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Impacts of an invasive grass on soil organic matter pools vary across a tree-mycorrhizal gradient

  • Matthew E. CraigEmail author
  • Nadia Lovko
  • S. Luke Flory
  • Justin P. Wright
  • Richard P. Phillips
Article

Abstract

Increases in carbon (C) inputs can augment soil organic matter (SOM), or reduce SOM by accelerating decomposition. Thus, there is a need to understand how and why ecosystems differ in their sensitivity to C inputs. Invasive plants that invade wide-ranging habitats, accumulate biomass rapidly, and contribute copious amounts of C to soil can be ideal for addressing this gap. We quantified the effects of the invasive C4 grass, Microstegium vimineum, on SOM in three temperate forests across plots varying in their relative abundance of arbuscular mycorrhizal (AM) versus ectomycorrhizal (ECM) trees. We hypothesized that invasion would differentially affect SOM along the mycorrhizal gradient owing to recognized patterns in nitrogen availability (AM > ECM) and the proportion of unprotected SOM (ECM > AM). Across all sites, M. vimineum was associated with lower particulate organic matter (POM) in ECM-dominated plots, consistent with our hypothesis that invader-derived C inputs should stimulate decomposers to acquire nitrogen from unprotected SOM in soils with low nitrogen availability. However, the pattern of lower POM in the ECM-dominated soils was offset by greater mineral-associated organic matter (MAOM)—and isotopic data suggest this was largely driven by native- rather than invader-derived SOM—implying an invasion-associated transfer of native-derived POM into MAOM. Our results demonstrate a context-dependent shift in the form of SOM in a system with presumably enhanced C inputs. This finding suggests a need to look beyond changes in total SOM stocks, as intrinsic SOM changes could lead to important long-term feedbacks on invasion or priming effects.

Keywords

Plant invasion Microstegium Priming Mycorrhizal fungi Carbon Nitrogen 

Notes

Acknowledgements

This work was funded by the US National Science Foundation Ecosystem Studies Program (Grant Nos. 1353296, 1354879, and 1353211). Moore’s Creek is part of Indiana University’s Research and Teaching preserve. Marissa Lee and Cathy Fahey assisted with study design and plot setup and collected most of the samples from DF and WF, respectively. Mark Sheehan assisted with plot setup at MC. Laura Podzikowski contributed to the laboratory analysis of soil covariates, and Robin Johnson and Eric Ungberg helped with sample processing. We thank Steve Kannenberg, Adrienne Keller, and two anonymous reviewers for feedback on this paper; and Mark Bradford for input on the design of this project.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10533_2019_577_MOESM1_ESM.docx (247 kb)
Supplementary material 1 (DOCX 247 kb)

References

  1. Anderson DW, Paul EA (1984) Organo-mineral complexes and their study by radiocarbon dating. Soil Sci Soc Am J 48:298–301CrossRefGoogle Scholar
  2. Baath E, Berg B, Lundgren B et al (1980) Effects of experimental acidification and liming on soil organisms and decomposition in a Scots pine forest. Pedobiologia 20:85–100Google Scholar
  3. Bayan MR, Eivazi F (1999) Selected enzyme activities as affected by free iron oxides and clay particle size. Commun Soil Sci Plant Anal 30:1561–1571CrossRefGoogle Scholar
  4. Bingham AH, Cotrufo MF (2016) Organic nitrogen storage in mineral soil: implications for policy and management. Sci Total Environ 551:116–126CrossRefGoogle Scholar
  5. Blagodatskaya E, Kuzyakov Y (2011) Priming effects in relation to soil conditions—mechanisms. In: Gliński J, Horabik J, Lipiec J (eds) Encyclopedia of agrophysics. Encyclopedia of earth sciences series. Springer, Dordrecht, pp 657–667CrossRefGoogle Scholar
  6. Bradford MA, Fierer N, Reynolds JF (2008) Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–974.  https://doi.org/10.1111/j.1365-2435.2008.01404.x CrossRefGoogle Scholar
  7. Bradford MA, Strickland MS, DeVore JL, Maerz JC (2012) Root carbon flow from an invasive plant to belowground foodwebs. Plant Soil 359:233–244.  https://doi.org/10.1007/s11104-012-1210-y CrossRefGoogle Scholar
  8. Bradford MA, Keiser AD, Davies C et al (2013) Empirical evidence that soil carbon formation from plant inputs is positively related to microbial growth. Biogeochemistry 113:271–281.  https://doi.org/10.1007/s10533-012-9822-0 CrossRefGoogle Scholar
  9. Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56–71CrossRefGoogle Scholar
  10. Cambardella CA, Elliott ET (1992) Particulate soil organic matter changes across a grassland cultivation sequence. Soil Sci Soc Am J 56:777–783CrossRefGoogle Scholar
  11. Cardinael R, Eglin T, Guenet B et al (2015) Is priming effect a significant process for long-term SOC dynamics? Analysis of a 52-years old experiment. Biogeochemistry 123:203–219.  https://doi.org/10.1007/s10533-014-0063-2 CrossRefGoogle Scholar
  12. Cardon ZG, Hungate BA, Cambardella CA et al (2001) Contrasting effects of elevated CO2 on old and new soil carbon pools. Soil Biol Biochem 33:365–373CrossRefGoogle Scholar
  13. Chen R, Senbayram M, Blagodatsky S et al (2014) Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories. Glob Chang Biol 20:2356–2367.  https://doi.org/10.1111/gcb.12475 CrossRefGoogle Scholar
  14. Craig ME, Fraterrigo JM (2017) Plant–microbial competition for nitrogen increases microbial activities and carbon loss in invaded soils. Oecologia 184:583–596.  https://doi.org/10.1007/s00442-017-3861-0 CrossRefGoogle Scholar
  15. Craig ME, Pearson SM, Fraterrigo JM (2015) Grass invasion effects on forest soil carbon depend on landscape-level land use patterns. Ecology 96:2265–2279.  https://doi.org/10.1890/14-1770.1 CrossRefGoogle Scholar
  16. Craig ME, Turner BL, Liang C et al (2018) Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter. Glob Chang Biol.  https://doi.org/10.1111/gcb.14132 Google Scholar
  17. Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113CrossRefGoogle Scholar
  18. Dassonville N, Vanderhoeven S, Vanparys V et al (2008) Impacts of alien invasive plants on soil nutrients are correlated with initial site conditions in NW Europe. Oecologia 157:131–140.  https://doi.org/10.1007/s00442-008-1054-6 CrossRefGoogle Scholar
  19. Di Lonardo DP, De Boer W, Gunnewiek PJAK et al (2017) Priming of soil organic matter: chemical structure of added compounds is more important than the energy content. Soil Biol Biochem 108:41–54.  https://doi.org/10.1016/j.soilbio.2017.01.017 CrossRefGoogle Scholar
  20. Dijkstra FA, Cheng W (2007) Moisture modulates rhizosphere effects on C decomposition in two different soil types. Soil Biol Biochem 39:2264–2274.  https://doi.org/10.1016/j.soilbio.2007.03.026 CrossRefGoogle Scholar
  21. Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exoctic understory indeciduous forests. Ecol Appl 11:1287–1300.  https://doi.org/10.2307/3060920 CrossRefGoogle Scholar
  22. Fontaine S, Barot S (2005) Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8:1075–1087.  https://doi.org/10.1111/j.1461-0248.2005.00813.x CrossRefGoogle Scholar
  23. Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320.  https://doi.org/10.1111/j.1461-0248.2004.00579.x CrossRefGoogle Scholar
  24. Fontaine S, Henault C, Aamor A et al (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96.  https://doi.org/10.1016/j.soilbio.2010.09.017 CrossRefGoogle Scholar
  25. 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.  https://doi.org/10.1038/nclimate1796 CrossRefGoogle Scholar
  26. Garten CTJ, Wullschleger SD (2000) Soil carbon dynamics beneath switchgrass as indicated by stable isotope analysis. J Environ Qual 29:645–653CrossRefGoogle Scholar
  27. Geisseler D, Horwath WR, Georg R, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms—a review. Soil Biol Biochem 42:2058–2067.  https://doi.org/10.1016/j.soilbio.2010.08.021 CrossRefGoogle Scholar
  28. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307.  https://doi.org/10.1016/j.scitotenv.2007.11.013 CrossRefGoogle Scholar
  29. Hughes RF, Uowolo A (2006) Impacts of Falcataria moluccana invasion on decomposition in Hawaiian lowland wet forests: the importance of stand-level controls. Ecosystems 9:977–991.  https://doi.org/10.1007/S10021-005-0083-9 CrossRefGoogle Scholar
  30. Keiluweit M, Bougoure JJ, Nico PS et al (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595.  https://doi.org/10.1038/NCLIMATE2580 CrossRefGoogle Scholar
  31. Kleber M, Eusterhues K, Keiluweit M et al (2015) Mineral-organic associations: formation, properties, and relevance in soil environments. Adv Agron 130:1–140.  https://doi.org/10.1016/bs.agron.2014.10.005 CrossRefGoogle Scholar
  32. Kourtev PS, Ehrenfeld JG, Haggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905.  https://doi.org/10.1016/S0038-0717(03)00120-2 CrossRefGoogle Scholar
  33. Koutika L, Vanderhoeven S, Chapuis-lardy L et al (2007) Assessment of changes in soil organic matter after invasion by exotic plant species. Biol Fertil Soils 44:331–341.  https://doi.org/10.1007/s00374-007-0210-1 CrossRefGoogle Scholar
  34. Kramer TD, Warren RJ, Tang Y, Bradford MA (2012) Grass invasions across a regional gradient are associated with declines in belowground carbon pools. Ecosystems 15:1271–1282.  https://doi.org/10.1007/s10021-012-9583-6 CrossRefGoogle Scholar
  35. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371CrossRefGoogle Scholar
  36. Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498CrossRefGoogle Scholar
  37. Lajtha K, Townsend KL, Kramer MG et al (2014) Changes to particulate versus mineral-associated soil carbon after 50 years of litter manipulation in forest and prairie experimental ecosystems. Biogeochemistry 119:341–360.  https://doi.org/10.1007/s10533-014-9970-5 CrossRefGoogle Scholar
  38. Lajtha K, Bowden RD, Crow S et al (2018) Science of the Total Environment The detrital input and removal treatment (DIRT) network: insights into soil carbon stabilization. Sci Total Environ 640–641:1112–1120.  https://doi.org/10.1016/j.scitotenv.2018.05.388 CrossRefGoogle Scholar
  39. Lankau RA, Nuzzo V, Spyreas G, Davis AS (2009) Evolutionary limits ameliorate the negative impact of an invasive plant. Proc Natl Acad Sci USA 106:15362–15367.  https://doi.org/10.1073/pnas.0913493107 CrossRefGoogle Scholar
  40. Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105.  https://doi.org/10.1038/nmicrobiol.2017.105 CrossRefGoogle Scholar
  41. Liao C, Peng R, Luo Y et al (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714CrossRefGoogle Scholar
  42. Lin G, Mccormack ML, Ma C, Guo D (2016) Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol 213:1440–1451.  https://doi.org/10.1111/nph.14206 CrossRefGoogle Scholar
  43. Luo Z, Wang E, Sun OJ (2016) A meta-analysis of the temporal dynamics of priming soil carbon decomposition by fresh carbon inputs across ecosystems. Soil Biol Biochem 101:96–103.  https://doi.org/10.1016/j.soilbio.2016.07.011 CrossRefGoogle Scholar
  44. Manzoni S, Taylor P, Richter A et al (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91CrossRefGoogle Scholar
  45. Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128.  https://doi.org/10.1016/j.soilbio.2016.12.004 CrossRefGoogle Scholar
  46. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174CrossRefGoogle Scholar
  47. Niklaus PA, Falloon P (2006) Estimating soil carbon sequestration under elevated CO2 by combining carbon isotope labelling with soil carbon cycle modelling. Glob Chang Biol 12:1909–1921.  https://doi.org/10.1111/j.1365-2486.2006.01215.x CrossRefGoogle Scholar
  48. Phillips RP, Finzi AC, Bernhardt ES (2011) Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol Lett 14:187–194CrossRefGoogle Scholar
  49. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51.  https://doi.org/10.1111/nph.12221 CrossRefGoogle Scholar
  50. Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1-117. http://CRAN.R-project.org/package=nlme
  51. Rasmussen C, Heckman K, Wieder WR et al (2018) Beyond clay: towards an improved set of variables for predicting soil organic matter content. Biogeochemistry 137:297–306.  https://doi.org/10.1007/s10533-018-0424-3 CrossRefGoogle Scholar
  52. Rousk K, Michelsen A, Rousk J (2016) Microbial control of soil organic matter mineralization responses to labile carbon in subarctic climate change treatments. Glob Chang Biol 22:4150–4161CrossRefGoogle Scholar
  53. Scharfy D, Eggenschwiler H, Olde Venterink H et al (2009) The invasive alien plant species Solidago gigantea alters ecosystem properties across habitats with differing fertility. J Veg Sci 20:1072–1085CrossRefGoogle Scholar
  54. Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56.  https://doi.org/10.1038/nature10386 CrossRefGoogle Scholar
  55. Schneider MPW, Scheel T, Mikutta R et al (2010) Sorptive stabilization of organic matter by amorphous Al hydroxide. Geochim Cosmochim Acta 74:1606–1619.  https://doi.org/10.1016/j.gca.2009.12.017 CrossRefGoogle Scholar
  56. Sessitsch A, Weilharter A, Gerzabek MH et al (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67:4215–4224.  https://doi.org/10.1128/AEM.67.9.4215 CrossRefGoogle Scholar
  57. Sistla SA, Moore JC, Simpson RT et al (2013) Long-term warming restructures Arctic tundra without changing net soil carbon storage. Nature 497:615–618.  https://doi.org/10.1038/nature12129 CrossRefGoogle Scholar
  58. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176CrossRefGoogle Scholar
  59. Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys, 2nd edn. United States Department of Agriculture–Natural Resources Conservation ServiceGoogle Scholar
  60. Sokol NW, Kuebbing SE, Bradford MA (2017) Impacts of an invasive plant are fundamentally altered by a co-occurring forest disturbance. Ecology 98:2133–2144.  https://doi.org/10.1002/ecy.1906 CrossRefGoogle Scholar
  61. Sokol NW, Kuebbing SE, Karlsen-Ayala E, Bradford MA (2018) Evidence for the primacy of living root inputs, not root or shoot litter, in forming soil organic carbon. New Phytol 221:233–246.  https://doi.org/10.1111/nph.15361 CrossRefGoogle Scholar
  62. Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210CrossRefGoogle Scholar
  63. Strickland MS, Devore JL, Maerz JC, Bradford MA (2010) Grass invasion of a hardwood forest is associated with declines in belowground carbon pools. Glob Chang Biol 16:1338–1350.  https://doi.org/10.1111/j.1365-2486.2009.02042.x CrossRefGoogle Scholar
  64. Strickland MS, Devore JL, Maerz JC, Bradford MA (2011) Loss of faster-cycling soil carbon pools following grass invasion across multiple forest sites. Soil Biol Biochem 43:452–454.  https://doi.org/10.1016/j.soilbio.2010.10.006 CrossRefGoogle Scholar
  65. Sulman BN, Phillips RP, Oishi AC et al (2014) Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nat Clim Chang 4:1099–1102.  https://doi.org/10.1038/NCLIMATE2436 CrossRefGoogle Scholar
  66. Sulman BN, Brzostek ER, Medici C et al (2017) Feedbacks between plant N demand and rhizosphere priming depend on type of mycorrhizal association. Ecol Lett 20:1043–1053.  https://doi.org/10.1111/ele.12802 CrossRefGoogle Scholar
  67. Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull 34:395–407.  https://doi.org/10.1134/S1062359007040127 CrossRefGoogle Scholar
  68. Ulmer M, Knuteson J, Patterson D (1994) Particle size analysis by hydrometer a routine method for determining clay fraction. Soil Surv Horizons 35:11–17CrossRefGoogle Scholar
  69. Van Groenigen K, Six J, Hungate BA et al (2006) Element interactions limit soil carbon storage. Proc Natl Acad Sci USA 103:6571–6574CrossRefGoogle Scholar
  70. Vilà M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708.  https://doi.org/10.1111/j.1461-0248.2011.01628.x CrossRefGoogle Scholar
  71. Zhang W, Wang X, Wang S (2013) Addition of external organic carbon and native soil organic carbon decomposition: a meta-analysis. PLoS ONE 8:e54779.  https://doi.org/10.1371/journal.pone.0054779 CrossRefGoogle Scholar
  72. Zhang X, Han X, Yu W et al (2017) Priming effects on labile and stable soil organic carbon decomposition: pulse dynamics over two years. PLoS ONE 12:e0184978CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA
  2. 2.Agronomy DepartmentUniversity of FloridaGainesvilleUSA
  3. 3.Department of BiologyDuke UniversityDurhamUSA

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