Example II of EPA STAR Proposal

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1 Example II of EPA STAR Proposal Name: Myra Carmen Hall Statement of Objectives: One of the most vivid memories from my childhood is riding with my father on a tractor. He stopped the tractor and lifted me off to show me a dung beetle rolling a ball of dung to its nest. My father took the time to explain the purpose of this strange beetle. At that moment I began to ceaslessly ask how and why questions about the world. Later I would take multiple tests meant to help me determine the best career path and over and over again the answer would be systems analyst. Invariably the guidance counselors would recommend engineering or computer sciences, but in my mind it was inevitable that I ended up in ecology. I cannot think of a field where a predisposition for systems analysis is a better fit. I am left in awe of the myriad of species that seeming coexist seamlessly in an environment. It is, I think, one of the greatunsolved puzzles in science. With the world changing at an ever-increasing pace there is a great deal to learn about natural habitats and very little time in which to do it. Everyday ecosystems are coming under pressure. Some are being destroyed outright, while other alterations may be less obvious, but no less detrimental. How is it possible for us to determine the effects of deforestation, housing development, or climate change on the world s ecosystems if we do not know how they work to begin with? Many people think that we know all the species that exist, yet within the last few years a new mammal species has been identified in South America, and a new order found in the insects. Just doing my masters research resulted in finding several unidentified parasitoid species. In the world of plants, new species are being cataloged everyday. The question most often posed by my nonscience friends is so what?. I am ashamed to admit that that is one of the most difficult questions for meto answer. So what if I found a new species of wasp? It is smaller than a flea and far less annoying and beyond a basic idea of how it fits into the community I studied, I have little idea of how or if it is important in the larger scheme of things. The inborn drive to find answers lead me to an undergraduate research project which in turn lead to a master s thesis that examined competition within a gallforming waps community. However, for every question I have answered a dozen questions without answers have cropped up. This in turn has lead me to continue my education and seek a doctrol degree in ecology. My current research looks at the affects of human impact on the global environment. By examining the impacts of elevated atmospheric carbon dioxide on plant and insect communities, I will be one step closer to answering one of the so what? questions. I am sure that as I finish my doctoral research that I will have more questions than I began with. I can only hope so.

2 Education and Experience: 8/01 to Present: Enrolled in Ph.D. Program at the University of Georgia 8/01 to Present: Research Assistant UGA, Department of Ecology. Contact Mark Hunter, (706) /98 8/01: Texas State University, MS Biology 8/00-5/01: Teaching Assistant TxSt, Department of Biology. Contact Caitlin Gabor, (512) /98 8/00: Teaching Assistant TxSt, Department of Biology. Contact Jim Ott, (512) /98 8/98: Research Assistant TxSt, Department of Biology. Contact Jim Ott, (512) /94 12/97: Texas State University, BS Wildlife Biology 10/89 10/93: United States Army Publications: N/A

3 Narrative Statement: Introduction Ecosystems are dynamic and are constantly influenced by environmental variability. Increasing atmospheric concentrations of CO 2 are expected to have pronounced effects on ecosystem composition and function. The mechanisms include direct effects on foliar quality, direct and indirect effects on herbivores and litter quality. Plant responses to elevated CO 2 concentrations are unpredictable due to inter- and intraspecific variation in plant species (Williams et al., 1986; Bazzaz, 1990; Lindroth et al., 1993; Curtis et al., 1996; Johnson et al., 1996; Norby et al., 1996; Cook et al., 1997; Ineson and Cotrufo, 1997; Van Gardingen et al., 1997; Woodward and Beerling, 1997). Interspecific differences are evident in variation in growth responses and biomass allocation, as well as magnitude and direction of changes in concentrations of primary and secondary metabolites. Garbutt and Bazzaz (1984) found that Phlox drummondii populations differed in time of flowering, number of flowers, and plant biomass in response to differing levels of elevated CO 2. Environmental factors also lead to different plant responses to elevated CO 2 further complicating the problem of predictability within and among species (Bazzaz, 1990). Understanding ecosystem changes depends ultimately on understanding lower scale functioning (Saxe et al., 1998). For example, the ecological and physiological effects of increasing concentrations of CO 2 on plant communities may include complex interactions among atmospheric CO 2, foliar quality, herbivores, and decomposition (Williams et al., 1986; Lindroth et al., 1993; Curtis et al., 1996; Johnson et al., 1996; Cook et al., 1997; Ineson and Cotrufo, 1997; Van Gardingen et al., 1997). My research proposes to examine such interactions. Atmospheric CO 2 changes foliar quality, which may affect insect herbivores, litter quality, decomposition processes, and soil nutrient availability. Insect herbivores, in turn, may affect foliar quality, which could lead to changes in litter quality, decomposition processes, and soil nutrient availability. More uncertain, however, are the direct interactions of CO 2 and insect herbivores. Insects have developed numerous strategies for utilizing plants as food. For example, feeding guilds of herbivores can be broadly categorized as chewers, suckers, miners, and borers. The nutritional quality of plant foliage has profound effects on herbivores (Feeny 1968; Coley and Aide, 1991; Feeny, 1992; Dury et al., 1998). Changes in plant chemistry affect the quality of herbivore diets and may result in behavioral changes (increased foraging time) and/or physiological changes (longer development times) (Koch and Mooney, 1996; Lindroth, 1996; Stiling et al., 1999). For example, to compensate for lower nitrogen concentrations in leaves under elevated CO 2, insect herbivores often increase their consumption rates by 20-80% (Lincoln et al., 1984; Lincoln and Couvet, 1989; Fajer, 1989; Fajer et al., 1989; Fajer et al., 1991; Lincoln et al., 1993; Johnson and Ball, 1996). Lepidopteran larvae exhibit increased mortality and slower growth rates when feeding on elevated CO 2 plants (Akey and Kimball, 1989; Fajer, 1989; Fajer et al., 1989; Fajer et al., 1991). Consequently, herbivores may become more susceptible to pathogens, parasitoids, and predators (Price et al., 1980; Koch and Mooney, 1996; Lindroth, 1996; Stiling et al., 1999). In the longest field study to date, insect herbivore populations have been shown to decline markedly under elevated CO 2 (Stiling et al., 1999, 2003). Given that herbivore damage can influence subsequent foliar (Karban and Baldwin,

4 1997; Agrawal et al., 1999) and litter quality (Findlay et al., 1996), declines in herbivore density under elevated CO 2 have the potential to influence decomposition and nutrient dynamics. The quality of leaf litter is an important determinant of decomposition rates and nutrient dynamics in many systems (Aber et al., 1990; Anderson, 1991; Saxe et al., 1998; Gholz et al., 2000; Hättenschweiler and Vitousek, 2000). Components influencing the quality of detritus include nitrogen concentrations, C:N ratios, and polyphenolic concentrations. Typically, high concentrations of nitrogen are positively correlated with decomposition rates while high C:N ratios and polyphenolic concentrations are negatively correlated with decomposition rates (Hättenschweiler and Vitousek, 2000). The ultimate result is a decrease in decomposition rates leading to decreases in nitrogen mineralization, which reduces soil nitrogen availability in the ecosystem. Previous studies of the effect of elevated CO 2 on litter quality have been equivocal. Some studies have found that litter quality is negatively affected by increased levels of atmospheric CO 2, (Norby et al., 1986; Couteaux et al., 1990; Cotrufo et al., 1994; Melillo et al., 1995) while other studies have found no effect of elevated CO 2 (O Neill and Norby, 1996; King et al., 2001). While both the quality and quantity of green leaf tissue have been shown to change as a result of elevated concentrations of atmospheric CO 2 (Lincoln et al., 1993; Lindroth et al., 1995; Saxe et al., 1998), links between the quality of green leaves and subsequent litter quality under elevated CO 2 are less well established (Couteaux et al., 1991; Kemp et al., 1994; Cotrufo and Insen, 1995; Gorissen et al., 1995; Torbert et al., 1995; Robinson et al., 1997; Cotrufo et al., 1998; Peñuelas and Estiarte, 1998; Saxe et al., 1998; Ceulemans et al., 1999; King et al., 2001). In general, nitrogen concentrations in green leaves decline and C:N ratios increase under elevated CO 2 (Lincoln et al., 1993; Ceulemans and Mousseau, 1994; Lindroth et al., 1995; Wilsey, 1996; Hughes and Bazzaz, 1997). There may also be increases in phenolic and polyphenolic concentrations in green leaves under elevated CO 2 (Roth and Lindroth, 1995: Lindroth et al., 1995; Agrell et al., 2000). However, when leaves senesce, CO 2 -mediated changes in green leaf quality may not always translate into changes in litter quality. While Saxe et al. (1998) found low nitrogen concentrations and high C:N ratios in litter under elevated CO 2, King et al. (2000) found no correspondence between green-leaf and litter chemistry. Mechanisms by which insects can influence litter quality include phytochemical induction (Findlay et al., 1996) and premature leaf abscission (Kahn and Cornell, 1983, Stiling et al., 1999). Given the importance of litter chemistry to decomposition processes and nutrient dynamics (Hättenschweiler and Vitousek, 2000), it is important to determine the mechanisms by which elevated CO 2 can influence litter quality. Objectives 1) To determine the effects of elevated CO 2 on foliar chemistry. Hypothesis 1: Foliar nitrogen concentrations decline in most species under elevated CO 2 but not for the nitrogen fixing Galactia elliottii. 2) To elucidate linkages between CO 2, foliar chemistry and insect herbivore-mediated damage on litter quality.

5 Hypothesis 2: Secondary metabolites (polyphenolics and lignin) and C:N ratios are effective predictors of herbivore-mediated changes in the decomposition process under elevated CO 2 conditions. 3) To determine the effects of insect herbivore damage on decomposition processes under elevated CO 2 conditions. Hypothesis 3: Leafminer-induced greenfall is a source of high-quality litter and reduced herbivore damage due to elevated CO 2 will have a greater effect on litter quality than do the direct effects of elevated CO 2. Study Site The study site lies within a two-hectare native scrub-oak community located at Kennedy Space Center, Florida. This woody ecosystem is controlled by a natural fire return cycle of 8 12 years, and the mature canopy is 3 5 meters high. There is seasonal litter fall, high rhizosphere production and high nutrient cycling. The last burn cycle was in 1996 prior to site set up. Sixteen 3.6 meter diameter plots, each enclosed with a clear polyester film open-top chamber 3.4 m in height, are utilized to control CO 2 levels. Chambers are overlaid on an octagonal framework of PVC pipe with a removable access door and frustrum to reduce dilution of air within the chamber by outside wind. All re-growth was cut to ground level in May 1996 and, since that time, the vegetation in eight of the chambers has been exposed to almost twice ambient CO 2 (700 ppm), while the other eight chambers have been exposed to ambient levels of CO 2 (350 ppm). The CO 2 is continuously supplied, 24 hours a day. Monitoring and control of CO 2 injection into each chamber is done by infrared gas analyzes in conjunction with manually adjusted needle valves. In ambient CO 2 chambers, the airflow is identical to that of the elevated CO 2 chambers but is not supplemented with CO 2. Four study species of plants dominate this community and are present in every chamber: three oak species, Quercus myrtifolia Willd, Q. chapmanii Sargent, Q. geminata Small, and a nitrogen fixing legume, Galactia elliottii Nuthall. Methods Green Leaf Chemistry Samples of fresh (green) leaves from each of the four study species will be collected for chemical analysis. Four undamaged leaves will be removed from each of three individuals per chamber from each of the three oak (Q. myrtifolia, Q. chapmanii, and Q. geminata) species every three months. A hole punch will be used to remove two disks of leaf tissue from each leaf. One disk will be used to obtain dry weight of the leaf area while the other disk will be placed into 70/30 acetone/water with 1mM ascorbic acid in the field and used for phenolic analysis. The remaining portion of the leaf will be returned to the lab, dried, and used for C:N and fiber analysis (cellulose, hemicellulose, lignin). Because of leaf size, the collection method for G. elliottii will differ slightly. Two opposite leaflets, each from three individuals of G. elliottii, will be collected from each chamber. One leaflet will be placed in acetone to be used for phenolic analysis; the opposite leaflet will be placed in a bag and used to obtain leaf weights and, subsequently, C:N and fiber analysis. Samples from different individual plants of a given species will be pooled within chambers so that chambers (8 per treatment) act as replicates.

6 Dried leaves will be ground to a fine powder and stored -80 C prior to analysis. Percent dry weight nitrogen and carbon will be estimated from leaf powder on a Carlo-Erba NA1500 model C/N analyzer. These data will also provide estimates of foliar C:N ratios. The carbon and nitrogen analysis data will be used to test the hypothesis that foliar nitrogen concentrations decline in most species under elevated CO 2 except the nitrogen fixing Galactia elliottii. Sub-samples of leaf powder (above) will also be used to assess the effects of elevated CO 2 on foliar concentrations of cellulose, hemicellulose, and lignin by sequential neutral detergent/acid detergent digestion on an Ankom fiber analyzer (Abrahamson et al., 2003). Tannin analysis will be conducted using leaf disks collected into 70% acetone in the field. The acetone will be removed by evaporation under reduced pressure. Proanthocyanidins, an estimate of condensed tannin, will be assayed using methods described in Rossiter et al. (1988). Total phenolics will be estimated using the Folin-Denis assay (Swain, 1979), and gallotannins (hydrolysable tannins) will be estimated using a potassium iodate technique developed by Bate- Smith (1977) and modified by Schultz and Baldwin (1982). Standards for tannin analysis will be generated by multiple sequential washes of bulk samples (one for each species) by acetone extraction. All tannin assays produce colorimetric readings, in proportion to tannin concentration, which will be quantified using a BioRad microplate reader. Leaf Litter Chemistry and Decomposition Examination of the rates of leaf decomposition (including litter quality) by type of herbivory (undamaged, mined, and chewed) will be conducted to test the hypothesis that leafminer-induced greenfall is a source of high-quality litter and reduced herbivore damage due to elevated CO 2 will have a greater effect on litter quality than the direct effects of elevated CO 2. Rates of leaf decomposition will focus on litter from the most common tree in the system, Quercus myrtifolia. Litter will be collected and pooled (by chamber CO 2 treatment) from litter trays in all chambers during April-May of 2004, when litter is most plentiful. This will give six litter types (elevated CO 2 and ambient CO 2 x 3 damage types). Litterbags will be 5 cm x 4 cm x 1.5-mm mesh and will contain 5 g of litter from one of the six treatments. The bags will be laid in a series of small rings in the chamber centers. Each chamber will receive 12 bags of each treatment (n=72 bags). One bag of each type will be removed from each chamber every three months for three years from time zero to time three years. The small size of the bags means that 24 bags can be placed on the soil surface inside each ring. Three rings will be employed in each chamber as there is not enough room for more rings or bags. Each bag will be covered by a one leaf thick layer of litter, available from the forest floor in each chamber. Starting at time zero, and every three months thereafter, mass loss and litter chemistry (lignin, C, N, C:N ratio, and tannins) from each bag will be measured using the chemical methods described above. Also from litterbags, two nitrogen pools will be followed over three years of decomposition: the mineral pools (NH 4 + and NO 3 - ) and dissolved organic nitrogen (DON). These measurements will allow both the direct effects of elevated CO 2 and indirect effects mediated by herbivory on nitrogen dynamics in litter to be determined. Mineral nitrogen will be assessed from colorimetric analysis. DON will be calculated as the difference between mineral nitrogen in persulfate digested and undigested extracts.

7 Significance of Study Given the rate of atmospheric CO 2 increases (approximately 4 ppm per year), it is important to develop general predictions for modeling ecosystem processes under such environmental changes. I will be able to assess whether herbivore-mediated changes in litter quality under elevated CO 2 influence key ecosystem processes. Direct effects on plants, insects, and litter have been the focus of prior research. It is time to move forward to consider indirect effects. CO 2 influences insects, which influence plants and litter. These indirect effects have yet to be characterized but may be of considerable importance. Models that do not include indirect effects are likely to be inaccurate. My research will provide important information for integrative predictions of ecosystem response to elevated atmospheric CO 2.

8 Literature Cited Aber, J. D, J. M. Melillo, and C. A. McClaugherty Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Can. J. Bot. 68: Abrahamson, W. G. and others Cynipid gall-wasp communities correlate with oak chemistry. Journal of Chemical Ecology 29, no. 1: Agrawal, A. A., S. Y. Strauss, and M. J. Stout Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53, no. 4: Agrell, J., E. P. McDonald, and R. L. Lindroth Effects of CO 2 and light on tree phytochemistry and insect performance. Oikos 88: Akey, D. H. and B. A. Kimball Growth and development of the beet armyworm on cotton grown in an enriched carbon dioxide atmosphere. Southwest Entomologist 14: Anderson, J. M The effects of climate change on decomposition processes in grassland and coniferous forests. Ecological Applications 1, no. 3: Bate-Smith, E. C Astringent tannins of Acer species. Phytochemistry 16: Bazzaz, F. A The response of natural ecosystems to the rising global CO 2 levels. Annu. Rev. Ecol. Syst. 21: Ceulemans, R., I. A. Janssens, and M. E. Jach Effects of CO 2 enrichment on trees and forests: lessons to be learned in view of future ecosystem studies. Annals of Botany 84: Ceulemans, R. and M. Mousseau Tansley review no 71: effects of elevated atmospheric CO 2 on woody plants. New Physiologist 127: Coley, P. D. and T. M. Aide A comparison of herbivory and plant defenses in temperate and tropical broadleaved forests. Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, Editors P. W. Price and others, New York: Wiley. Cook, A. C., W. C. Oechel, and B. Sveinbjornsson Using Icelandic CO 2 springs to understand the long-term effects of elevated atmospheric CO 2. Plant Responses to Elevated CO 2 : Evidence from Natural Springs, Editors A. Raschi and others, 272. Cambridge, United Kingdom: Cambridge University Press. Cotrufo, M. F. and P. Ineson Effects of enhanced atmospheric CO 2 and nutrient supply on the quality and subsequent decomposition of fine roots of Betula pendula Roth. & Picea sitchensis (Bong.) Carr. Plant and Soil 170:

9 Cotrufo, M. F., P. Ineson, and A. P. Rowland Decomposition of tree leaf litters grown under elevated CO 2 : effect of litter quality. Plant and Soil 163: Cotrufo, M. F. and others Elevated CO 2 affects field decomposition rate and palatability of tree leaf litter : importance of changes in substrate quality. Soil Biol. Biochem. 30, no. 12: Couteaux, M. M., M. Mousseau, and M. L. Celerier Increased atmospheric CO 2 and litter quality: decomposition of sweet chestnut leaf litter with animal food webs of different complexities. Oikos 61: Couteaux, M. M Mousseau M., M. L. Celerier, and P. Bottner Increased atmospheric CO 2 and litter quality: decomposition of sweet chestnut leaf litter with animal food webs of different complexities. Oikos 61: Curtis, P. S. and others Linking above- and belowground responses to rising CO 2 in northern deciduous forest species. Carbon Dioxide and Terrestrial Ecosystems, Editors G. W. Koch and H. A. Mooney, 443. San Diego, Ca.: Academic Press, Inc. Dury, S. J. and others The effects of increasing CO 2 and temperature on oak leaf palatability and the implications for herbivorous insects. Global Change Biology 4: Fajer, E. D The effects of enriched CO2 atmospheres on plant-insect herbivore interactions: growth responses of larvae of the specialist butterfly, Junonia coenia (Lepidoptera: Nymphalidae). Oecologia 81: Fajer, E. D., M. D. Bowers, and F. A. Bazzaz The effects of enriched carbon dioxide atmospheres on plant-insect herbivore interactions. Science 243: Enriched CO 2 atmospheres and the growth of the buckeye butterfly, Junonia coenia. Ecology 72, no. 2: Feeny, P Effect of oak leaf tannins on larval growth of the winter moth Operophtera brumata. Journal of Insect Physiology 14: The evolution of chemical ecology: contributions from the study of herbivorous insects. Herbivores: Their interactions with Secondary Plant Metabolites, Editors G. Rosenthal and M. Berenbaum, San Diego, CA: Academic Press. Findlay, S. and others Effects of damage to living plants on leaf litter quality. Ecological Applications 6: Garbutt, B. K. and F. A. Bazzaz The effect of elevated CO 2 on plants. III. Flower, fruit and seed production and abortion. New Phytologist 98: Gholz, H. L. and others Long-term dynamics of pine and hardwood litter in contrasting environments: toward a global model of decomposition. Global Change Biology 6: 751-

10 65. Gorissen, A. and others Grass root decomposition is retarded when grass has been grown under elevated CO 2. Soil Biology and Biochemistry 27: Hättenschwiler, S. and P. M. Vitousek The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends in Ecology and Evolution 15: Hughes, L. and F. A. Bazzaz Effect of elevated CO 2 on interactions between the western flower thrips, Frankliniella occidentalis (Thysanoptera: thripidae) and the common milkweed, Asclepias syriaca. Oecologia 109: Ineson, P. and M. F. Cotrufo Increasing concentrations of atmospheric CO 2 and decomposition processes in forest ecosystems. Plant Responses to Elevated CO 2 : Evidence from Natural Springs, Editors A. Raschi and others, 272. Cambridge, United Kingdom: Cambridge University Press. Johnson, D. W. and J. T. Ball Interactions between CO 2 and Nitrogen in forests: can we extrapolate from the seedling to the stand level? Carbon Dioxide and Terrestrial Ecosystems, Editors G. W. Koch and H. A. Mooney, 443. San Diego, Ca.: Academic Press, Inc. Johnson, D. W. and others Effects of CO 2 and N on growth and N dynamics in Ponderosa Pine: results from the first two growing seasons. Carbon Dioxide and Terrestrial Ecosystems, Editors G. W. Koch and H. A. Mooney, 443. San Diego, Ca.: Academic Press, Inc. Kahn, M. D. and H. V. Cornell Early leaf abscission and folivores: comments and considerations. American Naturalist 122: Karban, R. and I. T. Baldwin Induced Responses to Herbivory, 319. Chicago, Illinois: The University of Chicago Press. Kemp, P. R. and others Effects of elevated CO 2 and nitrogen fertilization pretreatments on decomposition on tallgrass prairie leaf litter. Plant and Soil 165: King, J. S. and others Chemistry and decomposition of litter from Populus tremuloides Michaux grown at elevated atmospheric CO 2 and varying N availability. Global Change Biology 7: Koch, G. W. and H. A. Mooney Carbon Dioxide and Terrestrial Ecosystems, 443. San Diego, Ca.: Academic Press, Inc. Lincoln, D. E. and D. Couvet The effect of carbon supply on allocation to allelochemicals and caterpillar consumption of peppermint. Oecologia 78: Lincoln, D. E., E. D. Fajer, and R. H. Johnson Plant-insect herbivore interactions in elevated CO 2 environments. TREE 8, no. 2: 64-8.

11 Lincoln, D. E., N. Sionit, and B. R. Strain Growth and feeding response of Pseudoplusia includens (Lepidoptera: Nocuidae) to host plants grown in controlled carbon dioxide atmospheres. Environmental Entomology 13: Lindroth, R. L CO 2 -mediated changes in tree chemistry and tree-lepidoptera interactions. Carbon Dioxide and Terrestrial Ecosystems, Editors G. W. Koch and H. A. Mooney, 443. San Diego, Ca.: Academic Press, Inc. Lindroth, R. L., G. E. Arteel, and K. K. Kinney Responses of three saturniid species to paper birch grown under enriched CO 2 atmospheres. Functional Ecology 9: Lindroth, R. L., K. K. Kinney, and C. L. Platz Responses of deciduous trees to elevated atmospheric CO 2 : productivity, phytochemistry, and insect performance. Ecology 74, no. 3: Melillo, J. M. and others Global change and its effects on soil organic carbon stocks New York: John Wiley & Sons. Norby, R. J., E. G. O'Neill, and R. J. Luxmoore Effects of atmospheric CO 2 enrichment on the growth and mineral nutrition of Quercus alba in nutrient-poor soil. Plant Physiology 82: O'Neill, E. G. and R. J. Norby Litter quality and decomposition rates of foliar litter produced under CO 2 enrichment. Carbon Dioxide and Terrestrial Ecosystems, Editors G. W. Koch and H. A. Mooney, 443. San Diego, Ca.: Academic Press, Inc. Peñuelas, J. and M. Estiarte Can elevated CO 2 affect secondary metabolism and ecosystem function? TREE 12, no. 1: Price, P. W. and others Interaction among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Sys. 11: Robinson, C. H. and others Elevated atmospheric CO 2 affects decomposition of Festuca vivepara (L.) Sm. litter and roots in experiments simulating environmental change in two contrasting artic ecosystems. Global Change Biology 3: Rossiter, M. C., J. C. Schultz, and I. T. Baldwin Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69: Roth, S. K. and R. L. Lindroth Elevated atmospheric CO 2 effects on phytochemistry, insect performance and insect parasitoid interactions. Global Change Biology 1: Saxe, H., D. S. Ellsworth, and J. Heath Tansley Review No. 98 Tree and forest functioning in an enriched CO 2 Atmosphere. New Phytologist 139, no. 3: Schultz, J. C. and I. T. Baldwin Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:

12 Stiling, P. and others Decreased leaf-miner abundance in elevated CO 2 : reduced leaf quality and increased parasitoid attack. Ecological Applications 9, no. 1: Stiling, P. Moon D. C. Hunter M. D. Colson J. Rossi A. M. Hymus G. J. Drake B. G Elevated CO 2 lowers relative and absolute herbivore density across all species of a scruboak forest. Oecologia 134: Swain, T The importance of flavonoids and related compounds in fern taxonomy and ecology. Bulletin of the Torrey Botanical Club 107: Torbert, H. A., S. A. Prior, and H. H. Rogers Elevated atmospheric carbon dioxide effects on cotton plant residue decomposition. Soil Science Society of America Journal 59: Van Gardingen, P. R. and others Long-term effects of enhanced CO 2 concentrations on leaf gas exchange: research opportunities using CO 2 springs. Long-term effects of enhanced CO 2 concentrations on leaf gas exchange: research opportunities using CO 2 springs Plant Responses to Elevated CO 2 : Evidence from Natural Springs, Editors A. Raschi and others, 272. Cambridge, United Kingdom: Cambridge University Press. Williams, W. E. and others The response of plants to elevated CO 2 IV. Tow deciduousforest tree communities. Oecologia (Berlin) 69: Wilsey, B. J Plant responses to elevated atmospheric CO 2 among terrestrial biomes. Oikos 76, no. 1: Woodward, F. I. and D. J. Beerling The dynamics of vegetation change: health warnings for equilibrium 'Dodo' models. Global Ecology and Biogeography Letters 6, no. 6:

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