions in damage to spruce and other coniferous trees by this voracious insect pest in the years and decades ahead.
In light of these several observations, the balance of evidence seems to suggest that earth’s woody plants will be better able to deal with the challenges provided by herbivorus insects as the air’s CO2 content continues 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/h/herbivoreswoodyplants.php.
Insects
As the atmosphere’s CO2 concentration climbs ever higher, it is important to determine how this phenomenon will affect the delicate balance that exists between earth’s plants and the insects that feed on them. In this section we thus review what has been learned about this subject with respect to aphids, moths, and other insects.
Additional information on this topic, including reviews on insects not discussed here, can be found at http://www.co2science.org/subject/i/subject_i.php under the heading Insects.
Aphids
Docherty et al. (1997) grew beech and sycamore saplings in glasshouses maintained at atmospheric CO2 concentrations of 350 and 600 ppm, while groups of three sap-feeding aphid species were allowed to feed on the saplings. Overall, the elevated CO2 had few significant effects on aphid feeding and performance. There was, however, a non-significant tendency for elevated CO2 to reduce the individual weights and population sizes of the aphids, suggesting that future increases in the air’s CO2 content might reduce aphid feeding pressures on beech and sycamore saplings, and possibly other plants as well.
Whittaker (1999) reviewed the scientific literature dealing with population responses of herbivorous insects to atmospheric CO2 enrichment, concentrating on papers resulting from relatively long-term studies. Based on all pertinent research reports available at that time, the only herbivorous insects that exhibited population increases in response to elevated CO2 exposure were those classified as phloem feeders, specifically, aphids. Although this finding appeared to favor aphids over plants, additional studies would complicate the issue and swing the pendulum back the other way.
Newman et al. (1999) grew tall fescue plants for two weeks in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm before inoculating them with aphids (Rhopalosiphum padi). After nine additional weeks of differential CO2 exposure, the plants were harvested and their associated aphids counted. Although elevated CO2 increased plant dry matter production by 37 percent, the plants grown in air of elevated CO2 concentration contained fewer aphids than the plants grown in ambient air.
Percy et al. (2002) grew the most widely distributed tree species in all of North America—trembling aspen—in twelve 30-m-diameter FACE rings in air maintained at (1) ambient CO2 and O3 concentrations, (2) ambient O3 and elevated CO2 (560 ppm during daylight hours), (3) ambient CO2 and elevated O3 (46.4-55.5 ppb during daylight hours), and (4) elevated CO2 and O3 over each growing season from 1998 through 2001. Throughout their experiment they assessed a number of the young trees’ growth characteristics, as well as the responses of the sap-feeding aphid Chaitophorus stevensis, which they say “infests aspen throughout its range.” This experiment revealed that, by itself, elevated CO2 did not affect aphid abundance, but it increased the densities of natural enemies of the aphids, which over the long term would tend to reduce aphid numbers. Also, by itself, elevated O3 did not affect aphid abundance, but it had a strong negative effect on natural enemies of aphids, which over the long term would tend to increase aphid numbers. When both trace gases were applied together, elevated CO2 completely counteracted the reduction in the abundance of natural enemies of aphids caused by elevated O3. Hence, elevated CO2 tended to reduce the negative impact of aphids on trembling aspen in this comprehensive study.
At about the same time, Holopainen (2002) reviewed the scientific literature dealing with the joint effects of elevated concentrations of atmospheric O3 and CO2 on aphid-plant interactions. After compiling the results of 26 pertinent studies, it was found that atmospheric CO2 enrichment increased aphid performance in six studies, decreased it in six studies, and had no significant impact on it in the remaining 14 studies. Similar results were found for aphid-plant interactions in the presence of elevated O3 concentrations.
Newman (2003) reviewed what was known and not known about aphid responses to concurrent increases in atmospheric CO2 and air temperature, while also investigating the subject via the aphid population model of Newman et al. (2003). This literature review and model analysis led him to conclude that when the air’s CO2 concentration and temperature are both elevated, “aphid population dynamics will be more similar to current ambient conditions than expected from the results of experiments studying either factor alone.” We can draw only the general conclusion, according to Newman, that “insect responses to CO2 are unlikely to all be in the same direction.” Nevertheless, he says that “the lack of a simple common phenomenon does not deny that there is some overriding generality in the responses by the system.” It’s just that we did not at that time know what that overriding generality was, which is why experimental work on the subject has continued apace.
Concentrating on thermal effects alone, Ma et al. (2004) conducted detailed experiments on the effects of high temperature, period of exposure, and developmental stage on the survival of the aphid Metopolophium dirhodum, which they say “is the most abundant of the three cereal aphid species in Germany and central European countries.” This protocol revealed, in their words, that “temperatures over 29°C for 8 hours significantly reduced survival, which decreased generally as the temperature increased.” They also determined that “exposing aphids to 32.5°C for 4 hours or longer significantly reduced survival,” and that “mature aphids had a lower tolerance of high temperatures than nymphs.” In light of what they observed, therefore, as well as what a number of other scientists had observed, Ma et al. concluded that “global warming may play a role in the long-term changes in the population abundance of M. dirhodum.” Specifically, they say that “an increase in TX [daily average temperature] of 1°C and MaxT [maximum daily temperature] of 1.3°C during the main period of the aphid population increase would result in a 33 percent reduction in peak population size,” while “an increase in TX of 2°C and MaxT of 2.6°C would result in an early population collapse (74 percent reduction of population size).” It would appear that a little global warming could greatly decrease aphid infestations of cereal crops grown throughout Germany and Central Europe.
Returning to the subject of joint CO2 and O3 effects on aphids, Awmack et al. (2004) conducted a two-year study at the Aspen FACE site near Rhinelander, Wisconsin, USA, of the individual and combined effects of elevated CO2 (+200 ppm) and O3 (1.5 x ambient) on the performance of Cepegillettea betulaefoliae aphids feeding on paper birch trees in what they call “the first investigation of the long-term effects of elevated CO2 and O3 atmospheres on natural insect herbivore populations.” At the individual scale, they report that “elevated CO2 and O3 did not significantly affect [aphid] growth rates, potential fecundity (embryo number) or offspring quality.” At the population scale, on the other hand, they found that “elevated O3 had a strong positive effect,” but that “elevated CO2 did not significantly affect aphid populations.”
In comparing their results with those of prior related studies, the three scientists report that “the responses of other aphid species to elevated CO2 or O3 are also complex.” In particular, they note that “tree-feeding aphids show few significant responses to elevated CO2 (Docherty et al., 1997), while crop-feeding species may respond positively (Awmack et al., 1997; Bezemer et al., 1998; Hughes and Bazzaz, 2001; Zhang et al., 2001; Stacey and Fellowes, 2002), negatively (Newman et al., 1999), or not at all (Hughes and Bazzaz, 2001), and the same species may show different responses on different host plant species (Awmack et al., 1997; Bezemer et al., 1999).” In summarizing their observations, they stated that “aphid individual performance did not predict population responses to CO2 and O3,” and they concluded that “elevated CO2 and O3 atmospheres are unlikely to affect C. betulaefoliae populations in the presence of natural enemy communities.”
In a study of a different aphid (Chaitophorus stevensis) conducted at the same FACE site, Mondor et al. (2004) focused on the subject of pheromones, which they say “are utilized by insects for several purposes, including alarm signaling,” and which in the case of phloem-feeding aphids induces high-density groups of them on exposed leaves of trembling aspen trees to disperse and move to areas of lower predation risk. In this experiment the four treatments were: control (367 ppm CO2, 38 ppb O3), elevated CO2 (537 ppm), elevated O3 (51 ppb), and elevated CO2 and O3 (537 ppm CO2, 51 ppb O3). Within each treatment, several aspen leaves containing a single aphid colony of 25 ± 2 individuals were treated in one of two different ways: (1) an aphid was prodded lightly on the thorax so as to not produce a visible pheromone droplet, or (2) an aphid was prodded more heavily on the thorax and induced to emit a visible pheromone droplet, after which, in the words of the scientists, “aphids exhibiting any dispersal reactions in response to pheromone emission as well as those exhibiting the most extreme dispersal response, walking down the petiole and off the leaf, were recorded over 5 min.”
Mondor et al.’s observations were striking. They found that the aphids they studied “have diminished escape responses in enriched carbon dioxide environments, while those in enriched ozone have augmented escape responses, to alarm pheromone.” In fact, they report that “0 percent of adults dispersed from the leaf under elevated CO2, while 100 percent dispersed under elevated O3,” indicating that the effects of elevated CO2 and elevated O3 on aphid response to pheromone alarm signaling are diametrically opposed to each other, with elevated O3 (which is detrimental to vegetation) helping aphids to escape predation and therefore live to do further harm to the leaves they infest, but with elevated CO2 (which is beneficial to vegetation) making it more difficult for aphids to escape predation and thereby providing yet an additional benefit to plant foliage. Within this context, therefore, ozone may be seen to be doubly bad for plants, while carbon dioxide may be seen to be doubly good. In addition, Mondor et al. state that this phenomenon may be of broader scope than what is revealed by their specific study, noting that other reports suggest that “parasitoids and predators are more abundant and/or efficacious under elevated CO2 levels (Stiling et al., 1999; Percy et al., 2002), but are negatively affected by elevated O3 (Gate et al., 1995; Percy et al., 2002).”
In another intriguing study, Chen et al. (2004) grew spring wheat from seed to maturity in high-fertility well-watered pots out-of-doors in open-top chambers (OTCs) maintained at atmospheric CO2 concentrations of 370, 550, and 750 ppm. Approximately two months after seeding, 20 apterous adult aphids (Sitobion avenae) from an adjacent field were placed upon the wheat plants of each of 25 pots in each OTC, while 15 pots were left as controls; and at subsequent 5-day intervals, both apterous and alate aphids were counted. Then, about one month later, 10 alate morph fourth instar nymphs were introduced onto the plants of each of nine control pots; for the next two weeks the number of offspring laid on those plants were recorded and removed daily to measure reproductive activity. At the end of the study, the wheat plants were harvested and their various growth responses determined.
Adherence to these protocols revealed that the introduced aphid populations increased after infestation, peaked during the grain-filling stage, and declined a bit as the wheat matured. On the final day of measurement, aphids in the 550-ppm CO2 treatment were 32 percent more numerous than those in ambient air, while aphids in the 750-ppm treatment were 50 percent more numerous. Alate aphids also produced more offspring on host plants grown in elevated CO2: 13 percent more in the 550-ppm treatment and 19 percent more in the 750-ppm treatment. As for the wheat plants, Chen et al. report that “elevated CO2 generally enhanced plant height, aboveground biomass, ear length, and number of and dry weight of grains per ear, consistent with most other studies.” With respect to above-ground biomass, for example, the 550-ppm treatment displayed an increase of 36 percent, while the 750-ppm treatment displayed an increase of 50 percent, in the case of both aphid-infested and non-infested plants.
In commenting on their findings, Chen et al. report that “aphid infestation caused negative effects on all the plant traits measured … but the negative effects were smaller than the positive effects of elevated CO2 on the plant traits.” Hence, they concluded that “the increased productivity occurring in plants exposed to higher levels of CO2 more than compensate for the increased capacity of the aphids to cause damage.” In this experiment, therefore, we have a situation where both the plant and the insect that feeds on it were simultaneously benefited by the applied increases in atmospheric CO2 concentration.
Last, in a study that investigated a number of plant-aphid-predator relationships, Chen et al. (2005) grew transgenic cotton plants for 30 days in well watered and fertilized sand/vermiculite mixtures in pots set in controlled-environment chambers maintained at atmospheric CO2 concentrations of 370, 700, and 1050 ppm. A subset of aphid-infected plants was additionally supplied with predatory ladybugs, while three generations of cotton aphids (Aphis gossypii) were subsequently allowed to feed on some of the plants. Based on measurements made throughout this complex set of operations, Chen et al. found that (1) “plant height, biomass, leaf area, and carbon:nitrogen ratios were significantly higher in plants exposed to elevated CO2 levels,” (2) “more dry matter and fat content and less soluble protein were found in A. gossypii in elevated CO2,” (3) “cotton aphid fecundity significantly increased … through successive generations reared on plants grown under elevated CO2,” (4) “significantly higher mean relative growth rates were observed in lady beetle larvae under elevated CO2,” and (5) “the larval and pupal durations of the lady beetle were significantly shorter and [their] consumption rates increased when fed A. gossypii from elevated CO2 treatments.” In commenting on the significance of their findings, Chen et al. say their study “provides the first empirical evidence that changes in prey quality mediated by elevated CO2 can alter the prey preference of their natural enemies,” and in this particular case, they found that this phenomenon could “enhance the biological control of aphids by lady beetle.”
In considering the totality of these many experimental findings, it would appear that the ongoing rise in the air’s CO2 content will likely not have a major impact, one way or the other, on aphid-plant interactions, although the scales do appear to be slightly tipped in favor of plants over aphids. Yet a third possibility is that both plants and aphids will be benefited by atmospheric CO2 enrichment, but with plants benefiting more.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/i/insectsaphids.php.
Butterflies
How will earth’s butterflies respond to atmospheric CO2 enrichment and global warming? We here explore what has been learned about the question over the past few years, beginning with a review of studies that focus on carbon dioxide and concluding with studies that focus on temperature.
In a study of Lotus corniculatus (a cyanogenic plant that produces foliar cyanoglycosides to deter against herbivory by insects) and the Common Blue Butterfly (Polyommatus icarus, which regularly feeds upon L. corniculatus because it possesses an enzyme that detoxifies cyanide-containing defensive compounds), Goverde et al. (1999) collected four genotypes of L. corniculatus differing in their concentrations of cyanoglycosides and tannins (another group of defensive compounds) near Paris, France. They then grew them in controlled-environment chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm, after which they determined the effects of the doubled CO2 concentration on leaf quality and allowed the larvae of the Common Blue Butterfly to feed upon the plants’ leaves. This work revealed that elevated CO2 significantly increased leaf tannin and starch contents in a genotypically dependent and -independent manner, respectively, while decreasing leaf cyanoglycoside contents independent of genotype. These CO2-induced changes in leaf chemistry increased leaf palatability, as indicated by greater dry weight consumption of CO2-enriched leaves by butterfly larvae. In addition, the increased consumption of CO2-enriched leaves led to greater larval biomass and shorter larval development times, positively influencing the larvae of the Common Blue Butterfly. Hence, it is not surprising that larval mortality was lower when feeding upon CO2-enriched as opposed to ambiently grown leaves.
Goverde et al. (2004) grew L. corniculatus plants once again, this time from seed in tubes recessed into the ground under natural conditions in a nutrient-poor calcareous grassland, where an extra 232 ppm of CO2 was supplied to them via a Screen-Aided CO2 Control (SACC) system (Leadley et al., 1997, 1999), and where insect larvae were allowed to feed on the plants (half of which received extra phosphorus fertilizer) for the final month of the experiment. The atmospheric CO2 enrichment employed in this experiment increased the total dry weight of plants growing on the unfertilized soil by 21.5 percent and that of plants growing on the phosphorus-enriched soil by 36.3 percent. However, the elevated CO2 treatment had no effect on pupal and adult insect mass, although Goverde et al. report there were “genotype-specific responses in the development time of P. icarus to elevated CO2 conditions,” with larvae originating from different mothers developing better under either elevated CO2 or ambient CO2, while for still others the air’s CO2 concentration had no effect on development.
In another study by some of the same researchers, Goverde et al. (2002) raised larvae of the satyrid butterfly (Coenonympha pamphilus) in semi-natural undisturbed calcareous grassland plots exposed to atmospheric CO2 concentrations of 370 and 600 ppm for five growing seasons. In doing so, they found that the elevated CO2 concentration increased foliar concentrations of total nonstructural carbohydrates and condensed tannins in the grassland plants; but in what is often considered a negative impact, they found that it also decreased foliar nitrogen concentrations. Nevertheless, this phenomenon had no discernible effect on butterfly growth and performance. Larval development time, for example, was not affected by elevated CO2, nor was adult dry mass. In fact, the elevated CO2 increased lipid concentrations in adult male butterflies by nearly 14 percent, while it marginally increased the number of eggs in female butterflies. The former of these responses is especially important, because lipids are used as energy resources in these and other butterflies, while increased egg numbers in females also suggests an increase in fitness.
Turning to the study of temperature effects on butterflies, Parmesan et al. (1999) analyzed distributional changes over the past century of non-migratory species whose northern boundaries were in northern Europe (52 species) and whose southern boundaries were in southern Europe or northern Africa (40 species). This work revealed that the northern boundaries of the first group shifted northward for 65 percent of them, remained stable for 34 percent, and shifted southward for 2 percent, while the southern boundaries of the second group shifted northward for 22 percent of them, remained stable for 72 percent, and shifted southward for 5 percent, such that “nearly all northward shifts involved extensions at the northern boundary with the southern boundary remaining stable.”
This behavior is precisely what we would expect to see if the butterflies were responding to shifts in the ranges of the plants upon which they depend for their sustenance, because increases in atmospheric CO2 concentration tend to ameliorate the effects of heat stress in plants and induce an upward shift in the temperature at which they function optimally. These phenomena tend to cancel the impetus for poleward migration at the warm edge of a plant’s territorial range, yet they continue to provide the opportunity for poleward expansion at the cold edge of its range. Hence, it is possible that the observed changes in butterfly ranges over the past century of concomitant warming and rising atmospheric CO2 concentration are related to matching changes in the ranges of the plants upon which they feed. Or, this similarity could be due to some more complex phenomenon, possibly even some direct physiological effect of temperature and atmospheric CO2 concentration on the butterflies themselves.
In any event, and in the face of the 0.8°C of global warming that occurred in Europe over the twentieth century, the consequences for European butterflies were primarily beneficial because, as Parmesan et al. describe the situation, “most species effectively expanded the size of their range when shifting northwards,” since “nearly all northward shifts involved extensions at the northern boundary with the southern boundary remaining stable.”
Across the Atlantic in America, Fleishman et al. (2001) used comprehensive data on butterfly distributions from six mountain ranges in the U.S. Great Basin to study how butterfly assemblages of that region may respond to IPCC-projected climate change. Whereas prior, more-simplistic analyses have routinely predicted the extirpation of great percentages of the butterfly species in this region in response to model-predicted increases in air temperature, Fleishman et al.’s study revealed that “few if any species of montane butterflies are likely to be extirpated from the entire Great Basin (i.e., lost from the region as a whole).”
In further discussing their results, the three researchers note that “during the Middle Holocene, approximately 8000-5000 years ago, temperatures in the Great Basin were several degrees warmer than today.” Thus, they go on say that “we might expect that most of the montane species—including butterflies—that currently inhabit the Great Basin would be able to tolerate the magnitude of climatic warming forecast over the next several centuries.” Consequently, it would appear that even if the global warming projections of the IPCC were true, the predictions of butterfly extinctions associated with those projections are almost certainly false.
Returning to the British Isles, Thomas et al. (2001) documented an unusually rapid expansion of the ranges of two butterfly species (the silver-spotted skipper butterfly and the brown argus butterfly) along with two cricket species (the long-winged cone-head and Roesel’s bush cricket). They write that the warming-induced “increased habitat breadth and dispersal tendencies have resulted in about 3- to 15-fold increases in expansion rates.”
In commenting on these findings, Pimm (2001) truly states the obvious when he says the geographical ranges of these insects are “expanding faster than expected,” and that the synergies involved in the many intricacies of the range expansion processes are also “unexpected.”
Crozier (2004) writes that “Atalopedes campestris, the sachem skipper butterfly, expanded its range from northern California into western Oregon in 1967, and into southwestern Washington in 1990,” where she reports that temperatures rose by 2-4°C over the prior half-century. Thus intrigued, and in an attempt to assess the importance of this regional warming for the persistence of A. campestris in the recently colonized areas, Crozier “compared population dynamics at two locations (the butterfly’s current range edge and just inside the range) that differ by 2-3°C.” Then, to determine the role of over-winter larval survivorship, she “transplanted larvae over winter to both sites.”
This work revealed, in her words, that “combined results from population and larval transplant analyses indicate that winter temperatures directly affect the persistence of A. campestris at its northern range edge, and that winter warming was a prerequisite for this butterfly’s range expansion.” Noting that “populations are more likely to go extinct in colder climates,” Crozier says “the good news about rapid climate change [of the warming type] is that new areas may be available for the introduction of endangered species.” Her work also demonstrates that the species she studied has responded to regional warming by extending its northern range boundary and thereby expanding its range.
Two years later, Davies et al. (2006) introduced their study of the silver-spotted skipper butterfly (Hesperia comma L.) by noting that during the twentieth century it “became increasingly rare in Britain [as] a result of the widespread reduction of sparse, short-turfed calcareous grassland containing the species’ sole larval host plant, sheep’s fescue grass [Festuca ovina L].” As a result, they describe the “refuge” colonies of 1982 as but a “remnant” of what once had been. The four researchers analyzed population density data together with estimates of the percentage bare ground and the percentage of sheep’s fescue available to the butterflies, based on surveys conducted in Surrey in the chalk hills of the North Downs, south of London, in 1982 (Thomas et al., 1986), 1991 (Thomas and Jones, 1993), 2000 (Thomas et al., 2001; Davies et al., 2005), and 2001 (R.J. Wilson, unpublished data). In addition, they assessed egg-laying rates in different microhabitats, as well as the effects of ambient and oviposition site temperatures on egg laying, and the effects of sward composition on egg location. This work revealed, in their words, that “in 1982, 45 habitat patches were occupied by H. comma [but] in the subsequent 18-year period, the species expanded and, by 2000, a further 29 patches were colonized within the habitat network.” In addition, they found that “the mean egg-laying rate of H. comma females increased with rising ambient temperatures,” and that “a wider range of conditions have become available for egg-laying.”
In discussing their findings, Davies et al. state that “climate warming has been an important driving force in the recovery of H. comma in Britain [as] the rise in ambient temperature experienced by the butterfly will have aided the metapopulation re-expansion in a number of ways.” First, they suggest that “greater temperatures should increase the potential fecundity of H. comma females,” and that “if this results in larger populations, for which there is some evidence (e.g. 32 of the 45 habitat patches occupied in the Surrey network experienced site-level increases in population density between 1982 and 2000), they will be less prone to extinction,” with “larger numbers of dispersing migrant individuals being available to colonize unoccupied habitat patches and establish new populations.” Second, they state that “the wider range of thermal and physical microhabitats used for egg-laying increased the potential resource density within each grassland habitat fragment,” and that “this may increase local population sizes.” Third, they argue that “colonization rates are likely to be greater as a result of the broadening of the species realized niche, [because] as a larger proportion of the calcareous grassland within the species’ distribution becomes thermally suitable, the relative size and connectivity of habitat patches within the landscape increases.” Fourth, they note that “higher temperatures may directly increase flight (dispersal) capacity, and the greater fecundity of immigrants may improve the likelihood of successful population establishment.” Consequently, Davies et al. conclude that “the warmer summers predicted as a consequence of climate warming are likely to be beneficial to H. comma within Britain,” and they suggest that “warmer winter temperatures could also allow survival in a wider range of microhabitats.”
In a concurrent study, Menendez et al. (2006) provided what they call “the first assessment, at a geographical scale, of how species richness has changed in response to climate change,” concentrating on British butterflies. This they did by testing “whether average species richness of resident British butterfly species has increased in recent decades, whether these changes are as great as would be expected given the amount of warming that has taken place, and whether the composition of butterfly communities is changing towards a dominance by generalist species.” By these means they determined that “average species richness of the British butterfly fauna at 20 x 20 km grid resolution has increased since 1970-82, during a period when climate warming would lead us to expect increases.” They also found, as expected, that “southerly habitat generalists increased more than specialists,” which require a specific type of habitat that is sometimes difficult for them to find, especially in the modern world where habitat destruction is commonplace. In addition, they were able to determine that observed species richness increases lagged behind those expected on the basis of climate change.
These results “confirm,” according to the nine UK researchers, “that the average species richness of British butterflies has increased since 1970-82.” However, some of the range shifts responsible for the increase in species richness take more time to occur than those of other species; they say their results imply “it may be decades or centuries before the species richness and composition of biological communities adjusts to the current climate.”
Also working in Britain, Hughes et al. (2007) examined evolutionary changes in adult flight morphology in six populations of the speckled wood butterfly—Pararge aegeria L. (Satyrinae)—along a transect from its distribution core to its warming-induced northward expanding range margin. The results of this exercise were then compared with the output of an individual-based spatially explicit model that was developed “to investigate impacts of habitat availability on the evolution of dispersal in expanding populations.” This work indicated that the empirical data the researchers gathered “were in agreement with model output,” and that they “showed increased dispersal ability with increasing distance from the distribution core,” which included favorable changes in thorax shape, abdomen mass, and wing aspect ratio for both males and females, as well as thorax mass and wing loading for females. In addition, they say that “increased dispersal ability was evident in populations from areas colonized >30 years previously.”
In discussing their findings, Hughes et al. suggest that “evolutionary increases in dispersal ability in expanding populations may help species track future climate changes and counteract impacts of habitat fragmentation by promoting colonization.” However, they report that in the specific situation they investigated, “at the highest levels of habitat loss, increased dispersal was less evident during expansion and reduced dispersal was observed at equilibrium, indicating that for many species, continued habitat fragmentation is likely to outweigh any benefits from dispersal.” Put another way, it would appear that global warming is proving not to be an insurmountable problem for the speckled wood butterfly, which is evolving physical characteristics that allow it to better keep up with the poleward migration of its current environmental niche, but that the direct destructive assaults of humanity upon its natural habitat could still end up driving it to extinction.
Analyzing data pertaining to the general abundance of Lepidoptera in Britain over the period 1864-1952, based on information assembled by Beirne (1955) via his examination of “several thousand papers in entomological journals describing annual abundances of moths and butterflies,” were Dennis and Sparks (2007), who report that “abundances of British Lepidoptera were significantly positively correlated with Central England temperatures in the current year for each month from May to September and November,” and that “increased overall abundance in Lepidoptera coincided significantly with increased numbers of migrants,” which latter data were derived from the work of Williams (1965). In addition, they report that Pollard (1988) subsequently found much the same thing for 31 butterfly species over the period 1976-1986, and that Roy et al. (2001) extended the latter investigation to 1997, finding “strong associations between weather and population fluctuations and trends in 28 of 31 species which confirmed Pollard’s (1988) findings,” all of which observations indicate that the warming-driven increase in Lepidopteran species and numbers in Britain has been an ongoing phenomenon ever since the end of the Little Ice Age.
Returning to North America for one final study, White and Kerr (2006), as they describe it, “report butterfly species’ range shifts across Canada between 1900 and 1990 and develop spatially explicit tests of the degree to which observed shifts result from climate or human population density,” the latter of which factors they describe as “a reasonable proxy for land use change,” within which broad category they include such things as “habitat loss, pesticide use, and habitat fragmentation,” all of which anthropogenic-driven factors have been tied to declines of various butterfly species. In addition, they say that to their knowledge, “this is the broadest scale, longest term dataset yet assembled to quantify global change impacts on patterns of species richness.”
This exercise led White and Kerr to discover that butterfly species richness “generally increased over the study period, a result of range expansion among the study species,” and they further found that this increase “from the early to late part of the twentieth century was positively correlated with temperature change,” which had to have been the cause of the change, for they also found that species richness was “negatively correlated with human population density change.”
Contrary to the doom-and-gloom prognostications of some experts, the supposedly unprecedented global warming of the twentieth century has been beneficial for the butterfly species that inhabit Canada, Britain, and the United States, as their ranges have expanded and greater numbers of species are now being encountered in each country.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/i/summaries/butterflies.php.
Moths
Kerslake et al. (1998) collected five-year-old heather plants from a Scottish moor and grew them in open-top chambers maintained at atmospheric CO2 concentrations of 350 and 600 ppm for 20 months, with and without soil nitrogen fertilization. At two different times during the study, larvae of Operophtera brumata, a voracious winter moth whose outbreaks have caused extensive damage to heather moorland in recent years, were allowed to feed upon current-year shoots for up to one month. The results obtained from this experiment revealed that the survivorship of larvae placed on CO2-enriched foliage was not significantly different from that of larvae placed on foliage produced in ambient air, regardless of nitrogen treatment. In addition, feeding upon CO2-enriched foliage did not affect larval growth rate, development, or final pupal weight. Consequently, Kerslake et al. concluded that their study “provides no evidence that increasing atmospheric CO2 concentrations will affect the potential for outbreak of Operophtera brumata on this host.”
Hattenschwiler and Schafellner (1999) grew seven-year-old spruce trees at atmospheric CO2 concentrations of 280, 420, and 560 ppm in various nitrogen deposition treatments for three years, after which they performed needle quality assessments and allowed nun moth (Lymantria monacha) larvae to feed upon current-year needles for 12 days. This moth is an especially voracious defoliator that resides in most parts of Europe and East Asia between 40 and 60° N latitude, and it is commonly regarded as the “coniferous counterpart” of its close relative the gypsy moth, which feeds primarily upon deciduous trees.
The two scientists determined from their observations that elevated CO2 significantly enhanced needle starch, tannin, and phenolic concentrations, while significantly decreasing needle water and nitrogen contents. Thus, atmospheric CO2 enrichment reduced overall needle quality from the perspective of this foliage-consuming moth, as nitrogen content is the primary factor associated with leaf quality. Increasing nitrogen deposition, on the other hand, tended to enhance needle quality, for it lowered starch, tannin, and phenolic concentrations while boosting needle nitrogen content. Nevertheless, the positive influence of nitrogen deposition on needle quality was not large enough to completely offset the quality reduction caused by elevated CO2.
In light of these observations, it was no surprise that larvae placed on CO2-enriched foliage consumed less needle biomass than larvae placed on low-CO2-grown foliage, regardless of nitrogen treatment, and that the larvae feeding on CO2-enriched foliage exhibited reduced relative growth rates and attained an average biomass that was only two-thirds of that attained by larvae consuming foliage produced at 280 ppm CO2. As a result, Hattenschwiler and Schafellner concluded that “altered needle quality in response to elevated CO2 will impair the growth and development of Lymantria monacha larvae,” which should lead to reductions in the degree of spruce tree destruction caused by this voracious defoliator.
Stiling et al. (2002) studied the effects of an approximate doubling of the air’s CO2 concentration on a number of characteristics of several insect herbivores feeding on plants native to a scrub-oak forest ecosystem at the Kennedy Space Center, Florida, USA, in eight ambient and eight CO2-enriched open-top chambers. They say that the “relative levels of damage by the two most common herbivore guilds, leaf-mining moths and leaf-chewers (primarily larval lepidopterans and grasshoppers), were significantly lower in elevated CO2 than in ambient CO2,” and that “the response to elevated CO2 was the same across all plant species.”
In a follow-up study to that of Stiling et al., which was conducted at the same facilities, Rossi et al. (2004), focused on the abundance of a guild of lepidopteran leafminers that attack the leaves of myrtle oak, as well as various leaf chewers that also like to munch on this species. Specifically, they periodically examined 100 marked leaves in each of the 16 open-top chambers for a total of nine months, after which, in their words, “differences in mean percent of leaves with leafminers and chewed leaves on trees from ambient and elevated chambers were assessed using paired t-tests.” This protocol revealed, in their words, that “both the abundance of the guild of leafmining lepidopterans and damage caused by leaf chewing insects attacking myrtle oak were depressed in elevated CO2.” Leafminer abundance was 44 percent lower (P = 0.096) in the CO2-enriched chambers compared to the ambient-air chambers, while the abundance of leaves suffering chewing damage was 37 percent lower (P = 0.072) in the CO2-enriched air.
Working with red maple saplings, Williams et al. (2003) bagged first instar gypsy moth larvae on branches of trees that were entering their fourth year of growth within open-top chambers maintained at four sets of CO2/temperature conditions: (1) ambient temperature, ambient CO2, (2) ambient temperature, elevated CO2 (ambient + 300 ppm), (3) elevated temperature (ambient + 3.5°C), ambient CO2, and (4) elevated temperature, elevated CO2. For these conditions they measured several parameters that were required to test their hypothesis that a CO2-enriched atmosphere would lead to reductions in foliar nitrogen concentrations and increases in defensive phenolics that would in turn lead to increases in insect mortality. The results they obtained indicated, in their words, “that larvae feeding on CO2-enriched foliage ate a comparably poorer food source than those feeding on ambient CO2-grown plants, irrespective of temperature.” Nevertheless, they determined that “CO2-induced reductions in foliage quality were unrelated to insect mortality, development rate and pupal weight.” As a result, they were forced to conclude that “phytochemical changes resulted in no negative effects on gypsy moth performance,” but neither did they help them.
Noting that increases in the atmosphere’s CO2 concentration typically lead to greater decreases in the concentrations of nitrogen in the foliage of C3 as opposed to C4 grasses, Barbehenn et al. (2004) say “it has been predicted that insect herbivores will increase their feeding damage on C3 plants to a greater extent than on C4 plants (Lincoln et al., 1984, 1986; Lambers, 1993). To test this hypothesis, they grew Lolium multiflorum (Italian ryegrass, a common C3 pasture grass) and Bouteloua curtipendula (sideoats gramma, a native C4 rangeland grass) in chambers maintained at either the ambient atmospheric CO2 concentration of 370 ppm or the doubled CO2 concentration of 740 ppm for two months, after which newly molted sixth-instar larvae of Pseudaletia unipuncta (a grass-specialist noctuid) and Spodoptera frugiperda (a generalist noctuid) were allowed to feed upon the two grasses.
As expected, Barbehenn et al. found that foliage protein concentration decreased by 20 percent in the C3 grass, but by only 1 percent in the C4 grass, when they were grown in CO2-enriched air; and they say that “to the extent that protein is the most limiting of the macronutrients examined, these changes represent a decline in the nutritional quality of the C3 grass.” However, and “contrary to our expectations,” in the words of Barbehenn et al., “neither caterpillar species significantly increased its consumption rate to compensate for the lower concentration of protein in [the] C3 grass,” and they note that “this result does not support the hypothesis that C3 plants will be subject to greater rates of herbivory relative to C4 plants in future [high-CO2] atmospheric conditions (Lincoln et al., 1984).” In addition, and “despite significant changes in the nutritional quality of L. multiflorum under elevated CO2,” they note that “no effect on the relative growth rate of either caterpillar species on either grass species resulted,” and that there were “no significant differences in insect performance between CO2 levels.” By way of explanation of these results, they suggest that “post-ingestive mechanisms could provide a sufficient means of compensation for the lower nutritional quality of C3 plants grown under elevated CO2.”
In light of these observations, Barbehenn et al. suggest “there will not be a single pattern that characterizes all grass feeders” with respect to their feeding preferences and developmental responses in a world where certain C3 plants may experience foliar protein concentrations that are lower than those they exhibit today, nor will the various changes that may occur necessarily be detrimental to herbivore development or to the health and vigor of their host plants. Nevertheless, subsequent studies continue to suggest that various moth species will likely be negatively affected by the ongoing rise in the air’s CO2 content.
A case in point is the study of Chen et al. (2005), who grew well watered and fertilized cotton plants of two varieties (one expressing Bacillus thurigiensis toxin genes and one a non-transgenic cultivar from the same recurrent parent) in pots placed within open-top chambers maintained at either 376 or 754 ppm CO2 in Sanhe County, Hebei Province, China, from planting in mid-May to harvest in October, while immature bolls were periodically collected and analyzed for various chemical characteristics and others were stored under refrigerated conditions for later feeding to larvae of the cotton bollworm. By these means they 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, and that it slightly decreased the body biomass of the cotton bollworm 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.
Bidart-Bouzat et al. (2005) grew three genotypes of mouse-ear cress (Arabidopsis thaliana) from seed in pots within controlled-environment chambers maintained at either ambient CO2 (360 ppm) or elevated CO2 (720 ppm). On each of half of the plants (the herbivory treatment) in each of these CO2 treatments, they placed two second-instar larvae of the diamondback moth (Plutella xylostella) at bolting time and removed them at pupation, which resulted in an average of 20 percent of each plant’s total leaf area in the herbivory treatment being removed. Then, each pupa was placed in a gelatin capsule until adult emergence and ultimate death, after which insect gender was determined and the pupa’s weight recorded. At the end of this herbivory trial, the leaves of the control and larvae-infested plants were analyzed for concentrations of individual glucosinolates—a group of plant-derived chemicals that can act as herbivore deterrents (Maruicio and Rausher, 1997)—while total glucosinolate production was determined by summation of the individual glucosinolate assays. Last, influences of elevated CO2 on moth performance and its association with plant defense-related traits were evaluated.
Overall, it was determined by these means that herbivory by larvae of the diamondback moth did not induce any increase in the production of glucosinolates in the mouse-ear cress in the ambient CO2 treatment. However, the three scientists report that “herbivory-induced increases in glucosinolate contents, ranging from 28% to 62% above basal levels, were found under elevated CO2 in two out of the three genotypes studied.” In addition, they determined that “elevated CO2 decreased the overall performance of diamondback moths.” And because “induced defenses can increase plant fitness by reducing subsequent herbivore attacks (Agrawal, 1999; Kessler and Baldwin, 2004),” according to Bidart-Bouzat et al., they suggest that “the pronounced increase in glucosinolate levels under CO2 enrichment may pose a threat not only for insect generalists that are likely to be more influenced by rapid changes in the concentration of these chemicals, but also for other insect specialists more susceptible than diamondback moths to high glucosinolate levels (Stowe, 1998; Kliebenstein et al., 2002).”
In a study of a major crop species, Wu et al. (2006) grew spring wheat (Triticum aestivum L.) from seed to maturity in pots placed within open-top chambers maintained at either 370 or 750 ppm CO2 in Sanhe County, Hebei Province, China, after which they reared three generations of cotton bollworms (Helicoverpa armigera Hubner) on the milky grains of the wheat, while monitoring a number of different bollworm developmental characteristics. In doing so, as they describe it, “significantly lower pupal weights were observed in the first, second and third generations,” and “the fecundity of H. armigera decreased by 10% in the first generation, 13% in the second generation and 21% in the third generation,” resulting in a “potential population decrease in cotton bollworm by 9% in the second generation and 24% in the third generation.” In addition, they say that “population consumption was significantly reduced by 14% in the second generation and 24% in the third generation,” and that the efficiency of conversion of ingested food was reduced “by 18% in the first generation, 23% in the second generation and 30% in the third generation.” As a result, they concluded that the “net damage of cotton bollworm on wheat will be less under elevated atmospheric CO2,” while noting that “at the same time, gross wheat production is expected to increase by 63% under elevated CO2.”
In another report of their work, Wu et al. (2007) write that “significant decreases in the protein, total amino acid, water and nitrogen content by 15.8%, 17.7%, 9.1% and 20.6% and increases in free fatty acid by 16.1% were observed in cotton bolls grown under elevated CO2.” And when fed with these cotton bolls, they say that the larval survival rate of H. armigera “decreased by 7.35% in the first generation, 9.52% in the second generation and 11.48% in the third generation under elevated CO2 compared with ambient CO2.” In addition, they observed that “the fecundity of H. armigera decreased by 7.74% in the first generation, 14.23% in the second generation and 16.85% in the third generation,” while noting that “fecundity capacity is likely to be reduced even further in the next generation.”
The synergistic effects of these several phenomena, in the words of Wu et al., “resulted in a potential population decrease in cotton bollworm by 18.1% in the second generation and 52.2% in the third generation under elevated CO2,” with the result that “the potential population consumption of cotton bollworm decreased by 18.0% in the second generation and 55.6% in the third generation … under elevated CO2 compared with ambient CO2.” And in light of these several findings, they concluded that “the potential population dynamics and potential population consumption of cotton bollworm will alleviate the harm to [cotton] plants in the future rising-CO2 atmosphere.”
In a different type of study, Esper et al. (2007) reconstructed an annually resolved history of population cycles of a foliage-feeding Lepidopteran commonly known as the larch budmoth (Zeiraphera diniana Gn.)—or LBM for short—within the European Alps in the southern part of Switzerland. As is typical of many such insect pests, they note that “during peak activity, populations may reach very high densities over large areas,” resulting in “episodes of massive defoliation and/or tree mortality” that could be of great ecological and economic significance.
The first thing the team of Swiss and US researchers thus did in this regard was develop a history of LBM outbreaks over the 1,173-year period AD 832-2004, which they describe as “the longest continuous time period over which any population cycle has ever been documented.”
They accomplished this feat using radiodensitometric techniques to characterize the tree-ring density profiles of 180 larch (Larix deciduas Mill.) samples, where “LBM outbreaks were identified based upon characteristic maximum latewood density (MXD) patterns in wood samples, and verified using more traditional techniques of comparison with tree-ring chronologies from non-host species,” i.e., fir and spruce. Then, they developed a matching temperature history for the same area, which was accomplished by combining “a tree-ring width-based reconstruction from AD 951 to 2002 integrating 1527 pine and larch samples (Buntgen et al., 2005) and a MXD-based reconstruction from AD 755 to 2004 based upon the same 180 larch samples used in the current study for LBM signal detection (Buntgen et al., 2006).”
Over almost the entire period studied, from its start in AD 832 to 1981, there were a total of 123 LBM outbreaks with a mean reoccurrence time of 9.3 years. In addition, the researchers say “there was never a gap that lasted longer than two decades.” From 1981 to the end of their study in 2004, however, there were no LBM outbreaks; since there had never before (within their record) been such a long outbreak hiatus, they concluded that “the absence of mass outbreaks since the 1980s is truly exceptional.”
To what do Esper et al. attribute this unprecedented recent development? Noting that “conditions during the late twentieth century represent the warmest period of the past millennium”—as per their temperature reconstruction for the region of the Swiss Alps within which they worked—they point to “the role of extraordinary climatic conditions as the cause of outbreak failure,” and they discuss what they refer to as the “probable hypothesis” of Baltensweiler (1993), who described a scenario by which local warmth may lead to reduced LBM populations.
Such may well be the case, but we hasten to add that atmospheric CO2 concentrations since 1980 have also been unprecedented over the 1,173-year period of Esper et al.’s study. Hence, the suppression of LBM outbreaks over the past quarter-century may have been the result of some synergistic consequence of the two factors (temperature and CO2) acting in unison, while a third possibility may involve only the increase in the air’s CO2 content.
Esper et al. say their findings highlight the “vulnerability of an otherwise stable ecological system in a warming environment,” in what would appear to be an attempt to attach an undesirable connotation to the observed outcome. This wording seems strange indeed, for it is clear that the “recent disruption of a major disturbance regime,” as Esper et al. refer to the suppression of LBM outbreaks elsewhere in their paper, would be considered by most people to be a positive outcome, and something to actually be welcomed.
Working with Antheraea polyphemus—a leaf-chewing generalist lepidopteran herbivore that represents the most abundant feeding guild in the hardwood trees that grow beneath the canopy of the unmanaged loblolly pine plantation that hosts the Forest Atmosphere Carbon Transfer and Storage (FACTS-1) research site in the Piedmont region of North Carolina, USA, where the leaf-chewer can consume 2-15 percent of the forest’s net primary production in any given year—Knepp et al. (2007) focused their attention on two species of oak tree—Quercus alba L. (white oak) and Quercus velutina Lam. (black oak)—examining host plant preference and larval performance of A. polyphemus when fed foliage of the two tree species that had been grown in either ambient or CO2-enriched air (to 200 ppm above ambient) in this long-running FACE experiment. In doing so, they determined that “growth under elevated CO2 reduced the food quality of oak leaves for caterpillars,” while “consuming leaves of either oak species grown under elevated CO2 slowed the rate of development of A. polyphemus larvae.” In addition, they found that feeding on foliage of Q. velutina that had been grown under elevated CO2 led to reduced consumption by the larvae and greater mortality. As a result, they concluded that “reduced consumption, slower growth rates, and increased mortality of insect larvae may explain [the] lower total leaf damage observed previously in plots of this forest exposed to elevated CO2,” as documented by Hamilton et al. (2004) and Knepp et al. (2005), which finding bodes well indeed for the growth and vitality of such forests in the years and decades ahead, as the air’s CO2 content continues to rise.
Kampichler et al. (2008) also worked with oak trees. Noting, however, that “systems studied so far have not included mature trees,” they attempted to remedy this situation by determining “the abundance of dominant leaf-galls (spangle-galls induced by the cynipid wasps Neuroterus quercusbaccarum and N. numismalis) and leaf-mines (caused by the larvae of the moth Tischeria ekebladella) on freely colonized large oaks in a mixed forest in Switzerland, which received CO2 enrichment [540 ppm vs. 375 ppm during daylight hours] from 2001 to 2004” via “the Swiss Canopy Crane (SCC) and a new CO2 enrichment technique (web-FACE)” in a forest that they say “is 80-120 years old with a canopy height of 32-38 m, consisting of seven deciduous and four coniferous species.” This work allowed the German, Mexican, and Swiss researchers to discover that although elevated CO2 reduced various leaf parameters (water content, proteins, non-structural carbohydrates, tannins, etc.) at the SCC site, “on the long term, their load with cynipid spangle-galls and leaf-mines of T. ekebladella was not distinguishable from that in oaks exposed to ambient CO2 after 4 years of treatment.” Kampichler et al. concluded that in the situation they investigated, “CO2 enrichment had no lasting effect in all three [animal] taxa, despite the substantial and consistent change in leaf chemistry of oak due to growth in elevated CO2.”
In conclusion, therefore, and considering the results of all of the studies reviewed in this section, it would appear that the ongoing rise in the air’s CO2 content will not result in greater damage to earth’s vegetation by the larvae of the many moths that inhabit the planet, and could reduce the damage they cause.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/i/summaries/moths.php.
Other Insects
Docherty et al. (1997), in addition to studying aphids, studied two sap-feeding leafhopper species that were allowed to feed on saplings of beech and sycamore that were grown in glasshouses maintained at atmospheric CO2 concentrations of 350 and 600 ppm. As far as they could determine, there were no significant effects of the extra CO2 on either the feeding or performance characteristics of either leafhopper species.
In a literature review of more than 30 studies published two years later, Whittaker (1999) found that chewing insects (leaf chewers and leaf miners) showed either no change or reductions in abundance in response to atmospheric CO2 enrichment, noting, however, that population reductions in this feeding guild were often accompanied by increased herbivory in response to CO2-induced reductions in leaf nitrogen content.
In an experiment conducted on a natural ecosystem in Wisconsin, USA—comprised predominantly of trembling aspen (Populus tremuloides Michx.)—Percy et al. (2002) studied the effects of increases in CO2 alone (to 560 ppm during daylight hours), O3 alone (to 46.4-55.5 ppb during daylight hours), and CO2 and O3 together on the forest tent caterpillar (Malacosoma disstria), a common leaf-chewing lepidopteran found in North American hardwood forests. By itself, elevated CO2 reduced caterpillar performance by reducing female pupal mass; while elevated O3 alone improved caterpillar performance by increasing female pupal mass. When both gases were applied together, however, the elevated CO2 completely counteracted the enhancement of female pupal mass caused by elevated O3. Hence, either alone or in combination with undesirable increases in the air’s O3 concentration, elevated CO2 tended to reduce the performance of the forest tent caterpillar. This finding is particularly satisfying because, in the words of Percy et al., “historically, the forest tent catepillar has defoliated more deciduous forest than any other insect in North America,” and because “outbreaks can reduce timber yield up to 90% in one year, and increase tree vulnerability to disease and environmental stress.”
In a study of yet another type of insect herbivore, Brooks and Whittaker (1999) removed grassland monoliths from the Great Dun Fell of Cumbria, UK—which contained eggs of a destructive xylem-feeding spittlebug (Neophilaenus lineatus)—and grew them in glasshouses maintained for two years at atmospheric CO2 concentrations of 350 and 600 ppm. During the course of their experiment, two generations of the xylem-feeding insect were produced; in each case, elevated CO2 reduced the survival of nymphal stages by an average of 24 percent. Brooks and Whittaker suggest that this reduction in survival rate may have been caused by CO2-induced reductions in stomatal conductance and transpirational water loss, which may have reduced xylem nutrient-water availability. Whatever the mechanism, the results of this study bode well for the future survival of these species-poor grasslands as the air’s CO2 content continues to rise.
In summing up the implications of the various phenomena described in this section, it would appear that both CO2-induced and warming-induced changes in the physical characteristics and behavioral patterns of a diverse assemblage of insect types portend good things for the biosphere in the years and decades to come.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/i/insectsother.php.
Shade
Is the growth-enhancing effect of atmospheric CO2 enrichment reduced when light intensities are less than optimal? The question may be important if a warmer world is also a cloudier world, as some climate models predict.
In a review of the scientific literature designed to answer this question, Kerstiens (1998) analyzed the results of 15 previously published studies of trees having differing degrees of shade tolerance, finding that elevated CO2 caused greater relative biomass increases in shade-tolerant species than in shade-intolerant or sun-loving species. In more than half of the studies analyzed, shade-tolerant species experienced CO2-induced relative growth increases that were two to three times greater than those of less shade-tolerant species.
In an extended follow-up review analyzing 74 observations from 24 studies, Kerstiens (2001) reported that twice-ambient CO2 concentrations increased the relative growth response of shade-tolerant and shade-intolerant woody species by an average of 51 and 18 percent, respectively. Similar results were reported by Poorter and Perez-Soba (2001), who performed a detailed meta-analysis of research results pertaining to this topic, and more recently by Kubiske et al. (2002), who measured photosynthetic acclimation in aspen and sugar maple trees. On the other hand, a 200-ppm increase in the air’s CO2 concentration was found to enhance the photosynthetic rates of sunlit and shaded leaves of sweetgum trees by 92 and 54 percent, respectively, at one time of year, and by 166 and 68 percent at another time (Herrick and Thomas, 1999). Likewise, Naumburg and Ellsworth (2000) reported that a 200-ppm increase in the air’s CO2 content boosted steady-state photosynthetic rates in leaves of four hardwood understory species by an average of 60 and 40 percent under high and low light intensities, respectively. Even though these photosynthetic responses were significantly less in shaded leaves, they were still substantial, with mean increases ranging from 40 to 68 percent for a 60 percent increase in atmospheric CO2 concentration.
Under extremely low light intensities, the benefits arising from atmospheric CO2 enrichment may be small, but oftentimes they are very important in terms of plant carbon budgeting. In the study of Hattenschwiler (2001), for example, seedlings of five temperate forest species subjected to an additional 200-ppm CO2 under light intensities that were only 3.4 and 1.3 percent of full sunlight exhibited CO2-induced biomass increases that ranged from 17 to 74 percent. Similarly, in the study of Naumburg et al. (2001), a 200-ppm increase in the air’s CO2 content enhanced photosynthetic carbon uptake in three of four hardwood understory species by more than two-fold in three of the four species under light irradiances that were as low as 3 percent of full sunlight.
In a final study, in which potato plantlets inoculated with an arbuscular mycorrhizal fungus were grown at various light intensities and super CO2 enrichment of approximately 10,000 ppm, Louche-Tessandier et al. (1999) found that the unusually high CO2 concentration produced an unusually high degree of root colonization by the beneficial mycorrhizal fungus, which typically helps supply water and nutrients to plants. And it did so irrespective of the degree of light intensity to which the potato plantlets were exposed.
So, whether light intensity is high or low, or leaves are shaded or sunlit, when the CO2 content of the air is increased, so too are the various biological processes that lead to plant robustness. Less than optimal light intensities do not negate the beneficial effects of atmospheric CO2 enrichment.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/lightinteraction.php.
Ozone
Plants grown in CO2-enriched air nearly always exhibit increased photosynthetic rates and biomass production relative to plants grown at the current ambient CO2 concentration. By contrast, plants exposed to elevated ozone concentrations typically display reductions in photosynthesis and growth in comparison with plants grown at the current ambient ozone concentration.
In discussing the problem of elevated tropospheric ozone (O3) concentrations, Liu et al. (2004) wrote that “ozone is considered to be one of the air pollutants most detrimental to plant growth and development in both urban and rural environments (Lefohn, 1992; Skarby et al., 1998; Matyssek and Innes, 1999),” because it “reduces the growth and yield of numerous agronomic crops as well as fruit and forest trees (Retzlaff et al., 1997; Fumagalli et al., 2001; Matyssek and Sandermann, 2003).” In addition, they say that ozone concentrations are “currently two to three times higher than in the early 1900s (Galloway, 1998; Fowler et al., 1999),” and that they likely “will remain high in the future (Elvingson, 2001).”
It is important to determine how major plants respond to concomitant increases in the abundances of these two trace gases of the atmosphere, as their concentrations will likely continue to increase for many years to come. We begin with a review of the literature with respect to various agriculture species, followed by a discussion on trees.
Additional information on this topic, including reviews on the interaction of CO2 and O3 not discussed here, can be found at http://www.co2 science.org/subject/o/subject_o.php under the heading Ozone.
Agricultural Species
Several studies have used soybean as a model plant to study the effects of elevated CO2 and ozone on photosynthesis and growth. Reid et al. (1998), for example, grew soybeans for an entire season at different combinations of atmospheric CO2 and ozone, reporting that elevated CO2 enhanced rates of photosynthesis in the presence or absence of ozone and that it typically ameliorated the negative effects of elevated ozone on carbon assimilation. At the cellular level, Heagle et al. (1998a) reported that at twice the current ambient ozone concentration, soybeans simultaneously exposed to twice the current ambient atmospheric CO2 concentration exhibited less foliar injury while maintaining significantly greater leaf chlorophyll contents than control plants exposed to elevated ozone and ambient CO2 concentrations. By harvest time, the plants grown in the elevated ozone/elevated CO2 treatment combination had produced 53 percent more total biomass than their counterparts did at elevated ozone and ambient CO2 concentrations (Miller et al., 1998). Finally, in analyzing seed yield, it was determined that atmospheric CO2 enrichment enhanced this parameter by 20 percent at ambient ozone, while it increased it by 74 percent at twice the ambient ozone concentration (Heagle et al., 1998b). Thus, elevated CO2 completely ameliorated the negative effects of elevated ozone concentration on photosynthetic rate and yield production in soybean.
The ameliorating responses of elevated CO2 to ozone pollution also have been reported for various cultivars of spring and winter wheat. In the study of Tiedemann and Firsching (2000), for example, atmospheric CO2 enrichment not only overcame the detrimental effects of elevated ozone on photosynthesis and growth, it overcame the deleterious consequences resulting from inoculation with a biotic pathogen as well. Although infected plants displayed less absolute yield than non-infected plants at elevated ozone concentrations, atmospheric CO2 enrichment caused the greatest relative yield increase in infected plants (57 percent vs. 38 percent).
McKee et al. (2000) reported that O3-induced reductions in leaf rubisco contents in spring wheat were reversed when plants were simultaneously exposed to twice-ambient concentrations of atmospheric CO2. In the study of Vilhena-Cardoso and Barnes (2001), elevated ozone concentrations reduced photosynthetic rates in spring wheat grown at three different soil nitrogen levels. However, when concomitantly exposed to twice-ambient atmospheric CO2 concentrations, elevated ozone had no effect on rates of photosynthesis, regardless of soil nitrogen. Going a step further, Pleijel et al. (2000) observed that ozone-induced reductions in spring wheat yield were partially offset by concomitant exposure to elevated CO2 concentrations. Similar results have been reported in spring wheat by Hudak et al. (1999) and in winter wheat by Heagle et al. (2000).
Cotton plants grown at elevated ozone concentrations exhibited 25 and 48 percent reductions in leaf mass per unit area and foliar starch concentration, respectively, relative to control plants grown in ambient air. When simultaneously exposed to twice-ambient CO2 concentrations, however, the reductions in these parameters were only 5 and 7 percent, respectively (Booker, 2000). With respect to potato, Wolf and van Oijen (2002) used a validated potato model to predict increases in European tuber production ranging from 1,000 to 3,000 kg of dry matter per hectare in spite of concomitant increases in ozone concentrations and air temperatures.
It is clear from these studies that elevated CO2 reduces, and nearly always completely overrides, the negative effects of ozone pollution on plant photosynthesis, growth, and yield. When explaining the mechanisms behind such responses, most authors suggest that atmospheric CO2 enrichment tends to reduce stomatal conductance, which causes less indiscriminate uptake of ozone into internal plant air spaces and reduces subsequent conveyance to tissues where damage often results to photosynthetic pigments and proteins, reducing plant growth and biomass production.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/o/ozoneplantsag.php.
Woody Species
Aspen
Karnosky et al. (1999) grew O3-sensitive and O3-tolerant aspen clones in 30-m diameter plots at the Aspen FACE site near Rhinelander, Wisconsin, USA, which were maintained at atmospheric CO2 concentrations of 360 and 560 ppm with and without exposure to elevated O3 (1.5 times ambient ozone concentration). After one year of growth at ambient CO2, elevated O3 had caused visible injury to leaves of both types of aspen, with the average percent damage in O3-sensitive clones being more than three times as great as that observed in O3-tolerant clones (55 percent vs. 17 percent, respectively). In combination with elevated CO2, however, O3-induced damage to leaves of these same clones was only 38 percent and 3 percent, respectively. Thus, elevated CO2 ameliorated much of the foliar damage induced by high O3 concentrations.
King et al. (2001) studied the same plants for a period of two years, concentrating on below-ground growth, where elevated O3 alone had no effect on fine-root biomass. When the two aspen clones were simultaneously exposed to elevated CO2 and O3, however, there was an approximate 66 percent increase in the fine-root biomass of both of them.
Also in the same experiment, Noormets et al. (2001) studied the interactive effects of O3 and CO2 on photosynthesis, finding that elevated CO2 increased rates of photosynthesis in both clones at all leaf positions. Maximum rates of photosynthesis were increased in the O3-tolerant clone by averages of 33 and 49 percent due to elevated CO2 alone and in combination with elevated O3, respectively, while in the O3-sensitive clone they were increased by 38 percent in both situations. Hence, CO2-induced increases in maximal rates of net photosynthesis were typically maintained, and sometimes increased, during simultaneous exposure to elevated O3.
Yet again in the same experiment, Oksanen et al. (2001) reported that after three years of treatment, ozone exposure caused significant structural injuries to thylakoid membranes and the stromal compartment within chloroplasts, but that these injuries were largely ameliorated by atmospheric CO2 enrichment. Likewise, leaf thickness, mesophyll tissue thickness, the amount of chloroplasts per unit cell area, and the amount of starch in leaf chloroplasts were all decreased in the high ozone treatment, but simultaneous exposure of the ozone-stressed trees to elevated CO2 more than compensated for the ozone-induced reductions.
After four years of growing five aspen clones with varying degrees of tolerance to ozone under the same experimental conditions, McDonald et al. (2002) developed what they termed a “competitive stress index,” based on the heights of the four nearest neighbors of each tree, to study the influence of competition on the CO2 growth response of the various clones as modified by ozone. In general, elevated O3 reduced aspen growth independent of competitive status, while the authors noted an “apparent convergence of competitive performance responses in +CO2 +O3 conditions,” which they say suggests that “stand diversity may be maintained at a higher level” in such circumstances.
Percy et al. (2002) utilized the same experimental setting to assess a number of the trees’ growth characteristics, as well as the responses of one plant pathogen and two insects with different feeding strategies that typically attack the trees. Of the plant pathogen studied, they say that “the poplar leaf rust, Melampsora medusae, is common on aspen and belongs to the most widely occurring group of foliage diseases.” As for the two insects, they report that “the forest tent caterpillar, Malacosoma disstria, is a common leaf-chewing lepidopteran in North American hardwood forests” and that “the sap-feeding aphid, Chaitophorus stevensis, infests aspen throughout its range.” Hence, the rust and the two insect pests the scientists studied are widespread and have significant deleterious impacts on trembling aspen and other tree species. As but one example of this fact, the authors note that, “historically, the forest tent caterpillar has defoliated more deciduous forest than any other insect in North America” and that “outbreaks can reduce timber yield up to 90% in one year, and increase tree vulnerability to disease and environmental stress.”
Percy et al. found that by itself, elevated O3 decreased tree height and trunk diameter, increased rust occurrence by nearly fourfold, improved tent caterpillar performance by increasing female pupal mass by 31 percent, and had a strong negative effect on the natural enemies of aphids. The addition of the extra CO2, however, completely ameliorated the negative effects of elevated O3 on tree height and trunk diameter, reduced the O3-induced enhancement of rust development from nearly fourfold to just over twofold, completely ameliorated the enhancement of female tent caterpillar pupal mass caused by elevated O3, and completely ameliorated the reduction in the abundance of natural enemies of aphids caused by elevated O3.
In a final study from the Aspen FACE site, Holton et al. (2003) raised parasitized and non-parasitized forest tent caterpillars on two quaking aspen genotypes (O3-sensitive and O3-tolerant) alone and in combination for one full growing season; they, too, found that elevated O3 improved tent caterpillar performance under ambient CO2 conditions, but not in CO2-enriched air.
In summary, it is clear that elevated ozone concentrations have a number of significant negative impacts on the well-being of North America’s most widely distributed tree species, while elevated carbon dioxide concentrations have a number of significant positive impacts. In addition, elevated CO2 often completely eliminates the negative impacts of elevated O3. If the tropospheric O3 concentration continues to rise as expected (Percy et al. note that “damaging O3 concentrations currently occur over 29% of the world’s temperate and subpolar forests but are predicted to affect fully 60% by 2100”), we might hope the air’s CO2 content continues to rise as well.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/o/ozoneaspen.php.
Beech
Liu et al. (2005) grew three- and four-year-old seedlings of European beech (Fagus sylvatica L.) for five months in well watered and fertilized soil in containers located within walk-in phytotrons maintained at either ambient or ambient + 300 ppm CO2 (each subdivided into ambient and double-ambient O3 concentration treatments, with maximum ozone levels restricted to <150 ppb), in both monoculture and in competition with Norway spruce, after which they examined the effects of each treatment on leaf non-structural carbohydrate levels (soluble sugars and starch). They found that the effects of elevated O3 alone on non-structural carbohydrate levels were small when the beech seedlings were grown in monoculture. When they were grown in mixed culture, however, the elevated O3 slightly enhanced leaf sugar levels, but reduced starch levels by 50 percent.
With respect to elevated CO2 alone, for the beech seedlings grown in both monoculture and mixed culture, levels of sugar and starch were significantly enhanced. Hence, when elevated O3 and CO2 significantly affected non-structural carbohydrate levels, elevated CO2 tended to enhance them, whereas elevated O3 tended to reduce them. In addition, the combined effects of elevated CO2 and O3 acting together were such as to produce a significant increase in leaf non-structural carbohydrates in both mixed and monoculture conditions. As a result, the researchers concluded that “since the responses to the combined exposure were more similar to elevated pCO2 than to elevated pO3, apparently elevated pCO2 overruled the effects of elevated pO3 on non-structural carbohydrates.”
In a slightly longer study, Grams et al. (1999) grew European beech seedlings in glasshouses maintained at average atmospheric CO2 concentrations of either 367 or 667 ppm for a period of one year. Then, throughout the following year, in addition to being exposed to the same set of CO2 concentrations the seedlings were exposed to either ambient or twice-ambient levels of O3. This protocol revealed that elevated O3 significantly reduced photosynthesis in beech seedlings grown at ambient CO2 concentrations by a factor of approximately three. By contrast, in the CO2-enriched air the seedlings did not exhibit any photosynthetic reduction due to the doubled O3 concentrations. In fact, the photosynthetic rates of the CO2-enriched seedlings actually rose by 8 percent when simultaneously fumigated with elevated O3, leading the researchers to conclude that “long-term acclimation to elevated CO2 supply does counteract the O3-induced decline of photosynthetic light and dark reactions.”
In a still longer study, Liu et al. (2004) grew three- and four-year-old beech seedlings for two growing seasons under the same experimental conditions as Liu et al. (2005) after the seedlings had been pre-acclimated for one year to either the ambient or elevated CO2 treatment. At the end of the study, the plants were harvested and fresh weights and dry biomass values were determined for leaves, shoot axes, coarse roots, and fine roots, as were carbohydrate (starch and soluble sugar) contents and concentrations for the same plant parts. This work falsified the hypothesis that “prolonged exposure to elevated CO2 does not compensate for the adverse ozone effects on European beech,” as it revealed that all “adverse effects of ozone on carbohydrate concentrations and contents were counteracted when trees were grown in elevated CO2.”
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/o/ozonebeech.php.
Birch
At the FACE facility near Rhinelander, Wisconsin, USA, King et al. (2001) grew a mix of paper birch and quaking aspen trees in 30-m diameter plots that were maintained at atmospheric CO2 concentrations of 360 and 560 ppm with and without exposure to elevated O3 (1.5 times the ambient O3 concentration) for a period of two years. In their study of the below-ground environment of the trees, they found that the extra O3 had no effect on the growth of fine roots over that time period, but that elevated O3 and CO2 together increased the fine-root biomass of the mixed stand by 83 percent.
One year later at the same FACE facility, Oksanen et al. (2001) observed O3-induced injuries in the thylokoid membranes of the chloroplasts of the birch trees’ leaves; the injuries were partially ameliorated in the elevated CO2 treatment. And in a study conducted two years later, Oksanen et al. (2003) say they “were able to visualize and locate ozone-induced H2O2 accumulation within leaf mesophyll cells, and relate oxidative stress with structural injuries.” However, they report that “H2O2 accumulation was found only in ozone-exposed leaves and not in the presence of elevated CO2,” adding that “CO2 enrichment appears to alleviate chloroplastic oxidative stress.”
Across the Atlantic in Finland, Kull et al. (2003) constructed open-top chambers around two clones (V5952 and K1659) of silver birch saplings that were rooted in the ground and had been growing there for the past seven years. These chambers were fumigated with air containing 360 and 720 ppm CO2 in combination with 30 and 50 ppb O3 for two growing seasons, after which it was noted that the extra O3 had significantly decreased branching in the trees’ crowns. This malady, however, was almost completely ameliorated by a doubling of the air’s CO2 concentration. In addition, after one more year of study, Eichelmann et al. (2004) reported that, by itself, the increase in the air’s CO2 content increased the average net photosynthetic rates of both clones by approximately 16 percent, while the increased O3 by itself caused a 10 percent decline in the average photosynthetic rate of clone V5952, but not of clone K1659. When both trace gases were simultaneously increased, however, the photosynthetic rate of clone V5952 once again experienced a 16 percent increase in net photosynthesis, as if the extra O3 had had no effect when applied in the presence of the extra CO2.
After working with the same trees for one additional year, Riikonen et al. (2004) harvested them and reported finding that “the negative effects of elevated O3 were found mainly in ambient CO2, not in elevated CO2.” In fact, whereas doubling the air’s O3 concentration decreased total biomass production by 13 percent across both clones, simultaneously doubling the air’s CO2 concentration increased total biomass production by 30 percent, thereby more than compensating for the deleterious consequences of doubling the atmospheric ozone concentration.
In commenting on this ameliorating effect of elevated CO2, the team of Finnish scientists said it “may be associated with either increased detoxification capacity as a consequence of higher carbohydrate concentrations in leaves grown in elevated CO2, or decreased stomatal conductance and thus decreasing O3 uptake in elevated CO2 conditions (e.g., Rao et al., 1995).” They also noted that “the ameliorating effect of elevated CO2 is in accordance with the results of single-season open-top chamber and growth chamber studies on small saplings of various deciduous tree species (Mortensen 1995; Dickson et al., 1998; Loats and Rebbeck, 1999) and long-term open-field and OTC studies with aspen and yellow-poplar (Percy et al., 2002; Rebbeck and Scherzer, 2002).”
In another paper to come out of the Finnish silver birch study, Peltonen et al. (2005) evaluated the impacts of doubled atmospheric CO2 and O3 concentrations on the accumulation of 27 phenolic compounds in the leaves of the trees, finding that elevated CO2 increased the concentration of phenolic acids (+25 percent), myricetin glycosides (+18 percent), catechin derivatives (+13 percent), and soluble condensed tannins (+19 percent). Elevated O3, on the other hand, increased the concentration of one glucoside by 22 percent, chlorogenic acid by 19 percent, and flavone aglycons by 4 percent. However, Peltonen et al. say this latter O3-induced production of antioxidant phenolic compounds “did not seem to protect the birch leaves from detrimental O3 effects on leaf weight and area, but may have even exacerbated them.” Last, in the combined elevated CO2 and O3 treatment, they found that “elevated CO2 did seem to protect the leaves from elevated O3 because all the O3-derived effects on the leaf phenolics and traits were prevented by elevated CO2.”
Meanwhile, back at the FACE facility near Rhinelander, Wisconsin, USA, Agrell et al. (2005) examined the effects of ambient and elevated concentrations of atmospheric CO2 and O3 on the foliar chemistry of birch and aspen trees, plus the consequences of these effects for host plant preferences of forest tent caterpillar larvae. In doing so, they found that “the only chemical component showing a somewhat consistent co-variation with larval preferences was condensed tannins,” and they discovered 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 concentration of birch leaves was 18 percent higher in the elevated CO2 and O3 treatment. Consequently, as atmospheric concentrations of CO2 and O3 continue to rise, the increases in condensed tannin concentrations likely to occur in the foliage of birch trees should lead to their leaves becoming less preferred for consumption by the forest tent caterpillar.
Concurrent with the work of Agrell et al., King et al. (2005) evaluated the effect of CO2 enrichment alone, O3 enrichment alone, and the net effect of both CO2 and O3 enrichment together on the growth of the Rhinelander birch trees, finding that relative to the ambient-air control treatment, elevated CO2 increased total biomass by 45 percent in the aspen-birch community, while elevated O3 caused a 13 percent reduction in total biomass relative to the control. Of most interest, the combination of elevated CO2 and O3 resulted in a total biomass increase of 8.4 percent relative to the control aspen-birch community. King et al. thus concluded that “exposure to even moderate levels of O3 significantly reduces the capacity of net primary productivity to respond to elevated CO2 in some forests.” Consequently, they suggested it makes sense to move forward with technologies that reduce anthropogenic precursors to photochemical O3 formation, because the implementation of such a policy would decrease an important constraint on the degree to which forest ecosystems can positively respond to the ongoing rise in the air’s CO2 concentration.
Another paper to come out of the Finnish silver birch study was that of Kostiainen et al. (2006), who studied the effects of elevated CO2 and O3 on various wood properties. Their work revealed that the elevated CO2 treatment had no effect on wood structure, but that it increased annual ring width by 21 percent, woody biomass by 23 percent, and trunk starch concentration by 7 percent. Elevated O3, on the other hand, decreased stem vessel percentage in one of the clones by 10 percent; it had no effect on vessel percentage in the presence of elevated CO2.
In discussing their results, Kostiainen et al. note that “in the xylem of angiosperms, water movement occurs principally in vessels (Kozlowski and Pallardy, 1997),” and that “the observed decrease in vessel percentage by elevated O3 may affect water transport,” lowering it. However, as they continue, “elevated CO2 ameliorated the O3-induced decrease in vessel percentage.” In addition, they note that “the concentration of nonstructural carbohydrates (starch and soluble sugars) in tree tissues is considered a measure of carbon shortage or surplus for growth (Korner, 2003).” They conclude that “starch accumulation observed under elevated CO2 in this study indicates a surplus of carbohydrates produced by enhanced photosynthesis of the same trees (Riikonen et al., 2004).” In addition, they report that “during winter, starch reserves in the stem are gradually transformed to soluble carbohydrates involved in freezing tolerance (Bertrand et al., 1999; Piispanen and Saranpaa, 2001), so the increase in starch concentration may improve acclimation in winter.”
Rounding out the suite of Rhinelander FACE studies of paper birch is the report of Darbah et al. (2007), who found that the total number of trees that flowered increased by 139 percent under elevated CO2 but only 40 percent under elevated O3. Likewise, with respect to the quantity of flowers produced, they found that elevated CO2 led to a 262 percent increase, while elevated O3 led to only a 75 percent increase. They also determined that elevated CO2 had significant positive effects on birch catkin size, weight, and germination success rate, with elevated CO2 increasing the germination rate of birch by 110 percent, decreasing seedling mortality by 73 percent, increasing seed weight by 17 percent, and increasing new seedling root length by 59 percent. They found just the opposite was true of elevated O3, as it decreased the germination rate of birch by 62 percent, decreased seed weight by 25 percent, and increased new seedling root length by only 15 percent.
In discussing their findings, Darbah et al. additionally report that “the seeds produced under elevated O3 had much less stored carbohydrate, lipids, and proteins for the newly developing seedlings to depend on and, hence, the slow growth rate.” As a result, they conclude that “seedling recruitment will be enhanced under elevated CO2 but reduced under elevated O3.”
In summary, from their crowns to their roots, birch trees are generally negatively affected by rising ozone concentrations. When the air’s CO2 content is also rising, however, these negative consequences may often be totally eliminated and replaced by positive responses.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/o/ozonebirch.php.
Yellow-Poplar
Scherzel et al. (1998) grew yellow-poplar seedlings in open-top chambers for four years at three different combinations of atmospheric O3 and CO2—(1) ambient O3 and ambient CO2, (2) doubled O3 and ambient CO2, and (3) doubled O3 and doubled CO2—to study the interactive effects of these gases on leaf-litter decomposition. This experiment revealed that the decomposition rates of yellow-poplar leaves were similar for all three treatments for nearly five months, after which time litter produced in the elevated O3 and elevated CO2 air decomposed at a significantly slower rate, such that even after two years of decomposition, litter from the elevated O3 and elevated CO2 treatment still contained about 12 percent more biomass than litter produced in the other two treatments. This reduced rate of decomposition under elevated O3 and CO2 conditions will likely result in greater carbon sequestration in soils supporting yellow-poplar trees over the next century or more.
Loats and Rebbeck (1999) grew yellow-poplar seedlings for ten weeks in pots they placed within growth chambers filled with ambient air, air with twice the ambient CO2 concentration, air with twice the ambient O3 concentration, and air with twice the ambient CO2 and O3 concentrations to determine the effects of elevated CO2 and O3 on photosynthesis and growth in this deciduous tree species. In doing so, they found that doubling the air’s CO2 concentration increased the rate of net photosynthesis by 55 percent in ambient O3 air, and that at twice the ambient level of O3 it stimulated net photosynthesis by an average of 50 percent. Similarly, the doubled CO2 concentration significantly increased total biomass by 29 percent, while the doubled O3 concentration had little impact on growth.
Last, Rebbeck et al. (2004) grew yellow poplar seedlings for five years within open-top chambers in a field plantation at Delaware, Ohio, USA, exposing them continuously from mid-May through mid-October of each year to either (1) charcoal-filtered air to remove ambient O3, (2) ambient O3, (3) 1.5 times ambient O3, and (4) 1.5 times ambient O3 plus 350 ppm CO2 above ambient CO2, while they periodically measured a number of plant parameters and processes. Throughout the study, the trees were never fertilized, and they received no supplemental water beyond some given in the first season.
Averaged over the experiment’s five growing seasons, the midseason net photosynthetic rate of upper canopy foliage at saturating light intensities declined by 10 percent when the trees were grown in ambient O3-air and by 14 percent when they were grown in elevated O3-air, when compared to the trees that were grown in the charcoal-filtered air, while seasonal net photosynthesis of foliage grown in the combination of elevated O3 and elevated CO2 was 57-80 percent higher than it was in the trees exposed to elevated O3 alone. There was also no evidence of any photosynthetic down regulation in the trees exposed to the elevated O3 and CO2 air, with some of the highest rates being observed during the final growing season. Consequently, Rebbeck et al. concluded that “elevated CO2 may ameliorate the negative effects of increased tropospheric O3 on yellow-poplar.” In fact, their results suggest that a nominally doubled atmospheric CO2 concentration more than compensates for the deleterious effects of a 50 percent increase in ambient O3 levels.
As the air’s CO2 content continues to rise, earth’s yellow-poplar trees will likely display substantial increases in photosynthetic rate and biomass production, even under conditions of elevated O3 concentrations; and the soils in which the trees grow should sequester ever greater quantities of carbon.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/o/ozoneyellowpoplar.php.
Low Temperatures
Only a handful of studies have attempted to determine what relationship, if any, exists between atmospheric CO2 enrichment and the ability of plants to withstand the rigors of low temperatures.
Loik et al. (2000) grew three Yucca species (brevifolia, schidigera, and whipplei) in pots placed within glasshouses maintained at atmospheric CO2 concentrations of 360 and 700 ppm and day/night air temperatures of 40/24°C for seven months, after which some of the plants were subjected to a two-week day/night air temperature treatment of 20/5°C. In addition, leaves from each Yucca species were removed and placed in a freezer that was cooled at a rate of 3°C per hour until a minimum temperature of ‑15°C was reached. These manipulations indicated that elevated CO2 lowered the air temperature at which 50 percent low-temperature-induced cell mortality occurred by 1.6, 1.4 and 0.8°C in brevifolia, schidigera and whipplei, respectively. On the basis of the result obtained for Y. brevifolia, Dole et al. (2003) estimated that “the increase in freezing tolerance caused by doubled CO2 would increase the potential habitat of this species by 14%.”
By contrast, Obrist et al. (2001) observed the opposite response. In an open-top chamber study of a temperate grass ecosystem growing on a nutrient-poor calcareous soil in northwest Switzerland, portions of which had been exposed to atmospheric CO2 concentrations of 360 and 600 ppm for a period of six years, they determined that the average temperature at which 50 percent low-temperature-induced leaf mortality occurred in five prominent species actually rose by an average of 0.7°C in response to the extra 240 ppm of CO2 employed in their experiment.
Most relevant investigations, however, have produced evidence of positive CO2 effects on plant low temperature tolerance. Sigurdsson (2001), for example, grew black cottonwood seedlings near Gunnarsholt, Iceland within closed-top chambers maintained at ambient and twice-ambient atmospheric CO2 concentrations for a period of three years, finding that elevated CO2 tended to hasten the end of the growing season. This effect was interpreted as enabling the seedlings to better avoid the severe cold-induced dieback of newly produced tissues that often occurs with the approach of winter in this region. Likewise, Wayne et al. (1998) found that yellow birch seedlings grown at an atmospheric CO2 concentration of 800 ppm exhibited greater dormant bud survivorship at low air temperatures than did seedlings grown at 400 ppm CO2.
Schwanz and Polle (2001) investigated the effects of elevated CO2 on chilling stress in micropropagated hybrid poplar clones that were subsequently potted and transferred to growth chambers maintained at either ambient (360 ppm) or elevated (700 ppm) CO2 for a period of three months. They determined that “photosynthesis was less diminished and electrolyte leakage was lower in stressed leaves from poplar trees grown under elevated CO2 as compared with those from ambient CO2.” Although severe chilling did cause pigment and protein degradation in all stressed leaves, the damage was expressed to a lower extent in leaves from the elevated CO2 treatment. This CO2-induced chilling protection was determined to be accompanied by a rapid induction of superoxide dismutase activity, as well as by slightly higher stabilities of other antioxidative enzymes.
Another means by which chilling-induced injury may be reduced in CO2-enriched air is suggested by the study of Sgherri et al. (1998), who reported that raising the air’s CO2 concentration from 340 to 600 ppm increased lipid concentrations in alfalfa thylakoid membranes while simultaneously inducing a higher degree of unsaturation in the most prominent of those lipids. Under well-watered conditions, for example, the 76 percent increase in atmospheric CO2 enhanced overall thylakoid lipid concentration by about 25 percent, while it increased the degree of unsaturation of the two main lipids by approximately 17 percent and 24 percent. Under conditions of water stress, these responses were found to be even greater, as thylakoid lipid concentration rose by approximately 92 percent, while the degree of unsaturation of the two main lipids rose by about 22 percent and 53 percent.
Several studies conducted over the past decade explain what these observations have to do with a plant’s susceptibility to chilling injury. Working with wild-type Arabidopsis thaliana and two mutants deficient in thylakoid lipid unsaturation, Hugly and Somerville (1992) found that “chloroplast membrane lipid polyunsaturation contributes to the low-temperature fitness of the organism,” and that it “is required for some aspect of chloroplast biogenesis.” When lipid polyunsaturation was low, they observed “dramatic reductions in chloroplast size, membrane content, and organization in developing leaves.” There was a positive correlation “between the severity of chlorosis in the two mutants at low temperatures and the degree of reduction in polyunsaturated chloroplast lipid composition.”
Working with tobacco, Kodama et al. (1994) demonstrated that the low-temperature-induced suppression of leaf growth and concomitant induction of chlorosis observed in wild-type plants was much less evident in transgenic plants containing a gene that allowed for greater expression of unsaturation in the fatty acids of leaf lipids. This observation and others led them to conclude that substantially unsaturated fatty acids “are undoubtedly an important factor contributing to cold tolerance.”
In a closely related study, Moon et al. (1995) found that heightened unsaturation of the membrane lipids of chloroplasts stabilized the photosynthetic machinery of transgenic tobacco plaints against low-temperature photoinibition “by accelerating the recovery of the photosystem II protein complex.” Likewise, Kodama et al. (1995), also working with transgenic tobacco plants, showed that increased fatty acid desaturation is one of the prerequisites for normal leaf development at low, nonfreezing temperatures; and Ishizaki-Nishizawa et al. (1996) demonstrated that transgenic tobacco plants with a reduced level of saturated fatty acids in most membrane lipids “exhibited a significant increase in chilling resistance.”
Many economically important crops, such as rice, maize and soybeans, are classified as chilling-sensitive and experience injury or death at temperatures between 0 and 15°C (Lyons, 1973). If atmospheric CO2 enrichment enhances their production and degree-of-unsaturation of thylakoid lipids, as it does in alfalfa, a continuation of the ongoing rise in the air’s CO2 content could increase the abilities of these important agricultural species to withstand periodic exposure to debilitating low temperatures. This phenomenon could provide the extra boost in food production that will be needed to sustain an increasing population in the years and decades ahead.
Earth’s natural ecosystems would also benefit from a CO2-induced increase in thylakoid lipids containing more-highly unsaturated fatty acids. Many plants of tropical origin, for example, suffer cold damage when temperatures fall below 20°C (Graham and Patterson, 1982). With improved lipid characteristics provided by the ongoing rise in the air’s CO2 content, such plants would be able to expand their ranges both poleward and upward in a higher-CO2 world.
More research remains to be done before we can accurately assess the extent of these potential biological benefits. In particular, we must conduct more studies of the effects of atmospheric CO2 enrichment on the properties of thylakoid lipids in a greater variety of plants. In the same experiments, we must assess the efficacy of these lipid property changes in enhancing plant tolerance of low temperatures. Such studies should rank high on the to-do list of relevant funding agencies.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/f/frosthardiness.php.
Nitrogen Deficiency
Numerous studies have investigated the effects of different soil nitrogen (N) concentrations on plant responses to increases in the air’s CO2 content, as it has been claimed that a deficiency of soil nitrogen lessens the relative growth stimulation in plants that is typically provided by elevated concentrations of atmospheric CO2. In this section, we evaluate the credibility of that claim for various crops, fungi, grasses and trees.
The results of these experiments indicate that some plants sometimes will not respond at all to atmospheric CO2 enrichment at low levels of soil N, while some will. Some plants respond equally well to increases in the air’s CO2 content when growing in soils exhibiting a whole range of N concentrations. Most common, however, is the observation that plants respond ever better to rising atmospheric CO2 concentrations as soil N concentrations rise. Interestingly, the current state of earth’s atmosphere and land surface is one of jointly increasing CO2 and N concentrations. Hence, the outlook is good for continually increasing terrestrial vegetative productivity in the years and decades ahead, as these trends continue.
Additional information on this topic, including reviews on nitrogen not discussed here, can be found at http://www.co2science.org/subject/g/subject_g.php under the heading Growth Response to CO2 With Other Variables: Nutrients: Nitrogen, as well as at http://www.co2science.org/subject/n/subject_n.php under the headings Nitrogen, Nitrogen Fixation and Nitrogen Use Efficiency.
Crops
Rice
Does a deficiency of soil nitrogen lessen the relative growth and yield stimulation of rice that is typically provided by elevated levels of atmospheric CO2? In exploring this question, Weerakoon et al. (1999) grew seedlings of two rice cultivars for 28 days in glasshouses maintained at atmospheric CO2 concentrations of 373, 545, 723 and 895 ppm under conditions of low, medium and high soil nitrogen content. After four weeks of treatment, photosynthesis was found to significantly increase with increasing nitrogen availability and atmospheric CO2 concentration. Averaged across all nitrogen regimes, plants grown at 895 ppm CO2 exhibited photosynthetic rates that were 50 percent greater than those observed in plants grown at ambient CO2. Total plant dry weight also increased with increasing atmospheric CO2. In addition, the percentage growth enhancement resulting from CO2 enrichment increased with increasing soil nitrogen; from 21 percent at the lowest soil nitrogen concentration to 60 percent at the highest concentration.
Using a different CO2 enrichment technique, Weerakoon et al. (2000) grew rice in open-top chambers maintained at atmospheric CO2 concentrations of approximately 350 and 650 ppm during a wet and dry growing season and under a range of soil nitrogen contents. Early in both growing seasons, plants exposed to elevated atmospheric CO2 concentrations intercepted significantly more sunlight than plants fumigated with ambient air, due to CO2-induced increases in leaf area index. This phenomenon occurred regardless of soil nitrogen content, but disappeared shortly after canopy closure in all treatments. Later, mature canopies achieved similar leaf area indexes at identical levels of soil nitrogen supply; but mean season-long radiation use efficiency, which is the amount of biomass produced per unit of solar radiation intercepted, was 35 percent greater in CO2-enriched vs. ambiently grown plants and tended to increase with increasing soil nitrogen content.
Utilizing a third approach to enriching the air about a crop with elevated levels of atmospheric CO2, Kim et al. (2003) grew rice crops from the seedling stage to maturity at atmospheric CO2 concentrations of ambient and ambient plus 200 ppm using FACE technology and three levels of applied nitrogen—low (LN, 4 g N m-2), medium (MN, 8 and 9 g N m-2) and high (HN, 15 g N m-2)—for three cropping seasons (1998-2000). They report that “the yield response to elevated CO2 in crops supplied with MN (+14.6%) or HN (+15.2%) was about twice that of crops supplied with LN (+7.4%),” confirming the importance of nitrogen availability to the response of rice to atmospheric CO2 enrichment previously determined by Kim et al. (2001) and Kobaysahi et al. (2001).
In light of these observations, it would appear that the maximum benefits of elevated levels of atmospheric CO2 for the growth and grain production of rice cannot be realized in soils that are highly deficient in nitrogen. Increasing nitrogen concentrations above what is considered adequate may not result in proportional gains in CO2-induced growth and yield enhancement.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenrice.php.
Wheat
Smart et al. (1998) grew wheat from seed for 23 days in controlled environment chambers maintained at atmospheric CO2 concentrations of 360 and 1000 ppm and two concentrations of soil nitrate, finding that the extra CO2 increased average plant biomass by approximately 15 percent, irrespective of soil nitrogen content. In a more realistic FACE experiment, however, Brooks et al. (2000) grew spring wheat for two seasons at atmospheric CO2 concentrations of 370 and 570 ppm at both high and low levels of nitrogen fertility; and they obtained twice the yield enhancement (16 percent vs. 8 percent) in the high nitrogen treatment.
In an experiment with one additional variable, Vilhena-Cardoso and Barnes (2001) grew spring wheat for two months in environmental chambers fumigated with air containing atmospheric CO2 concentrations of either 350 or 700 ppm at ambient and elevated (75 ppb) ozone concentrations, while the plants were simultaneously subjected to either low, medium or high levels of soil nitrogen. With respect to biomass production, the elevated CO2 treatment increased total plant dry weight by 44, 29 and 12 percent at the high, medium and low soil nitrogen levels, respectively. In addition, although elevated ozone alone reduced plant biomass, the simultaneous application of elevated CO2 completely ameliorated its detrimental effects on biomass production, irrespective of soil nitrogen supply.
Why do the plants of some studies experience a major reduction in the relative growth stimulation provided by atmospheric CO2 enrichment under low soil nitrogen conditions, while other studies find the aerial fertilization effect of elevated CO2 to be independent of root-zone nitrogen concentration? Based on studies of both potted and hydroponically grown plants, Farage et al. (1998) determined that low root-zone nitrogen concentrations need not lead to photosynthetic acclimation (less than maximum potential rates of photosynthesis) in elevated CO2, as long as root-zone nitrogen supply is adequate to meet plant nitrogen needs to maintain the enhanced relative growth rate that is made possible by atmospheric CO2 enrichment. When supply cannot meet this need, as is often the case in soils with limited nitrogen reserves, the aerial fertilization effect of atmospheric CO2 enrichment begins to be reduced and less-than-potential CO2-induced growth stimulation is observed. Nevertheless, the acclimation process is the plant’s “first line of defense” to keep its productivity from falling even further than it otherwise would, as it typically mobilizes nitrogen from “excess” rubisco and sends it to more needy plant sink tissues to allow for their continued growth and development (Theobald et al., 1998).
In conclusion, although atmospheric CO2 enrichment tends to increase the growth and yield of wheat under a wide range of soil nitrogen concentrations, including some that are very low, considerably greater CO2-induced enhancements are possible when more soil nitrogen is available, although the response can saturate at high soil nitrogen levels, with excess nitrogen providing little to no extra yield.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenwheat.php.
Other
Zerihun et al. (2000) grew sunflowers for one month in pots of three different soil nitrogen concentrations that were placed within open-top chambers maintained at atmospheric CO2 concentrations of 360 and 700 ppm. The extra CO2 of the CO2-enriched chambers reduced average rates of root nitrogen uptake by about 25 percent, which reduction, by itself, would normally tend to reduce tissue nitrogen contents and the relative growth rates of the seedlings. However, the elevated CO2 also increased photosynthetic nitrogen-use efficiency by an average of 50 percent, which increase normally tends to increase the relative growth rates of seedlings. Of these two competing effects, the latter was the more powerful, leading to an increase in whole plant biomass. After the one month of the study, for example, the CO2-enriched plants exhibited whole plant biomass values that were 44, 13 and 115 percent greater than those of the plants growing in ambient air at low, medium and high levels of soil nitrogen, respectively, thus demonstrating that low tissue nitrogen contents do not necessarily preclude a growth response to atmospheric CO2 enrichment, particularly if photosynthetic nitrogen-use efficiency is enhanced, which is typically the case, as it was in this study. Nevertheless, the greatest CO2-induced growth increase of Zerihun et al.’s study was exhibited by the plants growing in the high soil nitrogen treatment.
Deng and Woodward (1998) grew strawberries in environment-controlled glasshouses maintained at atmospheric CO2 concentrations of 390 and 560 ppm for nearly three months. In addition, the strawberries were supplied with fertilizers containing three levels of nitrogen. The extra CO2 increased rates of net photosynthesis and total plant dry weight at all three nitrogen levels, but the increases were not significant. Nevertheless, they provided the CO2-enriched plants with enough additional sugar and physical mass to support significantly greater numbers of flowers and fruits than the plants grown at 390 ppm CO2. This effect consequently led to total fresh fruit weights that were 42 and 17 percent greater in the CO2-enriched plants that received the highest and lowest levels of nitrogen fertilization, respectively, once again indicating a greater growth response at higher nitrogen levels.
Newman et al. (2003) investigated the effects of two levels of nitrogen fertilization and an approximate doubling of the air’s CO2 concentration on the growth of tall fescue, which is an important forage crop. The plants with which they worked were initially grown from seed in greenhouse flats, but after sixteen weeks they were transplanted into 19-liter pots filled with potting media that received periodic applications of a slow-release fertilizer. Then, over the next two years of outdoor growth, they were periodically clipped, divided and repotted to ensure they did not become root-bound; and at the end of that time, they were placed within twenty 1.3-m-diameter open-top chambers, half of which were maintained at the ambient atmospheric CO2 concentration and half of which were maintained at an approximately doubled CO2 concentration of 700 ppm. In addition, half of the pots in each CO2 treatment received 0.0673 kg N m-2 applied over a period of three consecutive days, while half of them received only one-tenth that amount, with the entire procedure being repeated three times during the course of the 12-week experiment. Newman et al. report that the plants grown in the high-CO2 air photosynthesized 15 percent more and produced 53 percent more dry matter (DM) under low N conditions and 61 percent more DM under high N conditions. In addition, they report that the percent organic matter (OM) was little changed, except under elevated CO2 and high N, when %OM (as %DM) increased by 3 percent. In this study too, therefore, the greatest relative increase in productivity occurred under high, as opposed to low, soil N availability.
Demmers-Derks et al. (1998) grew sugar beets as an annual crop in controlled-environment chambers at atmospheric CO2 concentrations of 360 and 700 ppm and air temperatures of ambient and ambient plus 3°C for three consecutive years. In addition to being exposed to these CO2 and temperature combinations, the sugar beets were supplied with solutions of low and high nitrogen content. Averaged across all three years and both temperature regimes, the extra CO2 of this study enhanced total plant biomass by 13 and 25 percent in the low and high nitrogen treatments, respectively. In addition, it increased root biomass by 12 and 26 percent for the same situations. As was the case with sunflowers, strawberries and tall fescue, elevated CO2 elicited the largest growth responses in the sugar beets that received a high, as opposed to a low, supply of nitrogen.
Also working with sugar beets were Romanova et al. (2002), who grew them from seed for one month in controlled environment chambers maintained at atmospheric CO2 concentrations of 350 and 700 ppm, while fertilizing them with three different levels of nitrate-nitrogen. In this study, the plants grown in CO2-enriched air exhibited rates of net photosynthesis that were approximately 50 percent greater than those displayed by the plants grown in ambient air, regardless of soil nitrate availability. These CO2-induced increases in photosynthetic carbon uptake contributed to 60, 40 and 30 percent above-ground organ dry weight increases in plants receiving one-half, standard, and three-fold levels of soil nitrate, respectively. Root weights, however, were less responsive to atmospheric CO2 enrichment, displaying 10 and 30 percent increases in dry weight at one-half and standard nitrate levels, but no increase at the high soil nitrate concentration. In this study, therefore, the role of soil nitrogen fertility was clearly opposite to that observed in the four prior studies in the case of above-ground biomass production, but was mixed in the case of belowground biomass production.
Switching to barley, Fangmeier et al. (2000) grew plants in containers placed within open-top chambers maintained at atmospheric CO2 concentrations of either 360 or 650 ppm and either a high or low nitrogen fertilization regime. As in the case of the above-ground biomass response of the sugar beets of Romanova et al., the elevated CO2 had the greatest relative impact on yield when the plants were grown under the less-than-optimum low-nitrogen regime, i.e., a 48 percent increase vs. 31 percent under high-nitrogen conditions.
Last, we report the pertinent results of the review and analysis of Kimball et al. (2002), who summarized the findings of most FACE studies conducted on agricultural crops since the introduction of that technology back in the late 1980s. In response to a 300-ppm increase in the air’s CO2 concentration, rates of net photosynthesis in several C3 grasses were enhanced by an average of 46 percent under conditions of ample soil nitrogen supply and by 44 percent when nitrogen was limiting to growth. With respect to above-ground biomass production, the differential was much larger, with the C3 grasses wheat, rice and ryegrass experiencing an average increase of 18 percent at ample nitrogen but only 4 percent at low nitrogen; while with respect to belowground biomass production, they experienced an average increase of 70 percent at ample nitrogen and 58 percent at low nitrogen. Similarly, clover experienced a 38 percent increase in belowground biomass production at ample soil nitrogen, and a 32 percent increase at low soil nitrogen. Finally, with respect to agricultural yield, which is the bottom line in terms of food and fiber production, wheat and ryegrass experienced an average increase of 18 percent at ample nitrogen, while wheat experienced only a 10 percent increase at low nitrogen.
In light of these several results, it can be safely concluded that although there are some significant exceptions to the rule, most agricultural crops generally experience somewhat greater CO2-induced relative (percentage) increases in net photosynthesis and biomass production even when soil nitrogen concentrations are a limiting factor.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenagriculture.php.
Fungi
Nearly all of earth’s plants become involved in intimate relationships with different fungal species at one point or another in their life cycles. Among other things, the fungi commonly aid plants in the acquisition of water and important soil nutrients. In addition, fungal-plant interactions are often impacted by variations in both atmospheric CO2 and soil nitrogen concentrations. In this subsection, we review how various aspects of fungal-plant interactions are influenced by elevated CO2 under varying soil nitrogen regimes.
In a one-year study conducted by Walker et al. (1998), ponderosa pine seedlings exposed to atmospheric CO2 concentrations of 525 and 700 ppm displayed total numbers of ectomycorrhizal fungi on their roots that were 170 and 85 percent greater, respectively, than those observed on roots of ambiently grown seedlings.
In the study of Rillig et al. (1998), three grasses and two herbs fumigated with ambient air and air containing an extra 350 ppm CO2 for four months displayed various root infection responses by arbuscular mycorrhizal fungi, which varied with soil nitrogen supply. At low soil nitrogen contents, elevated CO2 increased the percent root infection by this type of fungi in all five annual grassland species. However, at high soil nitrogen contents, this trend was reversed in four of the five species.
Finally, in the study of Rillig and Allen (1998), several important observations were made with respect to the effects of elevated CO2 and soil nitrogen status on fungal-plant interactions. First, after growing three-year-old shrubs at an atmospheric CO2 concentration of 750 ppm for four months, they reported insignificant 19 and 9 percent increases in percent root infected by arbuscular mycorrhizal fungi at low and high soil nitrogen concentrations, respectively. However, elevated CO2 significantly increased the percent root infection by arbuscules, which are the main structures involved in the symbiotic exchange of carbon and nutrients between a host plant and its associated fungi, by more than 14-fold at low soil nitrogen concentrations. In addition, the length of fungal hyphae more than doubled with atmospheric CO2 enrichment in the low soil nitrogen regime. In the high soil nitrogen treatment, elevated CO2 increased the percent root infection by vesicles, which are organs used by arbuscular mycorrhizal fungi for carbon storage, by approximately 2.5-fold.
In conclusion, these observations suggest that elevated CO2 will indeed affect fungal-plant interactions in positive ways that often depend upon soil nitrogen status. Typically, it appears that CO2-induced stimulations of percent root infection by various fungal components is greater under lower, rather than higher, soil nitrogen concentrations. This tendency implies that elevated CO2 will enhance fungal-plant interactions to a greater extent when soil nutrition is less-than-optimal for plant growth, which is the common case for most of earth’s ecosystems that are not subjected to cultural fertilization practices typical of intensive agricultural production.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenfungi.php.
Grasses
Perennial ryegrass (Lolium perenne L.) has been used as a model species in many experiments to help elucidate grassland responses to atmospheric CO2 enrichment and soil nitrogen availability. In the FACE study of Rogers et al. (1998), for example, plants exposed to 600 ppm CO2 exhibited a 35 percent increase in their photosynthetic rates without regard to soil nitrogen availability. However, when ryegrass was grown in plastic ventilated tunnels at twice-ambient concentrations of atmospheric CO2, the CO2-induced photosynthetic response was about 3-fold greater in a higher, as opposed to a lower, soil nitrogen regime (Casella and Soussana, 1997). Similarly, in an open-top chamber study conducted by Davey et al. (1999), it was reported that an atmospheric CO2 concentration of 700 ppm stimulated photosynthesis by 30 percent in this species when it was grown with moderate, but not low, soil nitrogen availability. Thus, CO2-induced photosynthetic stimulations in perennial ryegrass can be influenced by soil nitrogen content, with greater positive responses typically occurring under higher, as opposed to lower, soil nitrogen availability.
With respect to biomass production, van Ginkel and Gorissen (1998) reported that a doubling of the atmospheric CO2 concentration increased shoot biomass of perennial ryegrass by 28 percent, regardless of soil nitrogen concentration. In the more revealing six-year FACE study of Daepp et al. (2000), plants grown at 600 ppm CO2 and high soil nitrogen availability continually increased their dry matter production over that observed in ambient-treatment plots, from 8 percent more in the first year to 25 percent more at the close of year six. When grown at a low soil nitrogen availability, however, CO2-enriched plants exhibited an initial 5 percent increase in dry matter production, which dropped to a negative 11 percent in year two; but this negative trend was thereafter turned around, and it continually rose to reach a 9 percent stimulation at the end of the study. Thus, these data demonstrate that elevated CO2 increases perennial ryegrass biomass, even under conditions of low soil nitrogen availability, especially under conditions of long-term atmospheric CO2 enrichment.
Lutze et al. (1998) reported that microcosms of the C3 grass Danthonia richardsonii grown for four years in glasshouses fumigated with air containing 720 ppm CO2 displayed total photosynthetic carbon gains that were 15-34 percent higher than those of ambiently grown microcosms, depending on the soil nitrogen concentration. In a clearer depiction of photosynthetic responses to soil nitrogen, Davey et al. (1999) noted that photosynthetic rates of Agrostis capillaries subjected to twice-ambient levels of atmospheric CO2 for two years were 12 and 38 percent greater than rates measured in control plants grown at 350 ppm CO2 under high and low soil nitrogen regimes, respectively. They also reported CO2-induced photosynthetic stimulations of 25 and 74 percent for Trifolium repens subjected to high and low soil nitrogen regimes, respectively. Thus, we see that the greatest CO2-induced percentage increase in photosynthesis can sometimes occur under the least favorable soil nitrogen conditions.
With respect to biomass production, Navas et al. (1999) reported that 60 days’ exposure to 712 ppm CO2 increased biomass production of Danthonia richardsonii, Phalaris aquatica, Lotus pedunculatus, and Trifolium repens across a large soil nitrogen gradient. With slightly more detail, Cotrufo and Gorissen (1997) reported average CO2-induced increases in whole-plant dry weights of Agrostis capillaries and Festuca ovina that were 20 percent greater than those of their respective controls, regardless of soil nitrogen availability. In the study of Ghannoum and Conroy (1998), three Panicum grasses grown for two months at twice-ambient levels of atmospheric CO2 and high soil nitrogen availability displayed similar increases in total plant dry mass that were about 28 percent greater than those of their respective ambiently grown controls. At low nitrogen, however, elevated CO2 had no significant effect on the dry mass of two of the species, while it actually decreased that of the third species.
In summary, it is clear that atmospheric CO2 enrichment stimulates photosynthesis and biomass production in grasses and grassland species when soil nitrogen availability is high and/or moderate. Under lower soil nitrogen conditions, it is also clear that atmospheric CO2 enrichment can have the same positive effect on these parameters, but that it can also have a reduced positive effect, no effect, or (in one case) a negative effect. In light of the one long-term study that lasted six years, however, it is likely that—given enough time—grasslands have the ability to overcome soil nitrogen limitations and produce positive CO2-induced growth responses. Thus, because the rising CO2 content of the air is likely to continue for a long time to come, occasional nitrogen limitations on the aerial fertilization effect of atmospheric CO2 enrichment of grasslands will likely become less and less restrictive as time progresses.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogengrass.php.
Trees
Aspen
Does a deficiency of soil nitrogen lessen the relative growth stimulation of quaking aspen (Populus tremuloides Michx) that is typically provided by elevated concentrations of atmospheric CO2?
In exploring this question, Kubiske et al. (1998) grew cuttings of four quaking aspen genotypes for five months at CO2 concentrations of 380 or 720 ppm and low or high soil nitrogen in open-top chambers in the field in Michigan, USA. They found that the elevated CO2 treatment significantly increased net photosynthesis, regardless of soil nitrogen content, although there were no discernible increases in above-ground growth within the five-month study period. Belowground, however, elevated CO2 significantly increased fine root production, but only in the high soil nitrogen treatment.
Working at the same site, Zak et al. (2000) and Curtis et al. (2000) grew six aspen genotypes from cuttings in open-top chambers for 2.5 growing seasons at atmospheric CO2 concentrations of 350 and 700 ppm on soils containing either adequate or inadequate supplies of nitrogen. Curtis et al. report that at the end of this period the trees growing in the doubled-CO2 treatment exhibited rates of net photosynthesis that were 128 percent and 31 percent greater than those of the trees growing in the ambient-air treatment on the high- and low-nitrogen soils, respectively, while Zak et al. determined the CO2-induced biomass increases of the trees in the high- and low-nitrogen soils to be 38 percent and 16 percent, respectively.
In yet another study from the Michigan site, Mikan et al. (2000) grew aspen cuttings for two years in open-top chambers receiving atmospheric CO2 concentrations of 367 and 715 ppm in soils of low and high soil nitrogen concentrations. They report finding that elevated CO2 increased the total biomass of the aspen cuttings by 50 percent and 26 percent in the high and low soil nitrogen treatments, respectively, and that it increased coarse root biomass by 78 percent and 24 percent in the same respective treatments.
Last, but again at the same site, Wang and Curtis (2001) grew cuttings of two male and two female aspen trees for about five months in open-top chambers maintained at atmospheric CO2 concentrations of 380 and 765 ppm on soils of high and low nitrogen content. In the male cuttings, there was a modest difference in the CO2-induced increase in total biomass (58 percent and 66 percent in the high- and low-nitrogen soils, respectively), while in the female cuttings the difference was much greater (82 percent and 22 percent in the same respective treatments).
Considering the totality of these several observations, it would appear that the degree of soil nitrogen availability does indeed impact the aerial fertilization effect of atmospheric CO2 enrichment on the growth of aspen trees by promoting a greater CO2-induced growth enhancement in soils of adequate, as opposed to insufficient, nitrogen content.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenaspen.php.
Pine
In a review of eleven of their previously published papers dealing with both loblolly pine (Pinus taeda L.) and ponderosa pine (Pinus ponderosa Dougl.), Johnson et al. (1998) report that when soil nitrogen levels were so low as to be extremely deficient, or so high as to be toxic, growth responses to atmospheric CO2 enrichment in both species were negligible. For moderate soil nitrogen deficiencies, however, a doubling of the air’s CO2 content sometimes boosted growth by as much as 1,000 percent. In addition, atmospheric CO2 enrichment mitigated the negative growth response of ponderosa pine to extremely high soil nitrogen concentrations.
In a second paper published by some of the same scientists in the same year, Walker et al. (1998) describe how they raised ponderosa pine tree seedlings for two growing seasons in open-top chambers having CO2 concentrations of 350, 525 and 700 ppm on soils of low, medium and high nitrogen content. They report that elevated CO2 had little effect on most growth parameters after the first growing season, the one exception being belowground biomass, which increased with both CO2 and soil nitrogen. After two growing seasons, however, elevated CO2 significantly increased all growth parameters, including tree height, stem diameter, shoot weight, stem volume and root volume, with the greatest responses typically occurring at the highest CO2 concentration in the highest soil nitrogen treatment. Root volume at 700 ppm CO2 and high soil nitrogen, for example, exceeded that of all other treatments by at least 45 percent, as did shoot volume by 42 percent. Similarly, at high CO2 and soil nitrogen, coarse root and shoot weights exceeded those at ambient CO2 and high nitrogen by 80 and 88 percent, respectively.
Walker et al. (2000) published another paper on the same trees and treatments after five years of growth. At this time, the trees exposed to the twice-ambient levels of atmospheric CO2 had heights that were 43, 64 and 25 percent greater than those of the trees exposed to ambient air and conditions of high, medium and low levels of soil nitrogen, respectively. Similarly, the trunk diameters of the 700-ppm-trees were 24, 73 and 20 percent greater than the trunk diameters of the ambiently grown trees exposed to high, medium and low levels of soil nitrogen.
Switching to a different species, Entry et al. (1998) grew one-year-old longleaf pine seedlings for 20 months in pots of high and low soil nitrogen content within open-top chambers maintained at atmospheric CO2 concentrations of 365 or 720 ppm, finding that the elevated CO2 caused no overall change in whole-plant biomass at low soil nitrogen, but that at high soil nitrogen, it increased it by 42 percent. After two years of these treatments, Runion et al. (1999) also reported that rates of net photosynthesis were about 50 percent greater in the high CO2 treatment, irrespective of soil nitrogen content … and water content too.
Last, Finzi and Schlesinger (2003) measured and analyzed the pool sizes and fluxes of inorganic and organic nitrogen (N) in the floor and top 30 cm of mineral soil of the Duke Forest at the five-year point of a long-term FACE study, where half of the experimental plots are enriched with an extra 200 ppm of CO2. In commencing this study, they had originally hypothesized that “the increase in carbon fluxes to the microbial community under elevated CO2 would increase the rate of N immobilization over mineralization,” leading to a decline in the significant CO2-induced stimulation of forest net primary production that developed over the first two years of the experiment (DeLucia et al., 1999; Hamilton et al., 2002). Quite to the contrary, however, they discovered “there was no statistically significant change in the cycling rate of N derived from soil organic matter under elevated CO2.” Neither was the rate of net N mineralization significantly altered by elevated CO2, nor was there any statistically significant difference in the concentration or net flux of organic and inorganic N in the forest floor and top 30-cm of mineral soil after 5 years of CO2 fumigation. Hence, at this stage of the study, they could find no support for their original hypothesis, which suggests that the growth stimulation provided by elevated levels of atmospheric CO2 would gradually dwindle away to something rather insignificant before the stand reached its equilibrium biomass, although they continue to cling to this unsubstantiated belief.
Considering the totality of these several observations, it would appear that the degree of soil nitrogen availability impacts the effect of atmospheric CO2 enrichment on the growth of pine trees, with greater CO2-induced growth enhancement occurring in soils of adequate, as opposed to insufficient, nitrogen content. As in the case of aspen, however, there is evidence to suggest that at some point the response to increasing soil nitrogen saturates, and beyond that point, higher N concentrations may sometimes even reduce the forest growth response to elevated CO2.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenpine.php.
Spruce
Egli et al. (1998) rooted saplings of different genotypes of Norway spruce (Picea abies L. Karst.) directly into calcareous or acidic soils in open-top chambers and exposed them to atmospheric CO2 concentrations of 370 or 570 ppm and low or high soil nitrogen contents. They found that elevated CO2 generally stimulated light-saturated rates of photosynthesis under all conditions by as much as 35 percent, regardless of genotype, which consistently led to increased above-ground biomass production, also regardless of genotype, as well as without respect to soil type or nitrogen content.
Murray et al. (2000) grew Sitka spruce (Picea sitchensis (Bong.) Carr.) seedlings for two years in pots within open-top chambers maintained at atmospheric CO2 concentrations of 355 and 700 ppm. In the last year of the study, half of the seedlings received one-tenth of the optimal soil nitrogen supply recommended for this species, while the other half received twice the optimal amount. Under this protocol, the extra CO2 increased the seedlings’ light-saturated rates of net photosynthesis by 19 percent and 33 percent in the low- and high-nitrogen treatments, respectively, while it increased their total biomass by 0 percent and 37 percent in these same treatments. Nevertheless, Murray et al. note there was a reallocation of biomass from above-ground organs (leaves and stems) into roots in the low-nitrogen treatment; and they remark that this phenomenon “may provide a long-term mechanism by which Sitka spruce could utilize limited resources both more efficiently and effectively,” which suggests that although low soil nitrogen precluded a short-term CO2-induced growth response in this tree species, it is possible that the negative impact of nitrogen deficiency could be overcome in the course of much longer-term atmospheric CO2 enrichment.
In a related experiment, Liu et al. (2002) grew Sitka spruce seedlings in well-watered and fertilized pots within open-top chambers that were maintained for three years at atmospheric CO2 concentrations of either 350 or 700 ppm, after which the seedlings were planted directly into native nutrient-deficient forest soil and maintained at the same atmospheric CO2 concentrations for two more years in larger open-top chambers either with or without extra nitrogen being supplied to the soil. After the first three years of the study, they determined that the CO2-enriched trees possessed 11.6 percent more total biomass than the ambient-treatment trees. At the end of the next two years, however, the CO2-enriched trees supplied with extra nitrogen had 15.6 percent more total biomass than their similarly treated ambient-air counterparts, while the CO2-enriched trees receiving no extra nitrogen had 20.5 percent more biomass than their ambient-treatment counterparts.
In light of these several observations, it would appear that the degree of soil nitrogen availability affects the growth of spruce trees by promoting a greater CO2-induced growth enhancement in soils of adequate, as opposed to insufficient, nitrogen content. As in the cases of aspen and pine, however, at some point the response of spruce trees to increasing soil nitrogen saturates, and even higher nitrogen concentrations may reduce the growth response to elevated CO2 below that observed at optimal or low soil nitrogen concentrations.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/n/nitrogenspruce.php.
Other
Maillard et al. (2001) grew pedunculate oak seedlings for three to four months in greenhouses maintained at atmospheric CO2 concentrations of either 350 or 700 ppm under conditions of either low or high soil nitrogen concentration. The elevated CO2 of their study stimulated belowground growth in the seedlings growing in the nitrogen-poor soil, significantly increasing their root-to-shoot ratios. However, it increased both the below- and above-ground biomass of seedlings growing in nitrogen-rich soil. In fact, the CO2-enriched seedlings growing in the nitrogen-rich soil produced 217 and 533 percent more stem and coarse-root biomass, respectively, than their ambient-air counterparts growing in the same fertility treatment. Overall, the doubled CO2 concentration of the air in their study enhanced total seedling biomass by approximately 30 and 140 percent under nitrogen-poor and nitrogen-rich soil conditions, respectively.
Schortemeyer et al. (1999) grew seedlings of Acacia melanoxylon (a leguminous nitrogen-fixing tree native to south-eastern Australia) in hydroponic culture for six weeks in growth cabinets, where the air was maintained at CO2 concentrations of either 350 or 700 ppm and the seedlings were supplied with water containing nitrogen in a number of discrete concentrations ranging from 3 to 6,400 mmol m-3. In the two lowest of these nitrogen concentration treatments, final biomass was unaffected by atmospheric CO2 enrichment; but, as in the study of Maillard et al., it was increased by 5- to 10-fold at the highest nitrogen concentration.
Temperton et al. (2003) measured total biomass production in another N2-fixing tree—Alnus glutinosa (the common alder)—seedlings of which had been grown for three years in open-top chambers in either ambient or elevated (ambient + 350 ppm) concentrations of atmospheric CO2 and one of two soil nitrogen regimes (full nutrient solution or no fertilizer). In their study, by contrast, they found that the trees growing under low soil nutrient conditions exhibited essentially the same growth enhancement as that of the well-fertilized trees.
Rounding out the full gamut of growth responses, 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. They found that their doubling of the air’s CO2 concentration increased total seedling biomass by 134 percent in the low nitrogen treatment but by a smaller 98 percent in the high nitrogen treatment. In addition, the elevated CO2 led to greater root growth in the low nitrogen treatment, as indicated by a 33 percent higher root:shoot ratio.
In conclusion, different species of trees respond differently to atmospheric CO2 enrichment under conditions of low vs. high soil nitrogen fertility. The most common response is for the growth-promoting effects of atmospheric CO2 enrichment to be expressed to a greater degree when soil nitrogen fertility is optimal as opposed to less-than-optimal.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/o/ozonetreemisc.php.
High Salinity
In managed agricultural ecosystems, the buildup of soil salinity from repeated irrigations can sometimes reduce crop yields. Similarly, in natural ecosystems where exposure to brackish or salty water is commonplace, saline soils can induce growth stress in plants not normally adapted to coping with this problem. Thus, it is important to understand how rising atmospheric CO2 concentrations may interact with soil salinity to affect plant growth.
In the study of Ball et al. (1997), it was found that two Australian mangrove species with differing tolerance to salinity exhibited increased rates of net photosynthesis in response to a doubling of the atmospheric CO2 concentration, but only when exposed to salinity levels that were 25 percent, but not 75 percent, of full-strength seawater.
Mavrogianopoulos et al. (1999) reported that atmospheric CO2 concentrations of 800 and 1200 ppm stimulated photosynthesis in parnon melons by 75 and 120 percent, respectively, regardless of soil salinity, which ranged from 0 to 50 mM NaCl. Moreover, the authors noted that atmospheric CO2 enrichment partially alleviated the negative effects of salinity on melon yield, which increased with elevated CO2 at all salinity levels.
Maggio et al. (2002) grew tomatos at 400 and 900 ppm in combination with varying degrees of soil salinity and noted that plants grown in elevated CO2 tolerated an average root-zone salinity threshold value that was about 60 percent greater than that exhibited by plants grown at 400 ppm CO2 (51 vs. 32 mmol dm-3 Cl).
The review of Poorter and Perez-Soba (2001) found no changes in the effect of elevated CO2 on the growth responses of most plants over a wide range of soil salinities, in harmony with the earlier findings of Idso and Idso (1994).
These various studies suggest that elevated CO2 concentrations have either positive or no effects on plan growth where mild to moderate stresses may be present due to high soil salinity levels. Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/subject/s/salinity stress. php.
Elevated Temperature
Will plants continue to exhibit CO2-induced growth increases under conditions of elevated air temperature? In this section, we review the photosynthetic and growth responses of agricultural crops, grasslands and woody species to answer this question.
Agricultural Crops
The optimum growth temperature for several plants has been shown to rise substantially with increasing levels of atmospheric CO2 (McMurtrie and Wang, 1993; McMurtrie et al., 1992; Stuhlfauth and Fock, 1990; Berry and Bjorkman, 1980). This phenomenon was predicted by Long (1991), who calculated from well-established plant physiological principles that most C3 plants should increase their optimum growth temperature by approximately 5°C for a 300 ppm increase in the air’s CO2 content. One would thus also expect plant photosynthetic rates to rise with concomitant increases in the air’s CO2 concentration and temperature, as has indeed been previously shown to be true by Idso and Idso (1994). We here proceed to see if these positive CO2 and temperature interactions are still being supported in the recent scientific literature.
In the study of Zhu et al. (1999), pineapples grown at 700 ppm CO2 assimilated 15, 97 and 84 percent more total carbon than pineapples grown at the current ambient CO2 concentration in day/night air temperature regimes of 30/20 (which is optimal for pineapple growth at ambient CO2), 30/25, and 35/25 °C, respectively. Similarly, Taub et al. (2000) demonstrated that net photosynthetic rates of cucumbers grown at twice-ambient levels of atmospheric CO2 and air temperatures of 40°C were 3.2 times greater than those displayed by control plants grown at ambient CO2 and this same elevated air temperature. Thus, at air temperatures normally considered to be deleterious to plant growth, rates of photosynthesis are typically considerably greater for CO2 enriched vs. ambiently grown plants.
Reddy et al. (1999) grew cotton plants at air temperatures ranging from 2°C below to 7°C above ambient air temperatures and reported that plants simultaneously exposed to 720 ppm CO2 displayed photosynthetic rates that were 137 to 190 percent greater than those displayed by plants exposed to ambient CO2 concentrations across this temperature spectrum. Similarly, Cowling and Sage (1998) reported that a 200-ppm increase in the air’s CO2 concentration boosted photosynthetic rates of young bean plants by 58 and 73 percent at growth temperatures of 25 and 36°C, respectively. In addition, Bunce (1998) grew wheat and barley at 350 and 700 ppm CO2 across a wide range of temperatures and reported that elevated CO2 stimulated photosynthesis in these species by 63 and 74 percent, respectively, at an air temperature of 10°C and by 115 and 125 percent at 30°C. Thus, the percentage increase in photosynthetic rate resulting from atmospheric CO2 enrichment often increases substantially with increasing air temperature.
Elevated CO2 often aids in the recovery of plants from high temperature-induced reductions in photosynthetic capacity, as noted by Ferris et al. (1998), who grew soybeans for 52 days under normal air temperature and soil water conditions at atmospheric CO2 concentrations of 360 and 700 ppm, but then subjected them to an 8-day period of high temperature and water stress. After normal air temperature and soil water conditions were restored, the CO2-enriched plants attained photosynthetic rates that were 72 percent of their unstressed controls, while stressed plants grown at ambient CO2 attained photosynthetic rates that were only 52 percent of their respective controls.
CO2-induced increases in plant growth under high air temperatures have also been observed in a number of other agricultural species. In the previously mentioned study of Cowling and Sage (1998), for example, the 200-ppm increase in the air’s CO2 content boosted total plant biomass for wheat and barley by a combined average of 59 and 200 percent at air temperatures of 25 and 36°C. Similarly, Ziska (1998) reported that a doubling of the atmospheric CO2 concentration increased the total dry weight of soybeans by 36 and 42 percent at root zone temperatures of 25 and 30°C, respectively. Likewise, Hakala (1998) noted that spring wheat grown at 700 ppm CO2 attained total biomass values that were 17 and 23 percent greater than those attained by ambiently grown plants exposed to ambient and elevated (ambient plus 3°C) air temperatures. In addition, after inputting various observed CO2-induced growth responses of winter wheat into plant growth models, Alexandrov and Hoogenboom (2000) predicted 12 to 49 percent increases in wheat yield in Bulgaria even if air temperatures rise by as much as 4°C. Finally, in the study of Reddy et al. (1998), it was shown that elevated CO2 (700 ppm) increased total cotton biomass by 31 to 78 percent across an air temperature range from 20 to 40°C. Thus, the beneficial effects of elevated CO2 on agricultural crop yield is often enhanced by elevated air temperature.
In some cases, however, elevated CO2 does not interact with air temperature to further increase the growth-promoting effects of atmospheric CO2 enrichment, but simply allows the maintenance of the status quo. In the study of Demmers-Derks et al. (1998), for example, sugar beets grown at 700 ppm CO2 attained 25 percent more biomass than ambiently grown plants, regardless of air temperature, which was increased by 3°C. Similarly, in the study of Fritschi et al. (1999), elevated CO2 concentrations did not significantly interact with air temperature (4.5°C above ambient) to impact the growth of rhizoma peanut. Nonetheless, the 300-ppm increase in the air’s CO2 content increased total biomass by 52 percent, regardless of air temperature.
Finally, even if the air’s CO2 content were to cease rising or have no effect on plants, it is possible that temperature increases alone would promote plant growth and development. This was the case in the study of Wurr et al. (2000), where elevated CO2 had essentially no effect on the yield of French bean. However, a 4°C increase in air temperature increased yield by approximately 50 percent.
In conclusion, the recent scientific literature continues to indicate that as the air’s CO2 content rises, agricultural crops will likely exhibit enhanced rates of photosynthesis and biomass production that will not be diminished by any global warming that might occur concurrently. In fact, if the ambient air temperature rises, the growth-promoting effects of atmospheric CO2 enrichment will likely rise along with it.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/tempco2ag.php.
Grassland Species
In the study of Lilley et al. (2001), swards of Trifolium subterraneum were grown at 380 and 690 ppm CO2 in combination with simultaneous exposure to ambient and elevated (ambient plus 3.4°C) air temperature. After one year of treatment, they reported that elevated CO2 increased foliage growth by 19 percent at ambient air temperature. At elevated air temperature, however, plants grown at ambient CO2 exhibited a 28 percent reduction in foliage growth, while CO2-enriched plants still displayed a growth enhancement of 8 percent. Similarly, Morgan et al. (2001) reported that twice-ambient levels of atmospheric CO2 increased above-ground biomass in native shortgrass steppe ecosystems by an average of 38 percent, in spite of an average air temperature increase of 2.6°C. Likewise, when bahiagrass was grown across a temperature gradient of 4.5°C, Fritschi et al. (1999) reported that a 275 ppm increase in the air’s CO2 content boosted photosynthesis and above-ground biomass by 22 and 17 percent, respectively, independent of air temperature. Thus, at elevated air temperature, CO2-induced increases in rates of photosynthesis and biomass production are typically equal to or greater than what they are at ambient air temperature.
Other studies report similar results. Greer et al. (2000), for example, grew five pasture species at 18 and 28°C and reported that plants concomitantly exposed to 700 ppm CO2 displayed average photosynthetic rates that were 36 and 70 percent greater, respectively, than average rates exhibited by control plants subjected to ambient CO2 concentrations. Moreover, the average CO2-induced biomass increase for these five species rose dramatically with increasing air temperature: from only 8 percent at 18°C to 95 percent at 28°C. Thus, the beneficial effects of elevated CO2 on grassland productivity is often significantly enhanced by elevated air temperature.
Finally, temperature increases alone can promote grass growth and development. Norton et al. (1999) found elevated CO2 had essentially no effect on the growth of the perennial grass Agrostis curtisii after two years of fumigation; however, a 3°C increase in air temperature increased the growth of this species considerably.
In conclusion, grassland plants will likely exhibit enhanced rates of photosynthesis and biomass production as the air’s CO2 content rises that will not be diminished by any global warming that might occur concurrently. If the ambient air temperature rises, the growth-promoting effects of atmospheric CO2 enrichment will likely rise along with it.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/tempco2grass.php.
Trees
In the study of Kellomaki and Wang (2001), birch seedlings were grown at atmospheric CO2 concentrations of 350 and 700 ppm in combination with ambient and elevated (ambient plus 3°C) air temperatures. After five months of treatment, the authors reported that photosynthetic rates of CO2-enriched seedlings were 21 and 28 percent greater than those displayed by their ambiently grown counterparts at ambient and elevated air temperatures, respectfully. In another study, Carter et al. (2000) observed that a 300 ppm increase in the air’s CO2 content allowed leaves of sugar maple seedlings to remain green and non-chlorotic when exposed to air temperatures 3°C above ambient air temperature. On the other hand, seedlings fumigated with ambient air exhibited severe foliar chlorosis when exposed to the same elevated air temperatures. These results thus indicate that at elevated air temperatures, rates of photosynthesis are greater and foliar health is typically better in birch and sugar maples trees in CO2-enriched as opposed to ambient air.
Other studies report similar results. Sheu et al. (1999) grew a sub-tropical tree at day/night temperatures of 25/20°C (ambient) and 30/25°C (elevated) for six months and reported that seedlings exposed to 720 ppm CO2 displayed photosynthetic rates that were 20 and 40 percent higher, respectively, than that of their ambiently grown controls. In addition, the CO2-induced increases in total dry weight for this species were 14 and 49 percent, respectively, at ambient and elevated air temperatures. Likewise, Maherali et al. (2000) observed that a 5°C increase in ambient air temperature increased the CO2-induced biomass enhancement resulting from a 750 ppm CO2 enrichment of ponderosa pine seedlings from 42 to 62 percent. Wayne et al. (1998) reported that a 5°C increase in the optimal growth temperature of yellow birch seedlings fumigated with an extra 400 ppm CO2 increased the CO2-induced increase in biomass from 60 to 227 percent. The beneficial effects of elevated CO2 on tree species photosynthesis and growth can also be assessed during natural seasonal temperature changes, as documented by Hymus et al. (1999) for loblolly pine and Roden et al. (1999) for snow gum seedlings.
In some cases, however, there appear to be little interactive effects between elevated CO2 and temperature on photosynthesis and growth in tree species. When Tjoelker et al. (1998a), for example, grew seedlings of quaking aspen, paper birch, tamarack, black spruce and jack pine at atmospheric CO2 concentrations of 580 ppm, they reported average increases in photosynthetic rates of 28 percent, regardless of temperature, which varied from 18 to 30°C. After analyzing the CO2-induced increases in dry mass for these seedlings, Tjoelker et al. (1998b) further reported that dry mass values were about 50 and 20 percent greater for the deciduous and coniferous species, respectively, regardless of air temperature.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/tempco2trees.php.
Other
In a mechanistic model study of Mediterranean shrub vegetation, Osborne et al. (2000) reported that increased warming and reduced precipitation would likely decrease net primary production. However, when the same model was run at twice the ambient atmospheric CO2 concentration, it predicted a 25 percent increase in vegetative productivity, in spite of the increased warming and reduced precipitation. Although we tend to not review studies based on mechanistic models, it is also interesting to note that Bunce (2000) demonstrated that field-grown Taraxacum officinale plants exposed to 525 ppm CO2 and low air temperatures (between 15 and 25°C) displayed photosynthetic rates that were 10 to 30 percent greater than what was predicted by state-of-the-art biochemical models of photosynthesis for this range of temperatures. Thus, at both high and low air temperatures, elevated CO2 appears to be capable of significantly increasing the photosynthetic prowess of some plants.
In the real world, Stirling et al. (1998) grew five fast-growing native species at various atmospheric CO2 concentrations and air temperatures, finding that twice-ambient levels of atmospheric CO2 increased photosynthetic rates by 18-36 percent for all species regardless of air temperature, which was up to 3°C higher than ambient air temperature. In addition, atmospheric CO2 enrichment increased average plant biomass by 25 percent, also regardless of air temperature. Likewise, in a study of vascular plants from Antarctica, Xiong et al. (2000) reported that a 13°C rise in air temperature increased plant biomass by 2- to 3-fold. We can only imagine what the added benefit of atmospheric CO2 enrichment would do for these species.
Hamerlynck et al. (2000) demonstrated that the desert perennial shrub Larrea tridentata maintained more favorable midday leaf water potentials during a nine-day high-temperature treatment when fumigated with 700 ppm CO2, as compared to 350 ppm.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/tempco2growthres.php.
UV-B Radiation
Zhao et al. (2004) report that “as a result of stratospheric ozone depletion, UV-B radiation (280-320 nm) levels are still high at the Earth’s surface and are projected to increase in the near future (Madronich et al., 1998; McKenzie et al., 2003).” In reference to this potential development, they note that “increased levels of UV-B radiation are known to affect plant growth, development and physiological processes (Dai et al., 1992; Nogués et al., 1999),” stating that high UV-B levels often result in “inhibition of photosynthesis, degradation of protein and DNA, and increased oxidative stress (Jordan et al., 1992; Stapleton, 1992).” In light of the above observations, it is important to clarify how the ongoing rise in the air’s CO2 content might affect the deleterious effects of UV-B radiation on earth’s vegetation.
To investigate this question, Zhao et al. grew well watered and fertilized cotton plants in sunlit controlled environment chambers maintained at atmospheric CO2 concentrations of 360 or 720 ppm from emergence until three weeks past first-flower stage under three levels of UV-B radiation (0, 8 and 16 kJ m-2 d-1). On five dates between 21 and 62 days after emergence, they measured a number of plant physiological processes and parameters. Over the course of the experiment, the mean net photosynthetic rate of the upper-canopy leaves in the CO2-enriched chambers was increased—relative to that in the ambient-air chambers—by 38.3 percent in the low UV-B treatment (from 30.3 to 41.9 m m-2 s-1), 41.1 percent in the medium UV-B treatment (from 28.7 to 40.5 m m-2 s-1), and 51.5 percent in the high UV-B treatment (from 17.1 to 25.9 m m-2 s-1). In the medium UV-B treatment, the growth stimulation from the elevated CO2 was sufficient to raise net photosynthesis rates 33.7 percent above the rates experienced in the ambient air and no UV-B treatment (from 30.3 to 40.5 m m-2 s-1); but in the high UV-B treatment the radiation damage was so great that even with the help of the 51.5 percent increase in net photosynthesis provided by the doubled-CO2 air, the mean net photosynthesis rate of the cotton leaves was 14.5 percent less than that experienced in the ambient air and no UV-B treatment (dropping from 30.3 to 25.9 m m-2 s-1).
It should be noted that the medium UV-B treatment of this study was chosen to represent the intensity of UV-B radiation presently received on a clear summer day in the major cotton production region of Mississippi, USA, under current stratospheric ozone conditions, while the high UV-B treatment was chosen to represent what might be expected there following a 30 percent depletion of the ozone layer, which has been predicted to double the region’s reception of UV-B radiation from 8 to 16 kJ m-2 d-1. Consequently, a doubling of the current CO2 concentration and the current UV-B radiation level would reduce the net photosynthetic rate of cotton leaves by just under 10 percent (from 28.7 to 25.9 m m-2 s-1), whereas in the absence of a doubling of the air’s CO2 content, a doubling of the UV-B radiation level would reduce cotton net photosynthesis by just over 40 percent (from 28.7 to 17.1 m m-2 s-1).
Viewed in this light, it can be seen that a doubling the current atmospheric CO2 concentration would compensate for over three-fourths of the loss of cotton photosynthetic capacity caused by a doubling of the current UV-B radiation intensity. It may do better than that, for in the study of Zhao et al. (2003), it was reported that both Adamse and Britz (1992) and Rozema et al. (1997) found that doubled CO2 totally compensated for the negative effects of equally high UV-B radiation.
In another study (Qaderi and Reid, 2005), well watered and fertilized canola (Brassica napus L.) plants were grown from seed to maturity in pots within controlled environment chambers maintained at either 370 or 740 ppm CO2 with and without a daily dose of UV-B radiation in the amount of 4.2 kJ m-2, while a number of plant parameters were measured at various times throughout the growing season. With respect to the bottom-line result of final seed yield, this parameter was determined to be 0.98 g/plant in the control treatment (ambient CO2, with UV-B). Doubling the CO2 concentration increased yield by 25.5 percent to 1.23 g/plant. Alternatively, removing the UV-B radiation flux increased yield by 91.8 percent to 1.88 g/plant. Doing both (doubling the CO2 concentration while simultaneously removing the UV-B flux) increased final seed yield most of all, by 175.5 percent to 2.7 g/plant. Viewed from a different perspective, doubling the air’s CO2 concentration in the presence of the UV-B radiation flux enhanced final seed yield by 25.5 percent, while doubling CO2 in the absence of the UV-B radiation flux increased seed yield by 43.6 percent. In concluding their paper, the authors note that “previous studies have shown that elevated CO2 increases biomass and seed yield, whereas UV-B decreases them (Sullivan, 1997; Teramura et al., 1990).” Finding much the same thing in their study, they thus reckoned that “elevated CO2 may have a positive effect on plants by mitigating the detrimental effects caused by UV-B radiation.”
Two years later in a similar study of the same plant, Qaderi et al. (2007) grew well watered and fertilized canola plants from the 30-day-old stage until 25 days after anthesis in 1-L pots within controlled environment chambers exposed to either 4.2 kJ m-2 d-1 of UV-B radiation or no such radiation in air of either 370 or 740 ppm CO2, in order to determine the effects of these two parameters on the photosynthetic rates and water use efficiency of the maturing husks or siliquas that surround the plants’ seeds. Results indicated that for the plants exposed to 4.2 kJ m-2 d-1 of UV-B radiation, the experimental doubling of the air’s CO2 concentration led to a 29 percent increase in siliqua net photosynthesis, an 18 percent decrease in siliqua transpiration, and a 58 percent increase in siliqua water use efficiency; while for the plants exposed to no UV-B radiation, siliqua net photosynthesis was increased by a larger 38 percent, transpiration was decreased by a larger 22 percent and water use efficiency was increased by a larger 87 percent in the CO2-enriched air.
In another noteworthy study, Deckmyn et al. (2001) grew white clover plants for four months in four small greenhouses, two of which allowed 88 percent of the incoming UV-B radiation to pass through their roofs and walls and two of which allowed 82 percent to pass through, while one of the two greenhouses in each of the UV-B treatments was maintained at ambient CO2 (371 ppm) and the other at elevated CO2 (521 ppm). At the mid-season point of their study, they found that the 40 percent increase in atmospheric CO2 concentration stimulated the production of flowers in the low UV-B treatment by 22 percent and in the slightly higher UV-B treatment by 43 percent; while at the end of the season, the extra CO2 was determined to have provided no stimulation of biomass production in the low UV-B treatment, but it significantly stimulated biomass production by 16 percent in the high UV-B treatment.
The results of this study indicate that the positive effects of atmospheric CO2 enrichment on flower and biomass production in white clover are greater at more realistic or natural values of UV-B radiation than those found in many greenhouses. As a result, Deckmyn et al. say their results “clearly indicate the importance of using UV-B transmittant greenhouses or open-top chambers when conducting CO2 studies,” for if this is not done, their work suggests that the results obtained could significantly underestimate the magnitude of the benefits that are being continuously accrued by earth’s vegetation as a result of the ongoing rise in the air’s CO2 content.
In 2007, Koti et al. (2007) used Soil-Plant-Atmosphere-Research (SPAR) chambers at Mississippi State University (USA) to investigate the effects of doubled atmospheric CO2 concentration (720 vs. 360 ppm) on the growth and development of six well watered and fertilized soybean (Glycine max L.) genotypes grown from seed in pots filled with fine sand and exposed to the dual stresses of high day/night temperatures (38/30°C vs. 30/22°C) and high UV-B radiation levels (10 vs. 0 kJ/m2/day). Results led this group of authors to report that “elevated CO2 partially compensated [for] the damaging effects on vegetative growth and physiology caused by negative stressors such as high temperatures and enhanced UV-B radiation levels in soybean,” specifically noting, in this regard, CO2’s positive influence on the physiological parameters of plant height, leaf area, total biomass, net photosynthesis, total chlorophyll content, phenolic content and wax content, as well as relative plant injury.
In a study that did not include UV-B radiation as an experimental parameter, Estiarte et al. (1999) grew spring wheat in FACE plots in Arizona, USA, at atmospheric CO2 concentrations of 370 and 550 ppm and two levels of soil moisture (50 and 100 percent of potential evapotranspiration). They found that leaves of plants grown in elevated CO2 had 14 percent higher total flavonoid concentrations than those of plants grown in ambient air, and that soil water content did not affect the relationship. An important aspect of this finding is that one of the functions of flavonoids in plant leaves is to protect them against UV-B radiation. More studies of this nature should be conducted to see how general this beneficial response may be throughout the plant world.
In a study of UV-B and CO2 effects on a natural ecosystem, which was conducted at the Abisko Scientific Research Station in Swedish Lapland, Johnson et al. (2002) studied plots of subarctic heath composed of open canopies of downy birch and dense dwarf-shrub layers containing scattered herbs and grasses. For a period of five years, they exposed the plots to factorial combinations of UV-B radiation—ambient and that expected to result from a 15 percent stratospheric ozone depletion—and atmospheric CO2 concentration—ambient (around 365 ppm) and enriched (around 600 ppm)—after which they determined the amounts of microbial carbon (Cmic) and nitrogen (Nmic) in the soils of the plots.
When the plots were exposed to the enhanced UV-B radiation, the amount of Cmic in the soil was reduced to only 37 percent of what it was at the ambient UV-B level when the air’s CO2 content was maintained at the ambient concentration. When the UV-B increase was accompanied by the CO2 increase, however, not only was there not a decrease in Cmic, there was an actual increase of 37 percent. The amount of Nmic in the soil experienced a 69 percent increase when the air’s CO2 content was maintained at the ambient concentration; and when the UV-B increase was accompanied by the CO2 increase, Nmic rose even more, by 138 percent.
These findings, in the words of Johnson et al., “may have far-reaching implications … because the productivity of many semi-natural ecosystems is limited by N (Ellenberg, 1988).” The 138 percent increase in soil microbial N observed in this study to accompany a 15 percent reduction in stratospheric ozone and a 64 percent increase in atmospheric CO2 concentration (experienced in going from 365 ppm to 600 ppm) should significantly enhance the input of plant litter to the soils of these ecosystems, which phenomenon represents the first half of the carbon sequestration process, i.e., the carbon input stage. With respect to the second stage of keeping as much of that carbon as possible in the soil, Johnson et al. note that “the capacity for subarctic semi-natural heaths to act as major sinks for fossil fuel-derived carbon dioxide is [also] likely to be critically dependent on the supply of N,” as is indeed indicated to be the case in the literature review of Berg and Matzner (1997), who report that with more nitrogen in the soil, the long-term storage of carbon is significantly enhanced, as more litter is chemically transformed into humic substances when nitrogen is more readily available, and these more recalcitrant carbon compounds can be successfully stored in the soil for many millennia.
In light of these several findings, we conclude that the ongoing rise in the air’s CO2 content is a powerful antidote for the deleterious biological impacts that might possibly be caused by an increase in the flux of UV-B radiation at the surface of the earth due to any further depletion of the planet’s stratospheric ozone layer.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/u/uvbradiation.php.
Water Stress
As the CO2 content of the air continues to rise, nearly all of earth’s plants will exhibit increases in photosynthesis and biomass production. However, some experts claim that water stress will negate these benefits. In reviewing the scientific literature of the ten-year period 1983-1994, however, Idso and Idso (1994) found that water stress typically will not negate the CO2-induced stimulation of plant productivity. They found that the CO2-induced percentage increase in plant biomass production was often greater under water-stressed conditions than it was when plants were well-watered. We here review some more recent scientific literature in this area for agricultural, grassland and woody plant species.
Agricultural Species
During times of water stress, atmospheric CO2 enrichment often stimulates plants to develop larger-than-usual and more robust root systems to probe greater volumes of soil for scarce and much-needed moisture. Wechsung et al. (1999), for example, observed a 70 percent increase in lateral root dry weights of water-stressed wheat grown at 550 ppm CO2, while De Luis et al. (1999) reported a 269 percent increase in root-to-shoot ratio of water-stressed alfalfa growing at 700 ppm CO2. Thus, elevated CO2 elicits stronger-than-usual positive root responses in agricultural species under conditions of water stress.
Elevated levels of atmospheric CO2 also tend to reduce the openness of stomatal pores on leaves, thus decreasing plant stomatal conductance. This phenomenon, in turn, reduces the amount of water lost to the atmosphere by transpiration and, consequently, lowers overall plant water use. Serraj et al. (1999) report that water-stressed soybeans grown at 700 ppm CO2 reduced their total seasonal water loss by 10 percent relative to that of water-stressed control plants grown at 360 ppm CO2. In addition, Conley et al. (2001) noted that a 200-ppm increase in the air’s CO2 concentration reduced cumulative evapotranspiration in water-stressed sorghum by approximately 4 percent. Atmospheric CO2 enrichment thus increases plant water acquisition, by stimulating root growth, while it reduces plant water loss, by constricting stomatal apertures; and these dual effects typically enhance plant water-use efficiency, even under conditions of less-than-optimal soil water content. But these phenomena have other implications as well.
CO2-induced increases in root development together with CO2-induced reductions in stomatal conductance often contribute to the maintenance of a more favorable plant water status during times of drought. Sgherri et al. (1998) reported that leaf water potential, which is a good indicator of overall plant water status, was 30 percent higher (less negative and therefore more favorable) in water-stressed alfalfa grown at an atmospheric CO2 concentration of 600 ppm CO2 versus 340 ppm CO2. Wall (2001) reports that leaf water potentials were similar in CO2-enriched water-stressed plants and ambiently grown well-watered control plants, which implies a complete CO2-induced amelioration of water stress in the CO2-enriched plants. Similarly, Lin and Wang (2002) demonstrated that elevated CO2 caused a several-day delay in the onset of the water stress-induced production of the highly reactive oxygenated compound H2O2 in spring wheat.
If atmospheric CO2 enrichment thus allows plants to maintain a better water status during times of water stress, it is only logical to expect that such plants should exhibit greater rates of photosynthesis than ambiently grown plants. And so they do. With the onset of water stress in Brassica juncea, for example, photosynthetic rates dropped by 40 percent in plants growing in ambient air, while plants growing in air containing 600 ppm CO2 only experienced a 30 percent reduction in net photosynthesis (Rabha and Uprety, 1998). Ferris et al. (1998) reported that after imposing water-stress conditions on soybeans and allowing them to recover following complete rewetting of the soil, plants grown in air containing 700 ppm CO2 reached pre-stressed rates of photosynthesis after six days, while plants grown in ambient air never recovered to pre-stressed rates.
Reasoning analogously, it is also to be expected that plant biomass production would be enhanced by elevated CO2 concentrations under drought conditions. In exploring this idea, Ferris et al. (1999) reported that water-stressed soybeans grown at 700 ppm CO2 attained seed yields that were 24 percent greater than those of similarly water-stressed plants grown at ambient CO2 concentrations, while Hudak et al. (1999) reported that water-stress had no effect on yield in CO2-enriched spring wheat.
In some cases, the CO2-induced percentage biomass increase is actually greater for water-stressed plants than it is for well-watered plants. Li et al. (2000), for example, reported that a 180-ppm increase in the air’s CO2 content increased lower stem grain weights in water-stressed and well-watered spring wheat by 24 and 14 percent, respectively. Similarly, spring wheat grown in air containing an additional 280 ppm CO2 exhibited 57 and 40 percent increases in grain yield under water-stressed and well-watered conditions, respectively (Schutz and Fangmeier, 2001). Likewise, Ottman et al. (2001) noted that elevated CO2 increased plant biomass in water-stressed sorghum by 15 percent, while no biomass increase occurred in well-watered sorghum.
In summary, the conclusions of Idso and Idso (1994) are well supported by the recent peer-reviewed scientific literature, which indicates that the ongoing rise in the air’s CO2 content will likely lead to substantial increases in plant photosynthetic rates and biomass production, even in the face of stressful conditions imposed by less-than-optimum soil moisture conditions.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/growthwaterag.php.
Grassland Species
In the study of Leymarie et al. (1999), twice-ambient levels of atmospheric CO2 caused significant reductions in the stomatal conductance of water-stressed Arabidopsis thaliana. Similarly, Volk et al. (2000) reported that calcareous grassland species exposed to elevated CO2 concentrations (600 ppm) consistently exhibited reduced stomatal conductance, regardless of soil moisture availability. Thus, atmospheric CO2 enrichment clearly reduces stomatal conductance and plant transpiration and soil water depletion in grassland ecosystems.
In the case of four grassland species comprising a pasture characteristic of New Zealand, Clark et al. (1999) found that leaf water potential, which is a good indicator of plant water status, was consistently higher (less negative and, therefore, less stressful) under elevated atmospheric CO2 concentrations. Similarly, leaf water potentials of the water-stressed C4 grass Panicum coloratum grown at 1000 ppm CO2 were always higher than those of their water-stressed counterparts growing in ambient air (Seneweera et al., 2001). Indeed, Seneweera et al. (1998) reported that leaf water potentials observed in CO2-enriched water-stressed plants were an amazing three-and-a-half times greater than those observed in control plants grown at 350 ppm during drought conditions (Seneweera et al., 1998).
If atmospheric CO2 enrichment thus allows plants to maintain improved water status during times of water stress, it is only logical to expect that such plants will exhibit greater photosynthetic rates than similar plants growing in ambient air. In a severe test of this concept, Ward et al. (1999) found that extreme water stress caused 93 and 85 percent reductions in the photosynthetic rates of two CO2-enriched grassland species; yet their rates of carbon fixation were still greater than those observed under ambient CO2 conditions.
In view of the fact that elevated CO2 enhances photosynthetic rates during times of water stress, one would expect that plant biomass production would also be enhanced by elevated CO2 concentrations under drought conditions. And so it is. On the American prairie, for example, Owensby et al. (1999) reported that tallgrass ecosystems exposed to twice-ambient concentrations of atmospheric CO2 for eight years only exhibited significant increases in above- and below-ground biomass during years of less-than-average rainfall. Also, in the study of Derner et al. (2001), the authors reported that a 150-ppm increase in the CO2 content of the air increased shoot biomass in two C4 grasses by 57 percent, regardless of soil water content. Seneweera et al. (2001) reported that a 640-ppm increase in the air’s CO2 content increased shoot dry mass in a C4 grass by 44 and 70 percent under well-watered and water-stressed conditions, respectively. Likewise, Volk et al. (2000) grew calcareous grassland assemblages at 360 and 600 ppm CO2 and documented 18 and 40 percent CO2-induced increases in whole-community biomass under well-watered and water-stressed conditions, respectively.
In summary, the peer-reviewed scientific literature indicates that the ongoing rise in the air’s CO2 content will likely lead to substantial increases in plant photosynthetic rates and biomass production for grassland species even in the face of stressful environmental conditions imposed by less-than-optimum soil moisture contents.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/growthwatergrass.php.
Woody Species
During times of water stress, atmospheric CO2 enrichment often stimulates the development of larger-than-usual and more robust root systems in woody perennial species, which allows them to probe greater volumes of soil for scarce and much-needed moisture. Tomlinson and Anderson (1998), for example, report that greater root development in water-stressed red oak seedlings grown at 700 ppm CO2 helped them effectively deal with the reduced availability of moisture. These trees eventually produced just as much biomass as well-watered controls exposed to ambient air containing 400 ppm CO2. In addition, Polley et al. (1999) note that water-stressed honey mesquite trees subjected to an atmospheric CO2 concentration of 700 ppm produced 37 percent more root biomass than water-stressed control seedlings growing at 370 ppm.
Elevated levels of atmospheric CO2 also tend to reduce the area of open stomatal pore space on leaf surfaces, thus reducing plant stomatal conductance. This phenomenon, in turn, reduces the amount of water lost to the atmosphere via transpiration. Tognetti et al. (1998), for example, determined that stomatal conductances of mature oak trees growing near natural CO2 springs in central Italy were significantly lower than those of similar trees growing further away from the springs during periods of severe summer drought.
CO2-induced increases in root development together with CO2-induced reductions in stomatal conductance often contribute to the maintenance of a more favorable plant water status during times of drought. In the case of three Mediterranean shrubs, Tognetti et al. (2002) found that leaf water potential, which is a good indicator of plant water status, was consistently higher (less negative and, hence, less stressful) under twice-ambient CO2 concentrations. Similarly, leaf water potentials of water-stressed mesquite seedlings grown at 700 ppm CO2 were 40 percent higher than those of their water-stressed counterparts growing in ambient air (Polley et al., 1999), which is comparable to values of -5.9 and -3.4 MPa observed in water-stressed evergreen shrubs (Larrea tridentata) exposed to 360 and 700 ppm CO2, respectively (Hamerlynck et al., 2000).
Palanisamy (1999) observed water-stressed Eucalyptus seedlings grown at 800 ppm CO2 display greater net photosynthetic rates than their ambiently grown and water-stressed counterparts. Runion et al. (1999) observed the CO2-induced photosynthetic stimulation of water-stressed pine seedlings grown at 730 ppm CO2 to be nearly 50 percent greater than that of similar water-stressed pine seedlings grown at 365 ppm CO2. Similarly, Centritto et al. (1999a) found that water-stressed cherry trees grown at 700 ppm CO2 displayed net photosynthetic rates that were 44 percent greater than those of water-stressed trees grown at 350 ppm CO2. And Anderson and Tomlinson (1998) found that a 300-ppm increase in the air’s CO2 concentration boosted photosynthetic rates in well-watered and water-stressed red oak seedlings by 34 and 69 percent, respectively, demonstrating that the CO2-induced percentage enhancement in net photosynthesis in this species was essentially twice as great in water-stressed seedlings as in well-watered ones.
Sometimes, plants suffer drastically when subjected to extreme water stress. However, the addition of CO2 to the atmosphere often gives them an edge over ambiently growing plants. Tuba et al. (1998), for example, reported that leaves of a water-stressed woody shrub exposed to an atmospheric CO2 concentration of 700 ppm continued to maintain positive rates of net carbon fixation for a period that lasted three times longer than that observed for leaves of equally water-stressed control plants growing in ambient air. Similarly, Fernandez et al. (1998) discovered that herb and tree species growing near natural CO2 vents in Venezuela continued to maintain positive rates of net photosynthesis during that location’s dry season, while the same species growing some distance away from the CO2 source displayed net losses of carbon during this stressful time. Likewise, Fernandez et al. (1999) noted that after four weeks of drought, the deciduous Venezuelan shrub Ipomoea carnea continued to exhibit positive carbon gains under elevated CO2 conditions, whereas ambiently growing plants displayed net carbon losses. Polley et al. (2002) reported that seedlings of five woody species grown at twice-ambient CO2 concentrations survived 11 days longer (on average) than control seedlings when subjected to maximum drought conditions. Thus, in some cases of water stress, enriching the air with CO2 can mean the difference between life or death.
Arp et al. (1998) reported that six perennial plants common to the Netherlands increased their biomass under CO2-enriched conditions even when suffering from lack of water. In other cases, the CO2-induced percentage biomass increase is sometimes even greater for water-stressed plants than it is for well-watered plants. Catovsky and Bazzaz (1999), for example, reported that the CO2-induced biomass increase for paper birch was 27 percent and 130 percent for well-watered and water-stressed seedlings, respectively. Similarly, Schulte et al. (1998) noted that the CO2-induced biomass increase of oak seedlings was greater under water-limiting conditions than under well-watered conditions (128 percent vs. 92 percent), as did Centritto et al. (1999b) for basal trunk area in cherry seedlings (69 percent vs. 22 percent).
Finally, Knapp et al. (2001) developed tree-ring index chronologies from western juniper stands in Oregon, USA, finding that the trees recovered better from the effects of drought in the 1990’s, when the air’s CO2 concentration was around 340 ppm, than they did from 1900-1930, when the atmospheric CO2 concentration was around 300 ppm. In a loosely related study, Osborne et al. (2002) looked at the warming and reduced precipitation experienced in Mediterranean shrublands over the last century and concluded that primary productivity should have been negatively impacted in those areas. However, when the concurrent increase in atmospheric CO2 concentration was factored into their mechanistic model, a 25 percent increase in primary productivity was projected.
In summary, the peer-reviewed scientific literature indicates that the ongoing rise in the air’s CO2 content will likely lead to substantial increases in photosynthetic rates and biomass production in earth’s woody species in the years and decades ahead, even in the face of stressful conditions imposed by less-than-optimal availability of soil moisture.
Additional information on this topic, including reviews of newer publications as they become available, can be found at http://www.co2science.org/ subject/g/growthwaterwood.php.
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