Abstract
Background and Aims
Future climate conditions (warmer, wetter) are expected to change aboveground plant communities with linked belowground alterations (e.g. porewater chemistry) that can influence carbon dynamics. The aims of this study were 1) to determine if porewater phenolic compound concentrations reflect the changing aboveground plant community and 2) to elucidate if changes in phenolic compounds alter belowground carbon release.
Methods
We monitored the changes in vegetation biomass, porewater phenolic compound concentrations, respired CO2 and phenol oxidase enzyme activity in 84 intact peatland mesocosms exposed to elevated atmospheric CO2, elevated temperature, and decreased water table conditions in a full factorial design.
Results
Phenolic compound concentrations were indicative of the vascular plant expansion that occurred under warmer and anaerobic conditions, suggesting that phenolic compounds could be a simple indicator of northern plant community dynamics. Ecosystem CO2 respiration increased with rising phenolic compound concentrations, suggesting that phenolic compounds can decrease microbial carbon use efficiency in northern peatlands.
Conclusions
Using an aboveground-belowground framework we present a previously unrecognized mechanism influencing northern carbon dynamics; wherein, climate change conditions can restructure the plant community composition in turn increasing porewater phenolic concentrations, which results in decreased microbial carbon use efficiency and enhanced carbon release.
Similar content being viewed by others
Abbreviations
- AB-BG:
-
Above- and belowground
- CO2 :
-
Carbon dioxide
- CH4 :
-
Methane
References
A’Bear AD, Johnson SN, Jones TH (2014) Putting the ‘upstairs–downstairs' into ecosystem service: what can aboveground–belowground ecology tell Us? Biol Control 75:97–107. doi:10.1016/j.biocontrol.2013.10.004
Aerts R, Wallén B, Malmer N, De Caluwe H (2001) Nutritional constraints on Sphagnum-growth and potential decay in northern peatlands. Journal Ecol 89:292–299. doi:10.1046/j.1365-2745.2001.00539.x
Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340. doi:10.1038/ngeo846
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. doi:10.1111/j.1365-3040.2009.01926.x
Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominated modulate the soil microbiome. J Biol Chem 288:4502–4512. doi:10.1074/jbc.M112.433300
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511. doi:10.1038/nature13855
Bellisario LM, Bubier JL, Moore TR, Chanton JP (1999) Controls on CH4 emissions from a northern peatland. Global Biogeochem Cy 13:81–91. doi:10.1029/1998GB900021
Bernard JM (1990) Life history and vegetative reproduction in Carex. Can J Bot 68:1441–1448. doi:10.1139/b90-182
Bonnett SAF, Ostle N, Freeman C (2006) Seasonal variations in decomposition processes in a valley-bottom riparian peatland. Sci Total Environ 370:561–573. doi:10.1016/j.scitotenv.2006.08.032
Box JD (1983) Investigation of the folin-ciocalteau phenol reagent for the determination of polyphenolic substances in natural waters. Water Res 17:511–525. doi:10.1016/0043-1354(83)90111-2
Bragazza L, Freeman C (2007) High nitrogen availability reduces polyphenol content in Sphagnum peat. Sci Total Environ 377:439–443. doi:10.1016/j.scitotenv.2007.02.016
Bragazza L, Parisod J, Buttler A, Bardgett RD (2013) Biogeochemical plant-soil microbe feedback in response to climate warming in peatlands. Nat Clim Chang 3:273–277. doi:10.1038/nclimate1781
Bragazza L, Bardgett RD, Mitchell EAD, Buttler A (2015) Linking soil microbial communities to vascular plant abundance along a climate gradient. New Phytol 205:1175–1182. doi:10.1111/nph.13116
Brouns K, Verhoeven JTA, Hefting MM (2014) Short period of oxygenation releases latch on peat decomposition. Sci Total Environ 481:61–68. doi:10.1016/j.scitotenv.2014.02.030
Carroll P, Crill P (1997) Carbon balance of a temperature poor fen. Global Biogeochem Cy 11:349–356. doi:10.1029/97GB01365
Cates RG, Rhoades DF (1977) Patterns in the production of antiherbivore chemical defenses in plant communities. Biochem Syst Ecol 5:185–193. doi:10.1016/0305-1978(77)90003-5
Chivers MR, Turetsky MR, Waddington JM, Harden JW, McGuire AD (2009) Effects of experimental water table and temperature manipulations on ecosystem CO2 fluxes in an Alaskan rich fen. Ecosystems 12:1329–1342. doi:10.1007/s10021-009-9292-y
Churchill AC, Turetsky MR, McGuire AD, Hollingsworth TN (2014) Response of plant community structure and primary productivity to experimental drought and flooding in an Alaskan fen. Can J For Res 45:185–193. doi:10.1139/cjfr-2014-0100
Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. doi:10.1038/nature04514
Dieleman CM, Branfireun BA, McLaughlin JW, Lindo Z (2015) Climate change drives a shift in peatland ecosystem plant community: implications for ecosystem function and stability. Glob Chang Biol 21:388–395. doi:10.1111/gcb.12643
Dorrepaal E, Cornelissen JHC, Aerts R, Wallén BO, Van Logtestijn RSP (2005) Are growth forms consistent predictors of leaf litter quality and decomposability across peatlands along a latitudinal gradient? Journal Ecol 93:817–828. doi:10.1111/j.1365-2745.2005.01024.x
Dorrepaal E, Toet S, van Logtestijn RSP, Swart E, van de Weg MJ, Callaghan TV, Aerts R (2009) Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460:616–619. doi:10.1038/nature08216
Durán N, Rosa MA, D’Annibale A, Gianfreda L (2002) Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzym Microb Technol 31:907–931. doi:10.1016/S0141-0229(02)00214-4
Eppinga M, Rietkerk M, Wassen M, De Ruiter P (2009) Linking habitat modification to catastrophic shifts and vegetation patterns in bogs. Plant Ecol 200:53–68. doi:10.1007/s11258-007-9309-6
Faubert P, Rochefort L (2002) Response of peatland mosses to burial by wind-dispersed peat. Bryologist 105:96–103. doi:10.1639/00072745(2002)105[0096:ROPMTB]2.0.CO;2
Fenner N, Freeman C (2011) Drought-induced carbon loss in peatlands. Nat Geosci 4:895–900. doi:10.1038/ngeo1323
Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280. doi:10.1038/nature06275
Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3:395–398. doi:10.1038/nclimate1796
Gomez-Casanovas N, Matamala R, Cook DR, Gonzalez-Meler MA (2012) Net ecosystem exchange modifies the relationship between the autotrophic and heterotrophic components of soil respiration with abiotic factors in prairie grasslands. Glob Chang Biol 18:2532–2545. doi:10.1111/j.1365-2486.2012.02721.x
Gorham E (1991) Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl 1:182–195. doi:10.2307/1941811
Griffis TJ, Black TA, Gaumont-Guay D, Drewitt GB, Nesic Z, Barr AG, Morgenstern K, Kljun N (2004) Seasonal variation and partitioning of ecosystem respiration in a southern boreal aspen forest. Agric For Meteorol 125:207–223. doi:10.1016/j.agrformet.2004.04.006
Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211. doi:10.2307/1942661
IPCC (2013) The Physical Science Basis. In: Stocker TF, Qin D, Plattner G, MMB T, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) In: Climate Change 2014: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jassey VEJ, Chiapusio G, Binet P, Buttler A, Laggoun-Défarge F, Delarue F, Bernard N, Mitchell EAD, Toussaint M, Francez A, Gilbert D (2013) Above- and belowground linkages in Sphagnum peatland: climate warming affects plant-microbial interactions. Glob Chang Biol 19:811–823. doi:10.1111/gcb.12075
Joanisse GD, Bradley RL, Preston CM, Munson AD (2007) Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia. New Phytol 175:535–546. doi:10.1111/j.1469-8137.2007.02113.x
Kanerva S, Kitunen V, Loponen J, Smolander A (2008) Phenolic compounds and terpenes in soil organic horizon layers under silver birch, Norway spruce and scots pine. Biol Fertil Soils 44:547–556. doi:10.1007/s00374-007-0234-6
Kang H, Freeman C, Ashendon TW (2001) Effects of elevated CO2 on fen peat biogeochemistry. Sci Total Environ 279:45–50. doi:10.1016/S0048-9697(01)00724-0
Mason H (1948) The chemistry of melanin: III. mechanism of the oxidation of dihydroxyphenylalanine by trosinase. J Biol Chem 172:83–99
Meier C, Bowman W (2008) Phenolic-rich leaf carbon fractions differentially influence microbial respiration and plant growth. Oecologia 158:95–107. doi:10.1007/s00442-008-1124-9
Min K, Freeman C, Kang H (2015) The regulation by phenolic compounds of soil organic matter dynamics under a changing environment. Bio Med Res Int:Article ID 825098
Moore TR, Bubier JL, Frolking SE, Lafleur PM, Roulet NT (2002) Plant biomass and production and CO2 exchange in an ombrotrophic bog. J Ecol 90:25–36. doi:10.1046/j.0022-0477.2001.00633.x
Pind A, Freeman C, Lock MA (1994) Enzymic degradation of phenolic materials in peatlands — measurement of phenol oxidase activity. Plant Soil 159:227–231. doi:10.1007/BF00009285
Quin SLO, Artz RRE, Coupar AM, Woodin SJ (2015) Calluna vulgaris-dominated upland heathland sequesters more CO2 annually than grass-dominated upland heathland. Sci Total Environ 505:740–747. doi:10.1016/j.scitotenv.2014.10.037
Robroek BJM, Jassey VEJ, Kox MAR, Berendsen RL, Mills RTE, Cécillon L, Puissant J, Meima-Franke M, Bakker PAHM, Bodelier PLE (2015) Peatland vascular plant functional types affect methane dynamics by altering microbial community structure. J Ecol doi:. doi:10.1111/1365-2745.12413
Stevnbak K, Scherber C, Gladbach DJ, Beier C, Mikkelsen TN, Christensen S (2012) Interactions between above- and belowground organisms modified in climate change experiments. Nat Clim Chang 2:805–808. doi:10.1038/nclimate1544
Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem Cy 23:1–11. doi:10.1029/2008GB003327
Toberman H, Laiho R, Evans CD, Artz RRE, Fenner N, Straková P, Freeman C (2010) Long-term drainage for forestry inhibits extracellular phenol oxidase activity in Finnish boreal mire peat. Eur J Soil Sci 61:950–957. doi:10.1111/j.1365-2389.2010.01292.x
Treat CC, Wollheim WM, Varner RK, Grandy AS, Talbot J, Frolking S (2014) Temperature and peat type control CO2 and CH4 production in Alaskan permafrost peats. Glob Chang Biol 20:2674–2686. doi:10.1111/gcb.12572
Tsuneda A, Thormann MN, Currah RS (2001) Modes of cell-wall degradation of Sphagnum fuscum by acremoniumcf. curvulum and Oidiodendronmaius. Can J Bot 79:93–100. doi:10.1139/b00-149
Updegraff K, Bridgham SD, Pastor J, Weishampel P, Harth C (2001) Response of CO2 and CH4 emissions from peatlands to warming and water table manipulation. Ecol Appl 11:311–326. doi:10.1890/1051-0761(2001)011[0311:ROCACE]2.0.CO;2
Walker T, Ward S, Ostle N, Bardgett R (2015) Contrasting growth responses of dominant peatland plants to warming and vegetation composition. Oecologia 178:141–151. doi:10.1007/s00442-015-3254-1
Wang H, Richardson CJ, Ho M (2015) Dual controls on carbon loss during drought in peatlands. Nat Clim Chang 5:584–587. doi:10.1038/nclimate2643
Ward S, Ostle N, Oakley S, Quirk H, Henrys PA, Bardgett RD (2013) Warming effects on greenhouse gas fluxes in peatlands are modulated by vegetation composition. Ecol Lett 16:1285–1293. doi:10.1111/ele.12167
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633. doi:10.1126/science.1094875
Wardle DA, Jonsson M, Bansal S, Bardgett RD, Gundale MJ, Metcalfe DB (2012) Linking vegetation change, carbon sequestration and biodiversity: insights from island ecosystems in a long-term natural experiment. J Ecol 100:16–30. doi:10.1111/j.1365-2745.2011.01907.x
Williams C, Shingara E, Yavitt J (2000) Phenol oxidase activity in peatlands in New York state: response to summer drought and peat type. Wetlands 20:416–421. doi:10.1672/0277-5212(2000)020[0416:POAIPI]2.0.CO;2
Acknowledgments
We are grateful to Dr. C. Dean, Dean of the Western Faculty of Science for supporting our use of the Biotron, funding from the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant program (ZL, BB), Canada Research Chairs program (BB), NSERC Strategic Network support to the Canada Network for Aquatic Ecosystem Services (BB), Ontario Ministry of Natural Resources' Far North and Science and Research Branches (JM) and the Ontario Graduate Scholarship program (CD). We thank the numerous volunteers and work study students for their help, especially Aaron Craig, Camille Chemali, Nivetitha Erampamoorthy, Rebecca Doyle, Jeff Warner, Zach Moore, Caterina Carvalhal, Naryan Chattergoon, and Lucas Albano. Discussion with Greg Thorn and Asma Asemaninejad Hassankiadeh were appreciated. Additional thanks to Dr. H. Henry for technical advice on the phenol oxidase assay.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Zucong Cai.
Electronic supplementary material
Supplementary Table S1
(DOCX 12 kb)
Rights and permissions
About this article
Cite this article
Dieleman, C.M., Branfireun, B.A., McLaughlin, J.W. et al. Enhanced carbon release under future climate conditions in a peatland mesocosm experiment: the role of phenolic compounds. Plant Soil 400, 81–91 (2016). https://doi.org/10.1007/s11104-015-2713-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-015-2713-0