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Biology and Fertility of Soils

, Volume 51, Issue 5, pp 525–533 | Cite as

Drying and substrate concentrations interact to inhibit decomposition of carbon substrates added to combusted Inceptisols from a boreal forest

  • Donovan P. German
  • Steven D. Allison
Original Paper

Abstract

Climate change is expected to alter the mechanisms controlling soil organic matter (SOM) stabilization. Under climate change, soil warming and drying could affect the enzymatic mechanisms that control SOM turnover and dependence on substrate concentration. Here, we used a greenhouse climate manipulation in a mature boreal forest soil to test two specific hypotheses: (1) Rates of decomposition decline at lower substrate concentrations, and (2) reductions in soil moisture disproportionately constrain the degradation of low-concentration substrates. Using constructed soil cores, we measured decomposition rates of two polymeric substrates, starch and cellulose, as well as enzyme activities associated with degradation of these substrates. The greenhouse manipulation increased temperature by 0.8 °C and reduced moisture in the constructed cores by up to 90 %. We rejected our first hypothesis, as the rate of starch decomposition did not decrease with declining starch concentration under control conditions, but we did find support for hypothesis two: Drying led to lower decomposition rates for low-concentration starch. We observed a threefold reduction in soil respiration rates in bulk soils in the greenhouses over a 4-month period, but the C losses from the constructed cores did not vary among our treatments. Activities of enzymes that degrade cellulose and starch were elevated in the greenhouse treatments, which may have compensated for moisture constraints on the degradation of the common substrate (i.e., cellulose) in our constructed cores. This study confirms that substrate decomposition can be concentration-dependent and suggests that climate change effects on soil moisture could reduce rates of decomposition in well-drained boreal forest soils lacking permafrost.

Keywords

Microbial decomposition Starch Cellulose Carbon cycling Carbon dioxide Extracellular enzymes 

Notes

Acknowledgments

We thank Stephanie Kivlin, Jennifer Talbot, Darleen Masiak, Kathleen Marcelo, and Heros Amerkhanian for help in the field and/or laboratory. We also thank two anonymous reviewers for insightful comments that improved the manuscript. This study was funded by the University of California President’s Postdoctoral Fellowship and UC Irvine Laboratory Start Up Funds (to DPG), and a grant from the NSF Advancing Theory in Biology program (to SDA).

References

  1. Allison SD (2006) Brown ground: a soil carbon analogue for the Green World Hypothesis? Am Nat 167:619–627PubMedCrossRefGoogle Scholar
  2. Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Chang Biol 14:2898–2909CrossRefGoogle Scholar
  3. Allison SD, Treseder KK (2011) Climate change feedbacks to microbial decomposition in boreal soils. Fungal Ecol 4:362–374. doi: 10.1016/j.funeco.2011.01.003 CrossRefGoogle Scholar
  4. Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1–13Google Scholar
  5. Allison SD, McGuire KL, Treseder KK (2010a) Resistance of microbial and soil properties to warming treatment seven years after boreal fire. Soil Biol Biochem 42:1872–1878CrossRefGoogle Scholar
  6. Allison SD, Wallenstein MD, Bradford MA (2010b) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340CrossRefGoogle Scholar
  7. Allison SD, Lu Y, Weihe C, Goulden ML, Martiny AC, Treseder KK, Martiny JBH (2013) Microbial abundance and composition influence litter decomposition response to environmental change. Ecology 94:714–725. doi: 10.1890/12-1243.1 PubMedCrossRefGoogle Scholar
  8. Allison SD, Chacon SS, German DP (2014) Substrate concentration constraints on microbial decomposition. Soil Biol Biochem 79:43–49. doi: 10.1016/j.soilbio.2014.08.021 CrossRefGoogle Scholar
  9. Alster CJ, German DP, Lu Y, Allison SD (2013) Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland. Soil Biol Biochem 64:68–79CrossRefGoogle Scholar
  10. Bergner B, Johnstone J, Treseder KK (2004) Experimental warming and burn severity alter soil CO2 flux and soil functional groups in a recently burned boreal forest. Glob Chang Biol 10:1996–2004CrossRefGoogle Scholar
  11. Broadbent FE, Bartholomew WV (1949) The effect of quantity of plant material added to soil on its rate of decomposition. Soil Sci Soc Am J 13:271–274CrossRefGoogle Scholar
  12. Bronson DR, Gower ST, Tanner M, Linder S, van Herk I (2008) Response of soil surface CO2 flux in a boreal forest to ecosystem warming. Glob Chang Biol 14:856–867CrossRefGoogle Scholar
  13. Brzostek ER, Blair JM, Dukes JS, Frey SD, Hobbie SE, Melillo JM, Mitchell RJ, Pendall E, Reich PB, Shaver GR, Stefanski A, Tjoelker MG, Finzi AC (2012) The effect of experimental warming and precipitation change on proteolytic enzyme activity: positive feedbacks to nitrogen availability are not universal. Glob Chang Biol 18:2617–2625. doi: 10.1111/j.1365-2486.2012.02685.x CrossRefGoogle Scholar
  14. Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427CrossRefGoogle Scholar
  15. Conant RT, Ryan MG, Ågren GI, Birge HE, Davidson EA, Eliasson PE, Evans SE, Frey SD, Giardina CP, Hopkins FM, Hyvönen R, Kirschbaum MUF, Lavallee JM, Leifeld J, Parton WJ, Steinweg JM, Wallenstein MD, Martin Wetterstedt JÅ, Bradford MA (2011) Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob Chang Biol 17:3392–3404. doi: 10.1111/j.1365-2486.2011.02496.x CrossRefGoogle Scholar
  16. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173PubMedCrossRefGoogle Scholar
  17. Davidson EA, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Glob Chang Biol 4:217–227. doi: 10.1046/j.1365-2486.1998.00128.x CrossRefGoogle Scholar
  18. Ekschmitt K, Liu M, Vetter S, Fox O, Wolters V (2005) Strategies used by soil biota to overcome soil organic matter stability—why is dead organic matter left over in the soil? Geoderma 128:167–176CrossRefGoogle Scholar
  19. Ekschmitt K, Kandeler E, Poll C, Brune A, Buscot F, Friedrich M, Gleixner G, Hartmann A, Kästner M, Marhan S, Miltner A, Scheu S, Wolters V (2008) Soil-carbon preservation through habitat constraints and biological limitations on decomposer activity. J Plant Nutr Soil Sci 171:27–35. doi: 10.1002/jpln.200700051 CrossRefGoogle Scholar
  20. Geisseler D, Horwath WR, Scow KM (2011) Soil moisture and plant residue addition interact in their effect on extracellular enzyme activity. Pedobiol 54:71–78. doi: 10.1016/j.pedobi.2010.10.001 CrossRefGoogle Scholar
  21. German DP, Chacon SS, Allison SD (2011a) Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 92:1471–1480PubMedCrossRefGoogle Scholar
  22. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011b) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397CrossRefGoogle Scholar
  23. Gorham E (1991) Northern Peatlands: role in the carbon cycle and probably responses to climatic warming. Ecol Appl 1:182–195CrossRefGoogle Scholar
  24. Gulledge J, Schimel JP (2000) Controls on soil carbon dioxide and methane fluxes in a variety of Taiga forest stands in interior Alaska. Ecosystems 3:269–282. doi: 10.1007/s100210000025 CrossRefGoogle Scholar
  25. Hernandez DL, Hobbie SE (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335:397–411CrossRefGoogle Scholar
  26. IPCC (2014) Climate change 2014: synthesis reportGoogle Scholar
  27. Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436CrossRefGoogle Scholar
  28. King S, Harden J, Manies KL, Munster J, White LD (2002) Fate of carbon in Alaskan landscape project. Database for soils from eddy covariance tower sites, Delta Junction, Alaska. Open File Report 02–62. U. S. Geological Survey, Menlo Park, CA, USAGoogle Scholar
  29. Kleber M, Nico PS, Plante A, Filley T, Kramer M, Swanston C, Sollins P (2010) Old and stable soil organic matter is not necessarily chemically recalcitrant: implications for modeling concepts and temperature sensitivity. Glob Chang Biol 17:1097–1107CrossRefGoogle Scholar
  30. Ladd JN, Foster R, Nannipieri P, Oades JM (1996) Soil structure and biological activity. In: Stotzky G, Bollag J-M (eds) Soil biochemistry. Marcel Dekker, New York, pp 23–78Google Scholar
  31. Larsen JA (1980) The boreal ecosystem. Academic Press, Inc., LondonGoogle Scholar
  32. Manzoni S, Schimel JP, Porporato A (2011) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938. doi: 10.1890/11-0026.1 CrossRefGoogle Scholar
  33. Nannipieri P, Gianfreda L (1998) Kinetics of enzyme reactions in soil environments. In: Huang PM, Senesi N, Buffle J (eds) Structure and surface reactions of soil particles. John Wiley & Sons, New York, pp 449–479Google Scholar
  34. Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment. Marcel Dekker, New York, pp 1–33Google Scholar
  35. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762. doi: 10.1007/s00374-012-0723-0 CrossRefGoogle Scholar
  36. Or D, Smets BF, Wraith JM, Dechesne A, Friedman SP (2007) Physical constraints affecting bacterial habitats and activity in unsaturated porous media—a review. Adv Water Resour 30:1505–1527CrossRefGoogle Scholar
  37. Parton WJ, Schimel DS, Cole CV, Ojima DS (1987) Analysis of factors controlling soil organic-matter levels in great-plains grasslands. Soil Sci Soc Am J 51:1173–1179CrossRefGoogle Scholar
  38. Poll C, Marhan S, Back F, Niklaus PA, Kandeler E (2013) Field-scale manipulation of soil temperature and precipitation change soil CO2 flux in a temperate agricultural ecosystem. Agric Ecosyst Environ 165:88–97. doi: 10.1016/j.agee.2012.12.012 CrossRefGoogle Scholar
  39. Prescott CE, McDonald MA (1994) Effects of carbon and lime additions on mineralization of C and N in humus from cutovers of western red cedar - western hemlock forests of northern Vancouver Island. Can J Forest Res 24:2432–2438CrossRefGoogle Scholar
  40. Ratledge C (1994) Biochemistry of microbial degradation. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  41. Rustad L, Campbell J, Marion G, Norby R, Mitchell M, Hartley A, Cornelissen J, Gurevitch J, Gcte N (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562. doi: 10.1007/s004420000544 CrossRefGoogle Scholar
  42. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  43. Schimel JP, Helfer S, Alexander IJ (1992) Effects of starch additions on N turnover in Sitka spruce forest floor. Plant Soil 139:139–143CrossRefGoogle Scholar
  44. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56PubMedCrossRefGoogle Scholar
  45. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  46. Steinweg JM, Dukes JS, Wallenstein MD (2012) Modeling the effects of temperature and moisture on soil enzyme activity: linking laboratory assays to continuous field data. Soil Biol Biochem 55:85–92. doi: 10.1016/j.soilbio.2012.06.015 CrossRefGoogle Scholar
  47. Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. University of California Press, BerkeleyGoogle Scholar
  48. Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Glob Biogeochem Cycles 23, GB2023CrossRefGoogle Scholar
  49. Todd-Brown KEO, Hopkins FM, Kivlin SN, Talbot JM, Allison SD (2012) A framework for representing microbial decomposition in coupled climate models. Biogeochemical 109:19–33CrossRefGoogle Scholar
  50. Treseder KK, Mack MC, Cross A (2004) Relationships among fires, fungi, and soil dynamics in Alaskan boreal forests. Ecol Appl 14:1826–1838CrossRefGoogle Scholar
  51. von Lützow M, Kögel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition—what do we know? Biol Fertil Soils 46:1–15. doi: 10.1007/s00374-009-0413-8 CrossRefGoogle Scholar
  52. Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106CrossRefGoogle Scholar
  53. Wieder WR, Cleveland CC, Townsend AR (2011) Throughfall exclusion and leaf litter addition drive higher rates of soil nitrous oxide emissions from a lowland wet tropical forest. Glob Chang Biol 17:3195–3207. doi: 10.1111/j.1365-2486.2011.02426.x CrossRefGoogle Scholar
  54. Wieder WR, Bonan GB, Allison SD (2013) Global soil carbon predictions are improved by modelling microbial processes. Nature Clim Chang 3:909–912CrossRefGoogle Scholar
  55. Zhang T, Barry RG, Knowles K, Heginbottom JA, Brown J (2008) Statistics and characteristics of permafrost and ground-ice distribution in the northern hemisphere. Pol Geogr 31:47–68CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA
  2. 2.Department of Earth System ScienceUniversity of CaliforniaIrvineUSA

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