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Phenolics (Woody Species) -- Summary
As the air's CO2 concentration continues to rise, many of earth's plants are experiencing enhanced rates of photosynthetic carbon uptake, which phenomenon commonly leads to increased production of plant secondary carbon compounds, including phenolics.  As a result, atmospheric CO2 enrichment generally increases foliar phenolic concentrations, which often enhance plant resistance to herbivore and pathogen attack.  In this summary, therefore, we review the results of some of the studies that have dealt with this important subject over the past several years.

Penuelas et al. (2002) sampled leaves of three species of shrubs growing close to, and further away from, CO2-emitting springs in Pisa, Italy, to determine the long-term effects of elevated atmospheric CO2 on foliar concentrations of carbon-based secondary compounds.  They found that the extra 340 ppm of CO2 near the springs had very few long-term significant effects on foliar concentrations of most such substances, including phenolics, and those effects that were observed varied according to compound and plant species.  This result, however, is somewhat atypical of what is often observed, as several studies of temperate-region trees have shown leaf phenolic concentrations to rise by 20-60% in response to a doubling of the air's CO2 content (Koricheva et al., 1998; Peñuelas and Estiarte, 1998; McDonald et al., 1999; Agrell et al., 2000; Hartley et al., 2000), as has also been reported by Parsons et al. (2003) with respect to the total fine-root phenolic concentrations of warm-temperate conifers studied by King et al. (1997), Entry et al. (1998) and Runion et al. (1999).

One of the first such positive-result studies that we reviewed on our website was that of Gebauer et al. (1998), who grew loblolly pine seedlings in glasshouses maintained at atmospheric CO2 concentrations of 350 and 700 ppm for a total of five months, while subjecting them to four different levels of soil nitrogen fertilization.  Across all soil nitrogen regimes, this experiment revealed that the extra CO2 increased the above- and below-ground concentrations of seedling total phenolics by 21 and 35%, respectively.

Also working with loblolly pines were Booker and Maier (2001), who measured concentrations of total soluble phenolics in needles exposed for two years in branch chambers to ambient air and air enriched to as much as 350 ppm CO2 above ambient.  They found that needle concentrations of total soluble phenolics increased about 11% in response to elevated CO2, noting that this response was related to "the balance between carbohydrate sources and sinks," such that "the greater the source:sink ratio, the greater the concentration of phenolic compounds (Herms and Mattson, 1992; Peñuelas and Estiarte, 1998)."

On the other hand, working in the understory of the loblolly pine plantation in the Duke Forest FACE study, Hamilton et al. (2004) report they found no evidence of significant changes in total leaf phenolics in either of two years, in agreement 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)."  Nevertheless, they say 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 observed "the same pattern and magnitude of reduction."

In a somewhat similar FACE study of an ecosystem dominated by three species of oak tree (Quercus myrtifolia, Q. chapmanii and Q. geminata) plus the nitrogen-fixing legume Galactia elliottii at the Kennedy Space Center in Florida, USA, Hall et al. (2005) could detect 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; but when all four species were considered 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 CO2-induced decreases in all leaf damage categories associated with herbivory: 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, the researchers had no choice but to conclude 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."

Another pertinent study we have reviewed is that of Wetzel and Tuchman (2005), who grew trembling aspen seedlings for a period of three years in open-bottom root boxes out-of-doors within clear-plastic-wall open-top chambers maintained at either ambient (360 ppm) or elevated (720 ppm) atmospheric CO2 concentrations from early spring through leaf senescence.  During this period, green and naturally-senesced leaves were collected and analyzed for the fraction of leaf mass composed of total phenolics.  This exercise revealed that green leaf material contained 19.1% more total phenolics when the experimental seedlings were grown in CO2-enriched as opposed to ambient air, while senesced leaf material grown in CO2-enriched air contained 63.2% more total phenolics than similar leaf material grown in ambient air.

In a study conducted in Finland, Kuokkanen et al. (2003) grew two-year-old birch trees in the field in closed-top chambers exposed to either ambient air of 350 ppm CO2 or air enriched to a CO2 concentration of 700 ppm at either ambient temperatures or ambient temperatures plus 3°C for one full growing season.  During the middle of summer, when carbon-based secondary compounds of birch leaves are fairly stable, they picked several leaves from each tree and measured the concentrations of a number of physiologically-important substances they contained.  This work revealed that the concentration of total phenolics significantly increased in the birch leaves produced in the CO2-enriched air, as has also been observed in the experiments of Lavola and Julkunen-Titto (1994), Williams et al. (1994), Kinney et al. (1997), Bezemer and Jones (1998) and Kuokkanen et al. (2001).

Last of all, we report the findings of Coley et al. (2002), who studied nine different species of tropical trees that were rooted in the ground and grown in their natural environment near the Smithsonian Tropical Research Institute's experiment site in central Panama.  Their six-month open-top chamber study produced some impressive results, with eight of the nine species exhibiting positive leaf phenolic/tannin responses to a doubling of the air's CO2 content, the largest of which was a concentration increase of 119%.  The singular negative response was a 27% decline, while the mean response of all nine species was an increase of 48%.  These results are comparable to those obtained for temperate-region trees, and they provide the basis for Coley et al.'s primary conclusion, i.e., that although "both temperate and tropical trees show large interspecific variation in the extent of their response to CO2 ... the overwhelming pattern is for an increase in phenolics by approximately 50%."

In conclusion, the results of these several studies suggest that future increases in the air's CO2 concentration will likely enhance foliar phenolic concentrations in many shrubs and trees.  This phenomenon, in turn, should enhance woody-plant defense mechanisms that help deter herbivory, which should improve forest health, robustness and longevity the world over.

References
Agrell, J., McDonald, E.P. and Lindroth, R.L.  2000.  Effects of CO2 and light on tree phytochemistry and insect performance.  Oikos 88: 259-272.

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.

Booker, F.L. and Maier, C.A.  2001.  Atmospheric carbon dioxide, irrigation, and fertilization effects on phenolic and nitrogen concentrations in loblolly pine (Pinus taeda) needles.  Tree Physiology 21: 609-616.

Coley, P.D., Massa, M., Lovelock, C.E. and Winter, K.  2002.  Effect of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree.  Oecologia 133: 62-69.

Entry, J.A., Runion, G.B., Prior, S.A., Mitchell, R.J. and Rogers, H.H.  1998.  Influence of CO2 enrichment and nitrogen fertilization on tissue chemistry and carbon allocation in longleaf pine seedlings.  Plant and Soil 200: 3-11.

Finzi, A.C. and Schlesinger, W.H.  2002.  Species control variation in litter decomposition in a pine forest exposed to elevated CO2Global Change Biology 8: 1217-1229.

Gebauer, R.L.E., Strain, B.R. and Reynolds, J.F.  1998.  The effect of elevated CO2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda).  Oecologia 113: 29-36.

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., 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.

Hartley, S.E., Jones, C.G., Couper, G.C. and Jones, T.H.  2000.  Biosynthesis of plant phenolic compounds in elevated atmospheric CO2Global Change Biology 6: 497-506.

Herms, D.A. and Mattson, W.J.  1992.  The dilemma of plants: to grow or defend.  Quarterly Review of Biology 67: 283-335.

King, J.S., Thomas, R.B. and Strain, B.R.  1997.  Morphology and tissue quality of seedling root systems of Pinus taeda and Pinus ponderosa as affected by varying CO2, temperature, and nitrogen.  Plant and Soil 195: 107-119.

Kinney, K.K., Lindroth, R.L., Jung, S.M. and Nordheim, E.V.  1997.  Effects of CO2 and NO3 availability on deciduous trees, phytochemistry and insect performance.  Ecology 78: 215-230.

Koricheva, J., Larsson, S., Haukioja, E. and Keinanen, M.  1998.  Regulation of woody plant metabolism by resource availability: hypothesis testing by means of a meta-analysis.  Oikos 83: 212-226.

Kuokkanen, K., Julkunen-Titto, R., Keinanen, M., Niemela, P. and Tahvanainen, J.  2001.  The effect of elevated CO2 and temperature on the secondary chemistry of Betula pendula seedlings.  Trees 15: 378-384.

Kuokkanen, K., Yan, S. and Niemela, P.  2003.  Effects of elevated CO2 and temperature on the leaf chemistry of birch Betula pendula (Roth) and the feeding behavior of the weevil Phyllobius maculicornisAgricultural and Forest Entomology 5: 209-217.

Lavola, A. and Julkunen-Titto, R.  1994.  The effect of elevated carbon dioxide and fertilization on primary and secondary metabolites in birch, Betula pendua (Roth).  Oecologia 99: 315-321.

McDonald, E.P., Agrell, J. and Lindroth, R.L.  1999.  CO2 and light effects on deciduous trees: growth, foliar chemistry and insect performance.  Oecologia 119: 389-399.

Parsons, W.F.J., Kopper, B.J. and Lindroth, R.L.  2003.  Altered growth and fine root chemistry of Betula papyrifera and Acer saccharum under elevated CO2Canadian Journal of Forest Research 33: 842-846.

Peñuelas, J., Castells, E., Joffre, R. and Tognetti, R.  2002.  Carbon-based secondary and structural compounds in Mediterranean shrubs growing near a natural CO2 spring.  Global Change Biology 8: 281-288.

Peñuelas, J. and Estiarte, M.  1998.  Can elevated CO2 affect secondary metabolism and ecosystem function?  Trees 13: 20-24.

Runion, G.B., Entry, J.A., Prior, S.A., Mitchell, R.J. and Rogers, H.H.  1999.  Tissue chemistry and carbon allocation in seedlings of Pinus palustris subjected to elevated atmospheric CO2 and water stress.  Tree Physiology 19: 329-335.

Wetzel, R.G. and Tuchman, N.C.  2005.  Effects of atmospheric CO2 enrichment and sunlight on degradation of plant particulate and dissolved organic matter and microbial utilization.  Archiv fur Hydrobiologie 162: 287-308.

Williams, R.S., Lincoln, D.E. and Thomas, R.B.  1994.  Loblolly pine grown under elevated CO2 affects early instar pine sawfly performance.  Oecologia 98: 64-71.

Last updated 5 October 2005