Abstract
Aims
Photodegradation of senescent plant material has been identified as an important vector of aboveground carbon (C) loss in aridland ecosystems, but the consequences for biotic activity and soil C in the field are not well understood.
Methods
We established an experiment in a semiarid woodland in Patagonia, Argentina with attenuation of solar radiation and additions of leaf litter to evaluate impacts of photodegradation on changes in labile C and biotic activity in aboveground litter and surface soils.
Results
Litter decomposition was significantly accelerated by exposure to solar radiation. Moreover, labile sugars (hexoses and pentoses), microbial enzymatic activity (β-glucosidase activity) and available carbohydrates for cellulase degradation (saccharification) all significantly increased in sunlight-exposed litter. None of these stimulatory effects were observed in the surface soils exposed to sunlight. On the contrary, soil microbial biomass and β-glucosidase activity in surface soils were significantly greater only with litter addition and attenuated sunlight.
Conclusions
Our results suggest that photodegradation of plant litter (production of volatile compounds through photochemical mineralization) and photofacilitation (stimulation of biotic activity due to change in litter chemistry with exposure to sunlight) generate rapid turnover of C in aboveground litter. The consequences of this accelerated C turnover may be that a fraction of leaf litter decomposes and is directly released back to the atmosphere as CO2 and never enters soil organic matter pool. Taken together, these results highlight the functional importance of solar radiation in determining the C balance in semiarid ecosystems.
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References
Adair EC, Parton WJ, King JY, Brandt LA, Lin Y (2017) Accounting for photodegradation dramatically improves prediction of carbon losses in dryland systems. Ecosphere 8. https://doi.org/10.1002/ecs2.1892
Almagro M, Maestre FT, Martínez-López J, Valencia E, Rey A (2015) Climate change may reduce litter decomposition while enhancing the contribution of photodegradation in dry perennial Mediterranean grasslands. Soil Biol Biochem 90:214–223. https://doi.org/10.1016/j.soilbio.2015.08.006
Almagro M, Martínez-López J, Maestre FT, Rey A (2017) The contribution of photodegradation to litter decomposition in semiarid Mediterranean grasslands depends on its interaction with local humidity conditions, litter quality and position. Ecosystems 20:527–542. https://doi.org/10.1007/s10021-016-0036-5
Araujo PI (2012) Impactos de las plantaciones de pino sobre el ciclo de carbono a lo largo de un gradiente de precipitaciones en la Patagonia, Argentina. Faculty of Agronomy. University of Buenos Aires, Buenos Aires
Araujo PI, Austin AT (2015) A shady business: pine afforestation alters the primary controls on litter decomposition along a precipitation gradient in Patagonia, Argentina. J Ecol 103:1408–1420
Austin AT (2011) Has water limited our imagination for aridland biogeochemistry? Trends Ecol Evol 26:229–235
Austin AT, Ballaré CL (2010) Dual role of lignin in plant litter decomposition in terrestrial ecosystems. Proc Natl Acad Sci U S A 107:4618–4622. https://doi.org/10.1073/pnas.0909396107
Austin AT, Sala OE (2002) Carbon and nitrogen dynamics across a natural gradient of precipitation in Patagonia, Argentina. J Veg Sci 13:351–360
Austin AT, Vivanco L (2006) Plant litter decomposition in a semiarid ecosystem controlled by photodegradation. Nature 442:555–558
Austin AT, Méndez MS, Ballaré CL (2016) Photodegradation alleviates the lignin bottleneck for carbon turnover in terrestrial ecosystems. Proc Natl Acad Sci U S A 113:4392–4397. https://doi.org/10.1073/pnas.1516157113
Bai Y, Wu J, Xing Q, Pan Q, Huang J, Yang D, Han X (2008) Primary production and rain use efficiency across a precipitation gradient on the Mongolia plateau. Ecology 89:2140–2153
Baker NR, Allison SD (2015) Ultraviolet photodegradation facilitates microbial litter decomposition in a Mediterranean climate. Ecology 96:1994–2003. https://doi.org/10.1890/14-1482.1
Ball BA, Christman MP, Hall SJ (2019) Nutrient dynamics during photodegradation of plant litter in the Sonoran Desert. J Arid Environ 160:1–10. https://doi.org/10.1016/j.jaridenv.2018.09.004
Barnes PW, Throop HL, Hewins DB, Abbene ML, Archer SR (2012) Soil coverage reduces photodegradation and promotes the development of soil-microbial films on dryland leaf litter. Ecosystems 15:311–321
Barnes P, Throop H, Archer S, Breshears D, McCulley R, Tobler M (2015) Sunlight and soil–litter mixing: drivers of litter decomposition in drylands. In: Beyschlag W (ed) U Lüttge. Springer International Publishing, Progress in Botany, pp 273–302
Berenstecher P, Gangi D, González-Arzac A, Martínez ML, Chaves EJ, Mondino EA, Austin AT (2017) Litter microbial and soil faunal communities stimulated in the wake of a volcanic eruption in a semi-arid woodland in Patagonia, Argentina. Funct Ecol 31:245–259. https://doi.org/10.1111/1365-2435.12683
Bonan GB, Doney SC (2018) Climate, ecosystems, and planetary futures: the challenge to predict life in earth system models. Science 359:eaam8328
Bosco T, Bertiller MB, Carrera AL (2016) Combined effects of litter features, UV radiation, and soil water on litter decomposition in denuded areas of the arid Patagonian Monte. Plant Soil 406:71–82. https://doi.org/10.1007/s11104-016-2864-7
Brandt LA, King JY, Milchunas DG (2007) Effects of ultraviolet radiation on litter decomposition depend on precipitation and litter chemistry in a shortgrass steppe ecosystem. Glob Chang Biol 13:2193–2205
Brandt LA, Bohnet C, King JY (2009) Photochemically induced carbon dioxide production as a mechanism for carbon loss from plant litter in arid ecosystems. J Geophys Res-Biogeosci 114:G02004. https://doi.org/10.1029/2008JG000772
Brandt LA, King JY, Hobbie SE, Milchunas DG, Sinsabaugh RL (2010) The role of photodegradation in surface litter decomposition across a grassland ecosystem precipitation gradient. Ecosystems 13:765–781
Chantigny MH, Angers DA, Kaiser K, Kalbitz K (2008) Extraction and characterization of dissolved organic matter. In: MR Carter, EG Gergorich (eds) Soil sampling and methods of analysis, pp 617–635
Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761
Chen M, Parton WJ, Adair EC, Asao S, Hartman MD, Gao W (2016) Simulation of the effects of photodecay on long-term litter decay using DayCent. Ecosphere 7. https://doi.org/10.1002/ecs2.1631
Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995. https://doi.org/10.1111/gcb.12113
Day TA, Guénon R, Ruhland CT (2015) Photodegradation of plant litter in the Sonoran Desert varies by litter type and age. Soil Biol Biochem 89:109–122. https://doi.org/10.1016/j.soilbio.2015.06.029
Day TA, Bliss MS, Tomes AR, Ruhland CT, Guénon R (2018) Desert leaf litter decay: coupling of microbial respiration, water-soluble fractions and photodegradation. Glob Chang Biol 24:5454–5470. https://doi.org/10.1111/gcb.14438
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
Erdenebileg E, Ye X, Wang C, Huang Z, Liu G, Cornelissen JH (2018) Positive and negative effects of UV irradiance explain interaction of litter position and UV exposure on litter decomposition and nutrient dynamics in a semi-arid dune ecosystem. Soil Biol Biochem 124:245–254
Etchevehere P, Dimitri M (1972) Los suelos de la región andinopatagónica. In: Dimitri M (ed) Sinopsis general Colección Científica del INTA Buenos Aires. INTA, Buenos Aires, pp 83–95
Fellman JB, Petrone KC, Grierson PF (2013) Leaf litter age, chemical quality, and photodegradation control the fate of leachate dissolved organic matter in a dryland river. J Arid Environ 89:30–37. https://doi.org/10.1016/j.jaridenv.2012.10.011
Foereid B, Bellarby J, Meier-Augenstein W, Kemp H (2010) Does light exposure make plant litter more degradable? Plant Soil 333:275–285
Foereid B, Zarov EA, Latysh IM, Filippov IV, Lapshina ED (2018) Photo-exposure affects subsequent peat litter decomposition. Geoderma 315:104–110. https://doi.org/10.1016/j.geoderma.2017.10.059
Frank D, Reichstein M, Bahn M, Thonicke K, Frank D, Mahecha MD, Smith P, Van der Velde M, Vicca S, Babst F (2015) Effects of climate extremes on the terrestrial carbon cycle: concepts, processes and potential future impacts. Glob Chang Biol 21:2861–2880
Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store: a shortage of oxygen locks up carbon in peatlands by restraining a single enzymes. Nature 409:149
Gallo ME, Porras-Alfaro A, Odenbach KJ, Sinsabaugh RL (2009) Photoacceleration of plant litter decomposition in an arid environment. Soil Biol Biochem 41:1433–1441
Gaxiola A, Armesto JJ (2015) Understanding litter decomposition in semiarid ecosystems: linking leaf traits, UV exposure and rainfall variability. Front Plant Sci 6:140. https://doi.org/10.3389/fpls.2015.00140
Gliksman D, Rey A, Seligmann R, Dumbur R, Sperling O, Navon Y, Haenel S, De Angelis P, Arnone JA, Grünzweig JM (2017) Biotic degradation at night, abiotic degradation at day: positive feedbacks on litter decomposition in drylands. Glob Chang Biol 23:1564–1574. https://doi.org/10.1111/gcb.13465
Gliksman D, Haenel S, Grünzweig JM (2018a) Biotic and abiotic modifications of leaf litter during dry periods affect litter mass loss and nitrogen loss during wet periods. Funct Ecol 32:831–839. https://doi.org/10.1111/1365-2435.13018
Gliksman D, Navon Y, Dumbur R, Haenel S, Grünzweig JM (2018b) Higher rates of decomposition in standing vs. surface litter in a Mediterranean ecosystem during the dry and the wet seasons. Plant Soil 428:427–439. https://doi.org/10.1007/s11104-018-3696-4
Gonzalez-Polo M, Austin AT (2009) Spatial heterogeneity provides organic matter refuges for soil microbial activity in the Patagonian steppe, Argentina. Soil Biol Biochem 41:1348–1351
Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100
Harmon ME, Nadelhoffer KJ, Blair JM (1999) Measuring decomposition, nutrient turnover, and stores in plant litter. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, Oxford, pp 202–240
Henry HAL, Brizgys K, Field CB (2008) Litter decomposition in a California annual grassland: interactions between photodegradation and litter layer thickness. Ecosystems 11:545–554
Hess LJT, Austin AT (2014) Pinus ponderosa alters nitrogen dynamics and diminishes the climate footprint in natural ecosystems of Patagonia. J Ecol 102:610–621. https://doi.org/10.1111/1365-2745.12228
Hewins DB, Archer SR, Okin GS, McCulley RL, Throop HL (2013) Soil–litter mixing accelerates decomposition in a Chihuahuan desert grassland. Ecosystems 16:183–195. https://doi.org/10.1007/s10021-012-9604-5
Hewins DB, Sinsabaugh RL, Archer SR, Throop HL (2017) Soil–litter mixing and microbial activity mediate decomposition and soil aggregate formation in a sandy shrub-invaded Chihuahuan Desert grassland. Plant Ecol 218:459–474. https://doi.org/10.1007/s11258-017-0703-4
Hewins DB, Lee H, Barnes PW, McDowell NG, Pockman WT, Rahn T, Throop HL (2019) Early exposure to UV radiation overshadowed by precipitation and litter quality as drivers of decomposition in the northern Chihuahuan Desert. PLoS ONE 14:e0210470. https://doi.org/10.1371/journal.pone.0210470
Houghton R, Nassikas AA (2017) Global and regional fluxes of carbon from land use and land cover change 1850–2015. Glob Biogeochem Cycles 31:456–472
Huang G, Zhao HM, Li Y (2017) Litter decomposition in hyper-arid deserts: Photodegradation is still important. Sci Total Environ 601-602:784–792. https://doi.org/10.1016/j.scitotenv.2017.05.213
Kéfi S, Rietkerk M, Alados CL, Pueyo Y, Papanastasis VP, ElAich A, de Ruiter PC (2007) Spatial vegetation patterns and imminent desertification in Mediterranean arid ecosystems. Nature 449:213–217
King J, Brandt L, Adair E (2012) Shedding light on plant litter decomposition: advances, implications and new directions in understanding the role of photodegradation. Biogeochem 111:57–81
Lee H, Rahn T, Throop H (2012) An accounting of C-based trace gas release during abiotic plant litter degradation. Glob Chang Biol 18:1185–1195
Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68. https://doi.org/10.1038/nature16069
Licata JA, Gyenge JE, Fernandez ME, Schlichter TA, Bond BJ (2008) Increased water use by ponderosa pine plantations in northwestern Patagonia, Argentina compared with native forest vegetation. For Ecol Manag 255:753–764
Lieth H (1975) Modeling the primary productivity of the world. In: Lieth H, Whittaker RH (eds) Primary productivity of the biosphere. Springer, Berlin Heidelberg New York, pp 237–263
Lin Y, King JY (2014) Effects of UV exposure and litter position on decomposition in a California grassland. Ecosystems 17:158–168
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428
Muldavin EH, Moore DI, Collins SL, Wetherill KR, Lightfoot DC (2008) Aboveground net primary production dynamics in a northern Chihuahuan Desert ecosystem. Oecologia 155:123–132
Paruelo J, Lauenroth WK (1995) Regional patterns of normalized difference vegetation index in north American shrublands and grasslands. Ecology 76:1888–1898
Paul EA, Harris D, Klug MJ, Ruess RW (1999) The determination of microbial biomass. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, Oxford, pp 291–317
Predick KI, Archer SR, Aguillon SM, Keller DA, Throop HL, Barnes PW (2018) UV-B radiation and shrub canopy effects on surface litter decomposition in a shrub-invaded dry grassland. J Arid Environ 157:13–21. https://doi.org/10.1016/j.jaridenv.2018.06.007
Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochem 101:133–149
Raich JW, Russell AE, Vitousek PM (1997) Primary productivity and ecosystem development along an elevational gradient on Mauna Loa, Hawai'i. Ecology 78:707–721
Rozema J, Tosserams M, Nelissen HJM, van Heerwaarden L, Broekman RA, Flierman N (1997) Stratospheric ozone reduction and ecosystem processes: enhanced UV-B radiation affects chemical quality and decomposition of leaves of the dune grassland species Calamagrostis espigeios. Plant Ecol 128:284–294
Rutledge S, Campbell DI, Baldocchi D, Schipper LA (2010) Photodegradation leads to increased CO2 losses from terrestrial organic matter. Glob Chang Biol 16:3065–3074
Sala OE, Parton WJ, Joyce LA, Lauenroth WK (1988) Primary production of the central grassland region of the United States. Ecology 69:40–45
Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77:364–374
Schlesinger WH, Belnap J, Marion GM (2009) On carbon sequestration in desert ecosystems. Glob Chang Biol 15:1488–1490
Selig M, Weiss N, Ji Y (2008) Enzymatic saccharification of lignocellulosic biomass. Laboratory Analytical Procedure (LAP). Golden: National Renewable Energy Laboratory NREL/TP-510-42629
Sinsabaugh RL, Klug MJ, Collins HP, Yeager PE, Petersen SO (1999) Characterizing soil microbial communities. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, Oxford, pp 318–348
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. University of California Press, Berkeley
Uselman SM, Snyder KA, Blank RR, Jones TJ (2011) UVB exposure does not accelerate rates of litter decomposition in a semi-arid riparian ecosystem. Soil Biol Biochem 43:1254–1265
van Hees PA, Jones DL, Finlay R, Godbold DL, Lundström US (2005) The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13
Van Soest PJ (1963) Use of detergents in analysis of fibrous feeds II: a rapid method for the determination of fiber and lignin. Assoc Offi Analyt Chemists 46:829–835
Vance ED, Brookes PC (1987) An extraction method for measuring soil microbial biomass. Soil Biol Biochem 19:703–707
Vanderbilt K, White C, Hopkins O, Craig J (2008) Aboveground decomposition in arid environments: results of a long-term study in Central New Mexico. J Arid Environ 72:696–709
Vivanco L, Austin AT (2008) Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J Ecol 96:727–736
Wang J, Liu L, Wang X, Chen Y (2015) The interaction between abiotic photodegradation and microbial decomposition under ultraviolet radiation. Glob Chang Biol 21:2095–2104. https://doi.org/10.1111/gcb.12812
Wang J, Liu L, Wang X, Yang S, Zhang B, Li P, Qiao C, Deng M, Liu W (2017) High night-time humidity and dissolved organic carbon content support rapid decomposition of standing litter in a semi-arid landscape. Funct Ecol 31:1659–1668. https://doi.org/10.1111/1365-2435.12854
Acknowledgments
We thank A. González-Arzac, J. Moyano and L. Morillas-Vinuales for field and laboratory assistance in Patagonia and Buenos Aires. Financial support came from the University of Buenos Aires (UBACyT), Agencia Nacional de Promoción Científica y Tecnológica (PICT 2013-0148, PICT 2015-1231, PICT 2016-1780) of Argentina, the New Phytologist Trust and the L’Oréal-UNESCO Program for Women in Science. We sincerely thank H. Brockerof of the Estancia San Jorge for permission to establish study sites on their property. L. Vivanco and C.L. Ballaré provided helpful discussions and comments regarding the project. We thank three anonymous reviewers who contributed constructive criticism on an earlier version of this manuscript.
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AA conceived the study; MSM, MLM, PIA and AA conducted field work, MSM and MLM conducted laboratory work; AA and MSM wrote the paper: all authors edited versions of the manuscript.
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Méndez, M.S., Martinez, M.L., Araujo, P.I. et al. Solar radiation exposure accelerates decomposition and biotic activity in surface litter but not soil in a semiarid woodland ecosystem in Patagonia, Argentina. Plant Soil 445, 483–496 (2019). https://doi.org/10.1007/s11104-019-04325-1
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DOI: https://doi.org/10.1007/s11104-019-04325-1