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% 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% 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 minor 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, thus reducing the negative impacts of these agricultural chemicals on the environment.

In another study conducted on five scrub-oak forest species at the same experimental facility, Stiling et al. (2002b) 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, in fact, 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 [our italics]," which is a truly exciting observation.

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% 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 sixteen 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% 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% lower (P = 0.072) in the CO2-enriched air. The implications of these findings are rather obvious: myrtle oak trees growing in their natural habitat will likely suffer far 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 of 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 across-species mean increases of 6.8% for condensed tannins, 6.1% for hydrolyzable tannins, 5.1% for total phenolics and 4.3% for lignin. In addition, there were large and often significant CO2-induced decreases in all leaf damage categories among all species: chewing (-48%, P < 0.001), mines (-37%, P = 0.001), eye spot gall (-45%, P < 0.001), leaf tier (-52%, P = 0.012), leaf mite (-23%, P = 0.477) and leaf gall (-16%, 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 the final study to come out of the Florida scrub-oak ecosystem that we have reviewed, 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% in 2000, 18% in 2001 and 41% 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., 2005)."

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.

References
Dury, S.J., Good, J.E.G., Perrins, C.M., Buse, A. and Kaye, T. 1998. The effects of increasing CO2 and temperature on oak leaf palatability and the implications for herbivorous insects. Global Change Biology 4: 55-61.

Fajer, E.D., Bowers, M.D. and Bazzaz, F.A. 1991. The effects of enriched CO2 atmospheres on the buckeye butterfly, Junonia coenia. Ecology 72: 751-754.

Hall, M.C., Stiling, P., Hungate, B.A., Drake, B.G. and Hunter, M.D. 2005a. Effects of elevated CO2 and herbivore damage on litter quality in a scrub oak ecosystem. Journal of Chemical Ecology 31: 2343-2356.

Hall, M.C., Stiling, P., Moon, D.C., Drake, B.G. and Hunter, M.D. 2005b. Effects of elevated CO2 on foliar quality and herbivore damage in a scrub oak ecosystem. Journal of Chemical Ecology 31: 267-285.

Lindroth, R.L. 1996. CO2-mediated changes in tree chemistry and tree-Lepidoptera interactions. In: Koch, G.W. and Mooney, H,A. (Eds.). Carbon Dioxide and Terrestrial Ecosystems. Academic Press, San Diego, California, USA, pp. 105-120.

Rossi, A.M., Stiling, P., Moon, D.C., Cattell, M.V. and Drake, B.G. 2004. Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO2. Journal of Chemical Ecology 30: 1143-1152.

Stiling, P., Cattell, M., Moon, D.C., Rossi, A., Hungate, B.A., Hymus, G. and Drake, B.G. 2002a. Elevated atmospheric CO2 lowers herbivore abundance, but increases leaf abscission rates. Global Change Biology 8: 658-667.

Stiling, P., Moon, D.C., Hunter, M.D., Colson, J., Rossi, A.M., Hymus, G.J. and Drake, B.G. 2002b. Elevated CO2 lowers relative and absolute herbivore density across all species of a scrub-oak forest. Oecologia 134: 82-87.

Stiling, P., Rossi, A.M., Hungate, B., Dijkstra, P., Hinkle, C.R., Knot III, W.M., and Drake, B. 1999. Decreased leaf-miner abundance in elevated CO2: Reduced leaf quality and increased parasitoid attack. Ecological Applications 9: 240-244.