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). And after nine weeks, the plants growing in the CO2-enriched air had experienced a 37% increase in productivity and were covered with far fewer aphids than the plants growing in ambient air. The result, therefore, was a "win" for the favored plants and a "loss" for the destructive insects.

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 ever 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 full years. Survival of the spittlebug's nymphal states was reduced by 24% 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, into which they introduced the destructive agricultural mite Tetranychus urticae, observing that female mites produced 34% and 49% less offspring in the CO2-enriched chambers in their first and second generations, respectively. These reductions in the reproductive success of this invasive insect, which negatively affects more than 150 crop species worldwide, bodes well indeed for mankind's ability to grow the food we will need to feed our growing numbers in the years and decades ahead.

In a somewhat different type of study, 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 contents of two Mediterranean perennial grasses (Dactylis glomerata and Bromus erectus) by 15% and 87%, respectively, which compounds tend to enhance plant defensive and resistance mechanisms to attacks by both herbivores and pathogens.

Within a still more different context, 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," which could prove to be a big plus for nature in the event of inadvertent Bt gene transference to wild relatives of transgenic crop lines.

Moving forward in time a little faster, Barbehenn et al. (2004b) introduced their study of the subject by noting that increases in the air's CO2 content typically lead to greater decreases in the concentrations of nitrogen and, therefore, protein in the foliage of C3 as compared to C4 grasses, citing Wand et al. (1999) in this regard. And as a result, in the words of Barbehenn et al., "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 (which is always a good thing to do), the three researchers grew Lolium multiflorum Lam. (Italian ryegrass, a common C3 pasture grass) and Bouteloua curtipendula (Michx.) Torr. (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 grasses' foliage. And what did they learn?

As expected, foliage protein concentration decreased by 20% in the C3 grass, but by only 1% in the C4 grass, when they were grown in CO2-enriched air; and, in the words of Barbehenn et al., "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 their expectations, they found that "neither caterpillar species significantly increased its consumption rate to compensate for the lower concentration of protein in [the] C3 grass," noting 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 noted 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." And by way of explanation of these results, they suggested that "post-ingestive mechanisms could provide a sufficient means of compensation for the lower nutritional quality of C3 plants grown under elevated CO2."

Contrary to early simplistic thought on the matter, therefore, and in the estimation of Barbehenn et al., it is becoming ever more evident that "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.

Hard on the heels of their first paper (actually, immediately following it in the same issue of the same journal), Barbehenn et al. (2004a) described how they fed some of the identical foliage of the same experiment to grasshopper (Melanoplus sanguinipes) nymphs that had been reared to the fourth instar stage. In doing so, they observed that "M. sanguinipes did not significantly increase its consumption rate when feeding on the C3 grass grown under elevated CO2," which implied to them that "post-ingestive mechanisms enable these grasshoppers to compensate for variable nutritional quality in their host plants," leading them to further suggest that some of these post-ingestive responses may include "changes in gut size, food residence time, digestive enzyme levels, and nutrient metabolism (Simpson and Simpson, 1990; Bernays and Simpson, 1990; Hinks et al., 1991; Zanotto et al., 1993; Yang and Joern, 1994a,b)." Also, their data indicated that, if anything, M. sanguinipes growth rates were increased, perhaps by as much as 12%, when they fed upon the C3 foliage that had been produced in the CO2-enriched, as compared to the ambient-treatment, air.

Therefore, just as was found in the study of Barbehenn et al. (2004b), the CO2-induced decrease in leaf protein concentration observed in this study did not induce an increase in consumption in the C3 plant studied, nor did it reduce the growth rate of the herbivore studied. Therefore, with respect to this finding, the scientists stated that "although compensatory feeding was commonly observed in early studies [of this subject], the absence of compensatory feeding on C3 plants grown under elevated CO2 has since been observed frequently among herbivorous insects (Bezemer and Jones, 1998)," which suggests that the latter response may ultimately be found to be the more common of the two.

One year later, Bidart-Bouzat et al. (2005) grew three genotypes of mouse-ear cress (Arabidopsis thaliana) from seed in pots placed within controlled-environment chambers maintained at either ambient CO2 (360 ppm) or elevated CO2 (720 ppm). Then, on each of half of the plants (the herbivory treatment) in each of the 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% of each plant's total leaf area in the herbivory treatment being removed. Next, 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. Then, at the conclusion of the herbivory trial, 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, as reported by Maruicio and Rausher (1997) - after which total glucosinolate production was determined by summation of the individual glucosinolate assays. Last of all, various influences of elevated CO2 on moth performance and their association with plant defense-related traits were evaluated.

Overall, the data obtained from the experiment demonstrated 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, Bidart-Bouzat et al. reported 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 found 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)," the three researchers suggested 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)." And it is therefore tempting to speculate that the ongoing rise in the air's CO2 content will enable earth's vegetation to better withstand the ravages of marauding herbivores in the years and decades to come.

Jumping ahead three full years, Ayres et al. (2008) reported the responses of belowground nematode herbivores to atmospheric CO2 enrichment to approximately 350 ppm above ambient in experiments conducted on three grassland ecosystems in Colorado and California (USA) and Montpellier, France. With respect to the soils involved, they stated that "soil moisture increased in response to elevated CO2 in the California, Colorado, and French stud[ies] (Hungate et al., 1997; Nijs et al., 2000; Morgan et al., 2004)." And in regard to the plants involved, they indicated that "elevated CO2 increased root biomass by approximately 3-32% in the first 5 years of the Coloradoan study (Pendall et al., 2004), by 23% after 6 years in the Californian study (Rillig et al., 1999), and by 31% after 6 months in the French study (Dhillion et al., 1996)." And with respect to the nematodes involved, they said that "CO2 enrichment did not significantly affect the family richness, diversity, or PPI [plant parasitic nematode index] of herbivorous nematodes in the Colorado, California, or French study," noting that "in each experiment, neutral effects were the most frequent response to CO2 enrichment." And so it was that the seven researchers could only conclude that "one consequence of increased root production, without changes in belowground herbivore populations, might be greater plant inputs to soil," which "may lead to greater soil organic matter pools in grassland ecosystems, potentially enhancing soil carbon sequestration."

In a second paper from the same year, Lau et al. (2008) measured the amounts of herbivore and pathogen damage done to the common prairie legume Lespedeza capitata growing in ambient and elevated (560 ppm) CO2 treatments in the seventh and eighth full years (2004 and 2005) of the BioCON study (Reich et al., 2001) conducted at the Cedar Creek Natural History Area in Minnesota (USA), where the CO2 treatments were applied during the daylight hours of each growing season. In this setting, herbivore damage was inflicted by three types of pests - (1) generalist chewers (primarily grasshoppers), (2) Pachyschelus laevigatus (Coleoptera: Buprestidae), and (3) Tortriedon sp. (Lepidoptera) - while pathogen damage was caused by Pythium or Fusarium spp.

Interestingly, Lau et al. reported that they detected "no evidence that the CO2 treatments affected herbivore damage." But with respect to pathogen damage, they found that disease incidence "was lower in the elevated CO2 environment, although this difference [10% less in 2004 and 53% less in 2005] was statistically significant only in 2005 (P < 0.01)." Therefore, and because "disease caused major reductions in reproductive output," in the words of the five researchers, "the effects of CO2 on disease incidence may be important for L. capitata evolution and population dynamics," which phenomena should significantly benefit this species in a high-CO2 world of the future. In addition, they noted that Strengbom and Reich (2006), "working in the same experimental site ... also found that elevated CO2 ... reduced disease incidence on Solidago rigida."

Last of all, in what they described as "the first study that measured the effect of global atmospheric change on an omnivorous consumer," Coll and Hughes (2008) explored the impacts of elevated atmospheric CO2 on the behavior and performance of an omnivorous bug (Oechalia schellenbergii, Heteroptera: Pentatomidae) and its prey, a polyphagous chewing herbivorous pest (Helicoverpa armigera; Lepidoptera: Noctuidae), feeding on pea (Pisum sativum) foliage grown in controlled-environment cabinets maintained at atmospheric CO2 concentrations of either 360 or 700 ppm. This work revealed that the H. armigera pests that fed on the elevated CO2-grown pea plants were significantly smaller than those that fed on the ambient CO2-grown pea plants, and that the bigger O. schellenbergii bugs that fed on them "performed best when fed larvae from the elevated-CO2 treatment," because the prey of that treatment "were smaller and thus easier to subdue." In fact, only 13.3% of the predation attempts made on the larvae that were fed ambient-CO2-grown foliage were successful, as compared to 78.2% for the larvae that were fed elevated-CO2-grown foliage.

In light of their findings, the two researchers thus concluded that "elevated CO2 may benefit generalist predators through increased prey vulnerability, which would put pest species under higher risk of predation." Consequently, and "since omnivory is widespread in agroecosystems," they argued that "yield loss to most pest species will be lower under elevated atmospheric CO2 levels, compared to the current condition," which is good news for agriculture and great news for the people who depend upon it for their survival, which is nearly all of us.

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.

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