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Herbivory (Woody Plants - Maple) -- Summary
Insect pests have greatly vexed earth's trees 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 impact this phenomenon, for better or for worse. Consequently, in the paragraphs that follow, we review the results of several studies that have addressed this subject as it applies to three species of maple tree.

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 [our italics] 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, which would appear to confer an advantage upon this particular herbivore in this particular situation.

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% 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.

So what did they find? 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%," 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., 2003)."

Consequently, and in spite of all 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% 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 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 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, and especially its maple trees, 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."

But what if herbivore-induced damage happens to increase - for some strange reason in some situations - 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% of the saplings' leaf area was removed from half of the trees in order to study the impact of concomitant 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%. When the trees were stressed by simulated herbivory, however, the CO2-enriched maples produced 28% 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."

All in all, therefore, it would appear that earth's maple trees - and probably many, if not most, other trees - may 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.

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.

Cannon, R.J. 1998. The implications of predicted climate change for insect pests in the UK, with emphasis on non-indigenous species. Global Change Biology 4: 785-796.

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.

Hamilton, J.G., Zangerl, A.R., Berenbaum, M.R., Pippen, J., Aldea, M. and DeLucia, E.H. 2004. Insect herbivory in an intact forest understory under experimental CO2 enrichment. Oecologia 138: 10.1007/s00442-003-1463-5.

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.

Kruger, E.L., Volin, J.C. and Lindroth, R.L. 1998. Influences of atmospheric CO2 enrichment on the responses of sugar maple and trembling aspen to defoliation. New Phytologist 140: 85-94.

Lincoln, D.E., Fajer, E.D. and Johnson, R.H. 1993. Plant-insect herbivore interactions in elevated CO2 environments. Trends in Ecology and Evolution 8: 64-68.

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.

Whittaker, J.B. 1999. Impacts and responses at population level of herbivorous insects to elevated CO2. European Journal of Entomology 96: 149-156.

Williams, R.S., Lincoln, D.E. and Norby, R.J. 2003. Development of gypsy moth larvae feeding on red maple saplings at elevated CO2 and temperature. Oecologia 137: 114-122.

Last updated 20 June 2007