Dury et al. (1998) grew four-year-old pedunculate oak trees in pots within greenhouses maintained at ambient and twice-ambient atmospheric CO2 concentrations in combination with ambient and elevated (ambient plus 3°C) air temperatures for approximately one year. This work revealed that elevated CO2 had only minor and contrasting direct effects on leaf palatability: a temporary increase in foliar phenolic concentrations and decreases in leaf toughness and nitrogen content. The elevated temperature treatment, on the other hand, significantly reduced leaf palatability, because oak leaf toughness increased as a consequence of temperature-induced increases in condensed tannin concentrations. As a result, the researchers concluded that "a 3°C rise in temperature might be expected to result in prolonged larval development, increased food consumption, and reduced growth" for herbivores feeding on oak leaves in a CO2-enriched and warmer world of the future.

In a radically different type of experiment, Cornelissen et al. (2003) studied fluctuating asymmetry in the leaves of two species of schlerophyllous oaks - myrtle oak (Quercus myrtifolia) and sand live oak (Quercus geminata) - that dominate a native scrub-oak community at the Kennedy Space Center, Titusville, Florida (USA), which has served as the base of operations for a number of important open-top-chamber investigations of the effects of a 350-ppm increase in atmospheric CO2 concentration on this unique ecosystem; and to provide a little background for their study, we note that fluctuating asymmetry is the terminology used to describe small variations from perfect symmetry in otherwise bilaterally symmetrical characters in an organism (Moller and Swaddle, 1997), which asymmetry is believed to arise as a consequence of developmental instabilities experienced during ontogeny that may be caused by various stresses, including both genetic and environmental factors (Moller and Shykoff, 1999).

Based on measurements of (1) distances from the leaf midrib to the left and right edges of the leaf at its widest point and (2) leaf areas on the left and right sides of the leaf midrib, Cornelissen et al. determined that "asymmetric leaves were less frequent in elevated CO2, and, when encountered, they were less asymmetric than leaves growing under ambient CO2." In addition, they found that "Q. myrtifolia leaves under elevated CO2 were 15.0% larger than in ambient CO2 and Q. geminata leaves were 38.0% larger in elevated CO2 conditions." As a bonus, they also determined that "elevated CO2 significantly increased tannin concentration for both Q. myrtifolia and Q. geminata leaves" and that "asymmetric leaves contained significantly lower concentrations of tannins than symmetric leaves for both Q. geminata and Q. myrtifolia."

In commenting on their primary findings of reduced percentages of leaves experiencing asymmetry in the presence of elevated levels of atmospheric CO2 and the lesser degree of asymmetry exhibited by affected leaves in the elevated CO2 treatment, Cornelissen et al. say that "a possible explanation for this pattern is the fact that, in contrast to other environmental stresses, which can cause negative effects on plant growth, the predominant effect of elevated CO2 on plants is to promote growth with consequent reallocation of resources (Docherty et al., 1996)." Another possibility they discuss "is the fact that CO2 acts as a plant fertilizer," and, as a result, that "elevated CO2 ameliorates plant stress compared with ambient levels of CO2," which is one of the well-documented biological benefits of atmospheric CO2 enrichment (Idso and Idso, 1994).

With respect to the ancillary finding of CO2-induced increases in tannin concentrations in the leaves of both oak species (a mean increase of approximately 35% for Q. myrtifolia and 43% for Q. geminata), we note that this phenomenon may provide the two species with greater protection against herbivores, and that part of that protection may be associated with the observed CO2-induced reductions in the amount and degree of asymmetry in the leaves of the CO2-enriched trees. Consistent with this hypothesis, for example, Stiling et al. (1999, 2003) found higher abundances of leaf miners in the leaves of the trees in the ambient CO2 chambers, where asymmetric leaves were more abundant, while in the current study it was determined that leaf miners attacked asymmetric leaves more frequently than would be expected by chance alone in both CO2 treatments.

In a subsequent study conducted at the Kennedy Space Center's scrub-oak community, Hall et al. (2005b) evaluated foliar quality and herbivore damage in three oaks (Q. myrtifolia, Q. chapmanii and Q. geminata) plus the nitrogen-fixing legume Galactia elliottii at three-month intervals from May 2001 to May 2003, at which times samples of undamaged leaves were removed from each of the four species in all chambers and analyzed for various chemical constituents, while 200 randomly selected leaves of each species in each chamber were scored for the presence of six types of herbivore damage. Analyses of the data thereby obtained indicated that for condensed tannins, hydrolyzable tannins, total phenolics and lignin, in all four species there were always greater concentrations of all four leaf constituents in the CO2-enriched leaves, with across-species mean increases of 6.8% for condensed tannins, 6.1% for hydrolyzable tannins, 5.1% for total phenolics and 4.3% for lignin. In addition, there were large CO2-induced decreases in all leaf damage categories among all species: chewing (-48%), mines (-37%), eye spot gall (-45%), leaf tier (-52%), leaf mite (-23%) and leaf gall (-16%). Hall et al. thus concluded that the changes they observed in leaf chemical constituents and herbivore damage "suggest that damage to plants may decline as atmospheric CO2 levels continue to rise."

Last of all, and largely overlapping the investigation of Hall et al. (2005b), was the study of Hall et al. (2005a), who evaluated the effects of the Kennedy Space Center experiment's extra 350 ppm of CO2 on litter quality, herbivore activity, and their interactions, over the three-year-period 2000-2002. This endeavor indicated, in their words, that "changes in litter chemistry from year to year were far larger than effects of CO2 or insect damage, suggesting that these may have only minor effects on litter decomposition." The one exception to this finding was that "condensed tannin concentrations increased under elevated CO2 regardless of species, herbivore damage, or growing season," rising by 11% in 2000, 18% in 2001 and 41% in 2002 as a result of atmospheric CO2 enrichment, as best we can determine from the researchers' bar graphs. Also, the five scientists report that "lepidopteran larvae can exhibit slower growth rates when feeding on elevated CO2 plants (Fajer et al., 1991) and become more susceptible to pathogens, parasitoids, and predators (Lindroth, 1996; Stiling et al., 1999)," noting further that at their field site, "which hosts the longest continuous study of the effects of elevated CO2 on insects, herbivore populations decline markedly under elevated CO2 (Stiling et al., 1999, 2002, 2003; Hall et al., 2005b)."

In conclusion, it would appear that the large and continuous enhancement of condensed tannin concentrations in oak tree foliage produced in CO2-enriched air is a good omen for people worried about greenhouse gas-induced global warming, because methane emissions from ruminants feeding on foliage rich in condensed tannins tend to be lower than methane emissions from ruminants feeding on foliage of lower tannin concentration (see our Editorial of 7 Aug 2002). In addition, the marked tannin-induced declines in herbivore populations observed in CO2-enriched open-top-chamber studies bodes well for the ability of earth's vegetation to better resist herbivore attacks as the air's CO2 content continues to climb.

References
Cornelissen, T., Stiling, P. and Drake, B. 2003. Elevated CO2 decreases leaf fluctuating asymmetry and herbivory by leaf miners on two oak species. Global Change Biology 10: 27-36.

Docherty, M., Hurst, D.K., Holopainem, J.K. et al. 1996. Carbon dioxide-induced changes in beech foliage cause female beech weevil larvae to feed in a compensatory manner. Global Change Biology 2: 335-341.

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.

Idso, K.E. and Idso, S.B. 1994. Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: a review of the past 10 years' research. Agricultural and Forest Meteorology 69: 153-203.

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.

Moller, A.P. and Shykoff, P. 1999. Morphological developmental stability in plants: patterns and causes. International Journal of Plant Sciences 160: S135-S146.

Moller, A.P. and Swaddle, J.P. 1997. Asymmetry, Developmental Stability and Evolution. Oxford University Press, Oxford, UK.

Stiling, P., Cattell, M., Moon, D.C., Rossi, A., Hungate, B.A., Hymus, G. and Drake, B.G. 2002. 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. 2003. 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.