In an experiment conducted on a natural forest ecosystem in Wisconsin, USA, comprised predominantly of trembling aspen trees, Percy et al. (2002) studied the effects of increases in CO2 (to 560 ppm during daylight hours), O3 (to 46.4-55.5 ppb during daylight hours), and CO2 and O3 together on the forest tent caterpillar, a common leaf-chewing lepidopteran found in North American hardwood forests.  By itself, elevated CO2 reduced tent caterpillar performance by reducing female pupal mass; while elevated O3 alone enhanced tent 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 reduced the performance of the forest tent caterpillar, which finding is particularly satisfying because, in the words of Percy et al., "historically, the forest tent caterpillar 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."

Three years earlier, Stiling et al. (1999) had reported the results of what may possibly have been the first attempt to study the effects of elevated CO2 on trophic food webs in a natural ecosystem, specifically, a nutrient-poor scrub-oak community in Florida, USA, where sixteen open-top chambers of 3.6-m diameter were fumigated with air of either 350 or 700 ppm CO2 for approximately one year.  At the end of that period, total leaf miner densities were found to be 38% less on the CO2-enriched foliage than on the foliage produced by the plants growing in ambient air.  Moreover, atmospheric CO2 enrichment consistently reduced the numbers of all six species of leaf miners studied.  In a compensatory development, however, exposure to elevated CO2 increased the amount of leaf area consumed by the less-abundant leaf miners by approximately 40%.  Nevertheless, leaf miners in the CO2-enriched chambers experienced significantly greater mortality than those in the control chambers, although CO2-induced reductions in leaf nitrogen content were determined to have played a minor role in this phenomenon.  By far the greatest factor contributing to the higher leaf miner 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.

Subsequently, Stiling et al. (2002) reported even more dramatic effects of the elevated CO2 of this long-running experiment on leaf chewers.  The relative levels of damage by these insects (primarily larval lepidopterans and grasshoppers) were significantly lower in the elevated CO2 chambers than in the ambient CO2 chambers for all five of the plant species that accounted for over 98% of the total plant biomass of the ecosystem.  In addition, the response to elevated CO2 was the same across all plant species.  Also, they reported 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 on 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.  An interesting implication of these findings, as suggested by Stiling et al., 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," which is truly an exciting possibility.

In a further study of this ecosystem that 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 tree species, Rossi et al. (2004) followed 100 marked leaves in each of the ecosystem's eight ambient-air and eight CO2-enriched 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 [CO2] chambers were assessed using paired t-tests."  They report 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.

In yet another study conducted in the same ecosystem, Hall et al. (2005) concentrated on the four plant species that dominate the community and are present in every chamber, including three oaks (Quercus myrtifolia, Q. chapmanii and Q. geminata) and the nitrogen-fixing legume Galactia elliottii.  At three-month intervals from May 2001 to May 2003, samples of undamaged leaves were removed from each of the four species in all chambers and analyzed for various chemical constituents, while 200 randomly selected leaves of each species in each chamber were scored for the presence of six types of herbivore damage.  The results of these efforts indicated 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).  As a result, Hall et al. 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."

Shifting our attention to a third ecosystem, Hamilton et al. (2004) conducted a study at the Duke Forest FACE facility, where three 30-m-diameter FACE plots in a 17-year-old (in 2000) loblolly pine plantation in the Piedmont region of North Carolina have been continuously enriched with an extra 200 ppm of CO2 and three identical control plots have been similarly exposed to ambient air since 1996.  There, they measured the amount of leaf tissue damaged by insects and other herbivorous arthropods during two growing seasons in the deciduous forest understory, which contains 48 species of other woody plants (trees, shrubs and vines) that have naturally established themselves, concentrating on the loss of foliage due to herbivory that was experienced by three deciduous tree species: sweetgum, red maple and winged elm.

So what did they observe?  As Hamilton et al. describe it, "we found that elevated CO2 led to a trend toward reduced herbivory in [the] deciduous understory in a situation that included the full complement of naturally occurring plant and insect species."  In 1999, for example, they report that "elevated CO2 reduced overall herbivory by more than 40% with elm showing greater reduction than either red maple or sweetgum," 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 (Stilling et al., 2002)."  Consequently, and in spite of all 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 more likely, 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 impressive study of this most important question.

Last of all, in a subsequent three-year study conducted in the same forest understory, Knepp et al. (2005) assessed leaf damage on seven species of trees (red maple, redbud, sweetgum, black cherry, white oak, willow oak and winged elm) in 2001, 2002 and 2003, while five additional species (sugar maple, yellow poplar, red oak, black oak and black locust) 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," noting that "the percentage of leaf tissue damaged by insect herbivores was 3.8% per leaf under ambient CO2 and 3.3% 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% compared with 1.7% for plants under elevated CO2," which was "indicative of a 46% 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 highly desirable 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 discus is that "forest herbivory may decrease under elevated CO2 because of a decline in the abundance of chewing insects," citing the observations of Stilling 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 in a high-CO2 world of the future?  In their concluding paragraph, Knepp et al. say that "in 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."  We agree, noting that this sentiment appears to be the take-home message of the other studies reviewed in this summary as well.

References
Awmack, C.S. and Leather, S.R.  2002.  Host plant quality and fecundity in herbivorous insects.  Annual Review of Entomology 47: 817-844.

Bezemer, T.M. and Jones, T.H.  1998.  Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects.  Oikos 82: 212-222.

Coviella, C.E. and Trumble, J.T.  1999.  Effects of elevated atmospheric carbon dioxide on insect-plant interactions.  Conservation Biology 13: 700-712.

Finzi, A.C. and Schlesinger, W.H.  2002.  Species control variation in litter decomposition in a pine forest exposed to elevated CO2.  Global Change Biology 8: 1217-1229.

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

Hamilton, J.G., Zangerl, A.R., Berenbaum, M.R., Pippen, J.S., Aldea, M. and DeLucia, E.H.  2004.  Insect herbivory in an intact forest understory under experimental CO2 enrichment.  Oecologia 138: 566-573.

Hunter, M.D.  2001.  Effects of elevated atmospheric carbon dioxide on insect-plant interactions.  Agricultural and Forest Entomology 3: 153-159.

Knepp, R.G., Hamilton, J.G., Mohan, J.E., Zangerl, A.R., Berenbaum, M.R. and DeLucia, E.H.  2005.  Elevated CO2 reduces leaf damage by insect herbivores in a forest community.  New Phytologist 167: 207-218.

Percy, K.E., Awmack, C.S., Lindroth, R.L., Kubiske, M.E., Kopper, B.J., Isebrands, J.G., Pregitzer, K.S., Hendrey, G.R., Dickson, R.E., Zak, D.R., Oksanen, E., Sober, J., Harrington, R. and Karnosky, D.F.  2002.  Altered performance of forest pests under atmospheres enriched by CO2 and O3.  Nature 420: 403-407.

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., Moon, D.C., Hunter, M.D., Colson, J., Rossi, A.M., Hymus, G.J. and Drake, B.G.  2002.  Elevated CO2 lowers relative and absolute herbivore density across all species of a scrub-oak forest.  Oecologia DOI 10.1007/s00442-002-1075-5.

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.