Abstract
Anthropogenic activities are altering levels of atmospheric carbon dioxide (CO2) and tropospheric ozone (O3). These changes can alter phytochemistry, and in turn, influence ecosystem processes. We assessed the individual and combined effects of elevated CO2 and O3 on the phytochemical composition of two tree species common to early successional, northern temperate forests. Trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) were grown at the Aspen FACE (Free-Air Carbon dioxide and ozone Enrichment) facility under four combinations of ambient and elevated CO2 and O3. We measured, over three years (2006–08), the effects of CO2 and O3 on a suite of foliar traits known to influence forest functioning. Elevated CO2 had minimal effect on foliar nitrogen and carbohydrate levels in either tree species, and increased synthesis of condensed tannins and fiber in aspen, but not birch. Elevated O3 decreased nitrogen levels in both tree species and increased production of sugar, condensed tannins, fiber, and lignin in aspen, but not birch. The magnitude of responses to elevated CO2 and O3 varied seasonally for both tree species. When co-occurring, CO2 offset most of the changes in foliar chemistry expressed under elevated O3 alone. Our results suggest that levels of CO2 and O3 predicted for the mid-twenty-first century will alter the foliar chemistry of northern temperate forests with likely consequences for forest community and ecosystem dynamics.
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Ainsworth EA, Yendrek CR, Sitch S, Collins WJ, Emberson LD (2012) The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu Rev Plant Biol 63:637–661
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Bidart-Bouzat MG, Imeh-Nathaniel A (2008) Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol 50:1339–1354
Boeckler GA, Gershenzon J, Unsicker SB (2011) Salicinoids of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509
Bortier K, Ceulemans R, de Temmerman L (1999) Effects of tropospheric ozone on woody plants. In: Agrawal SB, Agrawal M (eds) Environmental pollution and plant responses. CRC Press, Boca Raton, pp. 153–182
Cabané M, Pireaxu J-C, Léger E, Weber E, Dizengremel P, Pollet B, Lapieree C (2004) Condensed lignins are synthesized in poplar leaves exposed to ozone. Plant Physiol 134:586–594
Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver AJ, Wehner M (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Couture JJ, Lindroth RL (2012) Atmospheric change alters performance of an invasive forest insect. Glob Chang Biol 18:3543–3557
Couture JJ, Lindroth RL (2013) Impacts of atmospheric change on forest-arthropod interactions. In: Matyssek R, Clarke N, Cudlin P, Mikkelsen J-P, Weiser G, Paoletti E (eds) Climate change, air pollution and global challenges: understanding and solutions from forest research. Elsevier, Netherlands, pp. 227–248
Couture JJ, Meehan TD, Lindroth RL (2012) Atmospheric change alters foliar quality of host trees and performance of two outbreak insect species. Oecologia 168:863–876
Couture JJ, Holeski LM, Lindroth RL (2014) Impacts of long-term exposure to elevated CO2 and O3 on aspen foliar chemistry across multiple developmental stages. Plant Cell Environ 37:758–765
Couture JJ, Meehan TD, Kruger EL, Lindroth RL (2015) Insect herbivory alters the impacts of atmospheric change on northern temperate forest. Nat Plants 15016. doi:10.1038/nplants.2015.16
Dickson RE, Lewin KF, Isebrands JG, Coleman MD, Heilman WE, Riemenschneider DE, Sober J, Host GE, Zak DR, Pregitzer KS, Karnosky DF (2000) Forest atmosphere carbon transfer storage-II (FACTS II) - the aspen free-air CO2 and O3 enrichment (FACE) project: An overview. Gen Tech Rep NC-214. USDA Forest Service, North Central Research Station, Rhinelander, WI
Drake JE, Gallet-Budynek A, Hofmockel KS, Bernhardt ES, Bilings SA, Jackson RB, Johnsen KS, Lichter J, McCarthy HR, McCormack ML, Moore DJP, Oren R, Palmroth S, Philips RP, Pippen JS, Pritchard SG, Treseder KK, Schlesinger WH, DeLucia EH, Finzi AC (2011) Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2. Ecol Lett 14:349–357
Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Glob Chang Biol 10:2121–2138
Filion M, Dutilleul P, Potvin C (2000) Optimum experimental design for free-air carbon dioxide enrichment (FACE) studies. Glob Chang Biol 6:843–854
Finzi A, Norby R, Carlo C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Iversen CM, Jackson RB, Kubiske ME, Ledford J, Liberloo M, Oren R, Polle A, Pritchard S, Zak DR, Schlesinger WH, Ceulemans R (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci U S A 104:14014–14019
Fowler D, Cape JN, Coyle M, Flechard C, Kuylenstierna J, Hicks K, Derwent D, Johnson C, Stevenson D (1999) The global exposure of forests to air pollutants. Water Air Soil Pollut 116:5–32
Hagerman AE, Riedl KM, Jones GA, Sovik KN, Ritchard NT, Hartzfeld PW, Riechel TL (1997) High molecular weight polyphenolics (tannins) as antioxidants. J Agric Food Chem 46:1887–1892
Hartmann DL, AMG KT, Rusticucci M, Alexander LV, Brönnimann S, Charabi Y, Dentener FJ, Dlugokencky EJ, Easterling DR, Kaplan A, Soden BJ, Thorne PW, Wild M, Zhai PM (2013) Observations: atmosphere and surface. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Holton MK, Lindroth RL, Nordheim EV (2003) Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2 and O3. Oecologia 137:233–244
IPCC, (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Core Writing Team, Pachauri RK, Reisinger A (eds) IPCC, Geneva 104 pp
Karnosky DF, Podila GK, Gagnon Z, Pechter P, Akkapeddi A, Sheng Y, Riemenschneider DE, Coleman MD, Dickson RE, Isebrands JG (1998) Genetic control of responses to interacting tropospheric ozone and CO2 in Populus tremuloides. Chemosphere 36:807–812
Kopper BJ, Lindroth RL (2003) Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103
Koricheva J (1999) Interpreting phenotypic variation in plant allelochemistry: problems with the use of concentrations. Oecologia 119:467–473
Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411
Kubiske ME, Quinn VS, Marquardt PE, Karnosky DF (2007) Effects of elevated atmospheric CO2 and/or O3 on intra- and interspecific competitive ability of aspen. Plant Biol 9:342–355
Lavola A, Julkunen-Tiitto R, Pääkkönen E (1994) Does ozone stress change the primary or secondary metabolites of birch (Betula pendula Roth)? New Phytol 126:637–642
Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21
Lindroth RL (2012) Atmospheric change, plant secondary metabolites and ecological interactions. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp. 120–153
Lindroth RL, Hwang S-H (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In: Romeo JT, Saunders JA, Barbosa P (eds) Recent advances in phytochemistry: phytochemical diversity and redundancy in ecological interactions. Plenum Press, New York, pp. 26–51
Lindroth RL, Hsia MTS, Scriber JM (1987) Seasonal patterns in the phytochemistry of three Populus species. Biochem Sys Ecol 15:681–686
Lindroth RL, Scriber JM, Hsia MTS (1988) Chemical ecology of the tiger swallowtail: mediation of host use by salicinoids. Ecology 69:814–822
Lindroth RL, Kopper BJ, Parsons WFJ, Bockheim JG, Karnosky DF, Hendry GF, Pregitzer KS, Isebrands JG, SoberJ (2001) Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environ Pollut 115:395–404
Lindroth RL, Osier TL, Wood SA, Barnhill HRA (2002) Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochem Syst Ecol 30:297–307
Liu L, King JS, Giardina CP (2005) Effects of elevated concentrations of atmospheric CO2 and tropospheric O3 on leaf litter production and chemistry in trembling aspen and paper birch. Tree Physiol 25:1151–1522
Long SP, Ainsworth EA, Rogers A, Ort DA (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annu Rev Plant Biol 55:591–628
Meehan TD, Couture JJ, Bennett AE, Lindroth RL (2014) Herbivore-mediated materials fluxes in northern deciduous forests under elevated carbon dioxide and ozone concentrations. New Phytol 204:397–407
Norby RJ, DeLucia EH, Gielen B, Calfapietra C, Giardina CP, King JS, Ledford J, McCarthy HR, Moore DJP, Ceulmans R, De Angelis P, Finzi AC, Karnosky DF, Kubiske ME, Lukac M, Pregitzer KS, Scarascia-Mugnozza GE, Schlesinger WH, Oren R (2005) Forest response to elevated CO2 is conserved across a broad range of productivity. Proc Natl Acad Sci U S A 102:18052–18056
Oksanen E (2003) Physiological responses of birch (Betula pendula) to ozone: a comparison between open-soil-grown trees exposed for six growing seasons and potted seedlings exposed for one season. Tree Physiol 23:603–614
Oksanen E, Riikonen J, Kaakinen S, Holopainen T, Vapaavuori E (2005) Structural characteristics and chemical composition of birch (Betula pendula) leaves are modified by increasing CO2 and ozone. Glob Chang Biol 11:732–748
Parsons WFJ, Brockheim JG, Lindroth RL (2008) Independent, interactive, and species-specific responses of leaf litter decomposition to elevated CO2 and O3 in a northern hardwood forest. Ecosystems 11:505–519
Phillips RP, Finzi AC, Bernhardt ES (2012) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194
Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230
Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant-arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336
Rowland AP, Roberts JD (1994) Lignin and cellulose fractionation in decomposition studies using acid-detergent fiber methods. Commun Soil Sci Plant Anal 25:269–277
Rubert-Nason KF, Holeski LM, Couture JJ, Gusse A, Undersander DJ, Lindroth RL (2013) Rapid phytochemical analysis of birch (Betula) and poplar (Populus) foliage by near-infrared reflectance spectroscopy. Anal Bioanal Chem 405:1333–1344
Talhelm AF, Pregitzer KS, Kubiske ME, Zak DR, Campany CE, Burton AJ, Dickson RE, Hendry GE, Isebrands JG, Lewin KF, Nagy J, Karnosky DF (2014) Elevated carbon dioxide and ozone alter productivity and ecosystem carbon content in northern temperate forests. Glob Chang Biol 8:2492–2504
Valkama E, Koricheva J, Oksanen E (2007) Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Chang Biol 13:184–201
Veteli TO, Mattson WJ, Niemelä P, Julkunen-Tiitto R, Kellomäki S, Kuokkanen K, Lavola A (2007) Do elevated temperature and CO2 generally have counteracting effects on phenolic phytochemistry of boreal trees? J Chem Ecol 33:287–296
Vigue LM, Lindroth RL (2010) Effects of genotype, elevated CO2 and elevated O3 on aspen phytochemistry and aspen leaf beetle Chrysomela crotchi performance. Agric For Entomol 12:267–276
Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Front Ecol Environ 5:475–482
Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14:1220–1226
Acknowledgements
We thank A. Gusse for assistance with phytochemical analysis via NIRS, P. A. Townsend for support to JJC during the writing of this manuscript, and multiple undergraduate students for their extensive field and laboratory assistance. Aspen FACE was supported principally by the Office of Science (BER), US Department of Energy, Grant No. DE-FG02-95ER62125 to Michigan Technological University, and Contract No. DE-AC02-98CH10886 to Brookhaven National Laboratory, the US Forest Service Northern Global Change Program and North Central Research Station, Michigan Technological University, and Natural Resources Canada – Canadian Forest Service. This work was supported by U.S. Department of Energy (Office of Science, BER) grant DE-FG02-06ER64232 and University of Wisconsin Hatch grant WIS04898 to RLL and USDA NIFA AFRI Fellowship grant 2012-67012-19900 to JJC.
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Couture, J.J., Meehan, T.D., Rubert-Nason, K.F. et al. Effects of Elevated Atmospheric Carbon Dioxide and Tropospheric Ozone on Phytochemical Composition of Trembling Aspen ( Populus tremuloides ) and Paper Birch ( Betula papyrifera ) . J Chem Ecol 43, 26–38 (2017). https://doi.org/10.1007/s10886-016-0798-4
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DOI: https://doi.org/10.1007/s10886-016-0798-4