Advertisement

Ecosystems

, Volume 22, Issue 4, pp 859–872 | Cite as

Linking Improvement of Soil Structure to Soil Carbon Storage Following Invasion by a C4 Plant Spartina alterniflora

  • Yanghui He
  • Xuhui ZhouEmail author
  • Weisong Cheng
  • Lingyan Zhou
  • Guodong Zhang
  • Guiyao Zhou
  • Ruiqiang Liu
  • Junjiong Shao
  • Kai Zhu
  • Weixin Cheng
Article

Abstract

Coastal wetlands are increasingly recognized as important ecosystems for long-term carbon (C) storage. However, how soil aggregation mediates C accumulation and sequestration in these ecosystems remains unclear. Using the 13C isotope tracer from the invasion of a C4 plant, Spartina alterniflora, into the native ecosystem originally covered by C3 plants across Eastern Chinese coastal wetlands, we investigated a potential C stabilization process via soil structural protection. We quantified changes in soil aggregates, soil organic carbon (SOC), soil total nitrogen (STN), and natural 13C isotope abundance within aggregate fractions across a chronosequence of 0-, 4-, 8-, and 12-year S. alterniflora invasion. Our results showed that soil aggregate stability increased significantly along the chronosequence. Meanwhile, SOC and STN concentrations increased with invasion time in the whole soil and aggregate fractions, which were linked to increasing soil aggregate stability. The contribution of S. alterniflora-derived SOC increased from 18.96 to 40.24% in the 0–20 cm layer and from 4.66 to 32.04% in the 20–40 cm layer across the chronosequence from 4 to 12 years with the highest proportion observed in macro-aggregates. Our results indicate that invasion of S. alterniflora to coastal wetlands can sequester more C largely due to formation and stabilization of soil aggregates by soil structural protection.

Keywords

coastal wetland Spartina alterniflora soil aggregates soil organic carbon soil total nitrogen stable carbon isotope 

Notes

Acknowledgements

This study was carried out at the Chongming Dongtan Nature Reserve, Shanghai. We acknowledge the practical help provided by Dan Wang, Qin Wang, and Haiqiang Guo. We thank Ming Li, Zhenggang Du, Yuanyuan Nie, and Xi Yang for assistance with field work. We would also like to thank anonymous reviewers for their critical comments/suggestions which improved the quality of the manuscript. This research was financially supported by the National Natural Science Foundation of China (Grant Nos. 31770559, 31370489, and 31600352), the Program for Professor of Special Appointment (Eastern Scholar) at Shanghai Institutions of Higher Learning, and “Thousand Young Talents” Program in China.

Supplementary material

10021_2018_308_MOESM1_ESM.docx (919 kb)
Supplementary material 1 (DOCX 918 kb)

References

  1. Abiven S, Menasseri S, Chenu C. 2009. The effects of organic inputs over time on soil aggregate stability: a literature analysis. Soil Biol Biochem 41:1–12.CrossRefGoogle Scholar
  2. Abramoff R, Xu X, Hartman M, O’Brien S, Feng W, Davidson E, Finzi A, Moorhead D, Schimel J, Torn M, Mayes MA. 2018. The Millennial model: in search of measurable pools and transformations for modeling soil carbon in the new century. Biogeochemistry 137:51–71.CrossRefGoogle Scholar
  3. Agrawal A, Nepstad D, Chhatre A. 2011. Reducing emissions from deforestation and forest degradation. Ann Rev Environ Resour 36:373–96.CrossRefGoogle Scholar
  4. Alongi DM. 2002. Present state and future of the world’s mangrove forests. Environ Conserv 29:33–49.CrossRefGoogle Scholar
  5. An SQ, Gu BH, Zhou CF, Wang ZS, Deng ZF, Zhi YB, Li HL, Chen L, Yu DH, Liu YH. 2007. Spartina invasion in China: implications for invasive species management and future research. Weed Res 47:183–91.CrossRefGoogle Scholar
  6. Balesdent J, Wagner GH, Mariotti A. 1988. Soil organic matter turnover in long-term field experiments as revealed by carbon-13 natural abundance. Soil Sci Soc Am J 52:118–24.CrossRefGoogle Scholar
  7. Barto EK, Alt F, Oelmann Y, Wilcke W, Rillig MC. 2010. Contributions of biotic and abiotic factors to soil aggregation across a land use gradient. Soil Biol Biochem 42:2316–24.CrossRefGoogle Scholar
  8. Bronick CJ, Lal R. 2005. Soil structure and management: a review. Geoderma 124:3–22.CrossRefGoogle Scholar
  9. Bull ID, van Bergen PF, Bol R, Brown S, Gledhill AR, Gray AJ, Harkness DD, Woodbury SE, Evershed RP. 1999. Estimating the contribution of Spartina anglica biomass to saltmarsh sediments using compound specific carbon isotope measurements. Org Geochem 30:477–83.CrossRefGoogle Scholar
  10. Buyanovsky GA, Aslam M, Wagner GH. 1994. Carbon turnover in soil physical fractions. Soil Sci Soc Am J 58:1167–73.CrossRefGoogle Scholar
  11. Cécillon L, de Mello NA, De Danieli S, Brun JJ. 2010. Soil macroaggregate dynamics in a mountain spatial climate gradient. Biochemistry 97:31–43.Google Scholar
  12. Chambers LG, Guevara R, Boyer JN, Troxler TG, Davis SE. 2016. Effects of salinity and inundation on microbial community structure and function in a mangrove peat soil. Wetlands 36:361–71.CrossRefGoogle Scholar
  13. Chen ZY, Li B, Zhong Y, Chen JK. 2004. Local competitive effects of introduced Spartina alterniflora on Scirpus mariqueter at Dongtan of Chongming Island, the Yangtze River estuary and their potential ecological consequences. Hydrobiologia 528:99–106.CrossRefGoogle Scholar
  14. Cheng XL, Luo YQ, Chen JQ, Lin GH, Chen JK, Li B. 2006. Short-term C4 plant Spartina alterniflora invasions change the soil carbon in C3 plant dominated tidal wetlands on a growing estuarine island. Soil Biol Biochem 38:3380–6.CrossRefGoogle Scholar
  15. Cheng XL, Chen JQ, Luo YQ. 2008. Assessing the effects of short-term Spartina alterniflora invasion on labile and recalcitrant C and N pools by means of soil fractionation and stable C and N isotopes. Geoderma 145:177–84.CrossRefGoogle Scholar
  16. Chiang PN, Wang MK, Chiu CY, King HB, Hwong JL. 2004. Change in the grassland-forest boundary at Ta-Ta-Chia long term ecological research (LTER) site detected by stable isotope ratio of soil organic matter. Chemosphere 54:217–24.CrossRefPubMedGoogle Scholar
  17. Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC. 2003. Global carbon sequestration in tidal, saline wetland soils. Glob Biogeochem Cycles 17:1111.CrossRefGoogle Scholar
  18. Choi Y, Wang Y. 2004. Dynamics of carbon sequestration in a coastal wetland using radiocarbon measurements. Glob Biogeochem Cycles 18:4016.CrossRefGoogle Scholar
  19. Christensen BT. 2001. Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–53.CrossRefGoogle Scholar
  20. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD. 2013. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–18.CrossRefGoogle Scholar
  21. Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–92.CrossRefPubMedGoogle Scholar
  22. Denef K, Six J, Merckx R, Paustian K. 2002. Short-term effects of biological and physical forces on aggregate formation in soils with different clay mineralogy. Plant Soil 246:185–200.CrossRefGoogle Scholar
  23. Desjardins T, Carneirofilho A, Mariotti A, Chauvel A, Girardin C. 1996. Changes of the forest-savanna boundary in Brazilian Amazonia during the Holocene revealed by stable isotope ratio of soil organic carbon. Oecologia 108:749–56.CrossRefPubMedGoogle Scholar
  24. Desjardins T, Folgarait PJ, Pando-Bahuon A, Girardin C, Lavelle P. 2006. Soil organic matter dynamics along a rice chronosequence in north-eastern Argentina: evidence from natural 13C abundance and particle size fractionation. Soil Biol Biochem 38:2753–61.CrossRefGoogle Scholar
  25. Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M. 2011. Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–7.CrossRefGoogle Scholar
  26. Duarte CM, Middelburg J, Caraco N. 2005. Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2:1–8.CrossRefGoogle Scholar
  27. Duarte CM, Losada IJ, Hendriks IE, Mazarrasa I, Marba N. 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nat Clim Change 3:961–8.CrossRefGoogle Scholar
  28. Duiker SW, Rhoton FE, Torrent J, Smeck NE, Lal R. 2003. Iron (hydr)oxide crystallinity effects on soil aggregation. Soil Sci Soc Am J 67:606–11.CrossRefGoogle Scholar
  29. Fourqurean JW, Duarte CM, Kennedy H, Marbà N, Holmer M, Mateo MA, Apostolaki ET, Kendrick GA, Krause-Jensen D, McGlathery KJ. 2012. Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5:505–9.CrossRefGoogle Scholar
  30. Franzluebbers AJ, Arshad MA. 1997. Particulate organic carbon content and potential mineralization as affected by tillage and texture. Soil Sci Soc Am J 61:1382–6.CrossRefGoogle Scholar
  31. Gale W, Cambardella C, Bailey T. 2000. Root-derived carbon and the formation and stabilization of aggregates. Soil Sci Soc Am J 64:201–7.CrossRefGoogle Scholar
  32. Gebrehiwet T, Koretsky MC, Krishnamurthy RV. 2008. Influence of Spartina and Juncus on salt marsh sediments. III. Organic geochemistry. Chem Geol 255:114–19.CrossRefGoogle Scholar
  33. Golchin A, Baldock JA, Oades JM. 1997. A model linking organic matter decomposition, chemistry, and aggregate dynamics. In: Lal R, Kimble JM, Follett RF, Stewart BA, Eds. Soil processes and the carbon cycle. New York: CRC Press. p 245–66.Google Scholar
  34. Graves CJ, Makrides EJ, Schmidt VT, Giblin AE, Cardon ZG, Rand DM. 2016. Functional responses of salt marsh microbial communities to long-term nutrient enrichment. Appl Environ Microbiol 82:2862–71.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Green EP, Short FT. 2003. World atlas of seagrasses. Berkeley (CA): California University Press.Google Scholar
  36. Harvey HR, Mannino A. 2001. The chemical composition and cycling of particulate and macromolecular dissolved organic matter in temperate estuaries as revealed by molecular organic tracers. Org Geochem 32:527–42.CrossRefGoogle Scholar
  37. Hemminga MA, Cattrijsse A, Wielemaker A. 1996. Bedload and nearbed detritus transport in a tidal saltmarsh creek. Estuar Coast Shelf Sci 42:55–62.CrossRefGoogle Scholar
  38. IPCC. 2013. 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: Cambridge University Press.Google Scholar
  39. Jastrow JD. 1996. Soil aggregate formation and the accrual of particulate and mineral-associated organic matter. Soil Biol Biochem 28:665–76.CrossRefGoogle Scholar
  40. Jastrow JD, Boutton TW, Miller RM. 1996. Carbon dynamics of aggregate-associated organic matter estimated by carbon-13 natural abundance. Soil Sci Soc Am J 60:801–7.CrossRefGoogle Scholar
  41. Jastrow JD, Miller RM, Lussenhop J. 1998. Contributions of interacting biological mechanisms to soil aggregate stabilization in restored prairie. Soil Biol Biochem 30:905–16.CrossRefGoogle Scholar
  42. Jenkinson DS, Coleman K. 2008. The turnover of organic carbon in subsoils. Part 2. Modelling carbon turnover. Eur J Soil Sci 59:400–13.CrossRefGoogle Scholar
  43. Kelleway JJ, Saintilan N, Macreadie PI, Ralph PJ. 2016. Sedimentary factors are key predictors of carbon storage in SE Australian saltmarshes. Ecosystems 19:865–80.CrossRefGoogle Scholar
  44. Kemper WD, Rosenau RC. 1986. Aggregate stability and size distribution. In: Klute A, Ed. Methods of Soil Analysis. Part 1. 2nd ednAgron. Monogr. 9, Madison (WI): ASA. p 425–42.Google Scholar
  45. Kennedy H, Beggins J, Duarte CM et al. 2010. Seagrass sediments as a global carbon sink: isotopic constraints. Global Biogeochem Cycles 24:57.  https://doi.org/10.1029/2010gb003848.CrossRefGoogle Scholar
  46. Killham K, Amato M, Ladd JN. 1993. Effect of substrate location in soil and soil pore-water regime on carbon turnover. Soil Biol Biochem 25:57–62.CrossRefGoogle Scholar
  47. Kirwan ML, Megonigal JP. 2013. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504:53–60.CrossRefPubMedGoogle Scholar
  48. Koven CD, Riley WJ, Subin ZM et al. 2013. The effect of vertically resolved soil biogeochemistry and alternate soil C and N models on C dynamics of CLM4. Biogeosciences 10:7109–31.CrossRefGoogle Scholar
  49. Kristensen E, Bouillon S, Dittmar T, Marchand C. 2008. Organic carbon dynamics in mangrove ecosystems: a review. Aquat Bot 89:201–19.CrossRefGoogle Scholar
  50. Krull ES, Baldock JA, Skjemstad JO. 2003. Importance of mechanisms and processes of the stabilisation of soil organic matter for modelling carbon turnover. Funct Plant Biol 30:207–22.CrossRefGoogle Scholar
  51. Liao JD, Boutton TW, Jastrow JD. 2006. Storage and dynamics of carbon and nitrogen in soil physical fractions following woody plant invasion of grassland. Soil Biol Biochem 38:3184–96.CrossRefGoogle Scholar
  52. Liao C, Luo Y, Jiang L, Zhou X, Wu X, Fang C, Chen J, Li B. 2007. Invasion of Spartina alterniflora enhanced ecosystem carbon and nitrogen stocks in the Yangtze estuary, China. Ecosystems 10:1351–61.CrossRefGoogle Scholar
  53. Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B. 2008. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–14.CrossRefGoogle Scholar
  54. Lin GH, Ehleringer JR, Rygiewicz PT, Johnson MG, Tingey DT. 1999. Elevated CO2 and temperature impacts on different components of soil CO2 efflux in Douglas-fir terracosms. Glob Change Biol 5:157–68.CrossRefGoogle Scholar
  55. Luo Y, Ahlström A, Allison SD et al. 2015. Towards more realistic projections of soil carbon dynamics by earth system models. Glob Biogeochem Cycles .  https://doi.org/10.1002/2015gb005239.CrossRefGoogle Scholar
  56. Ma Z, Melville DS, Liu J, Chen Y, Yang H, Ren W, Zhang Z, Piersma T, Li B. 2014. Rethinking China’s new great wall. Science 346:912–14.CrossRefPubMedGoogle Scholar
  57. Mcleod E, Chmura GL, Bouillon S, Salm R, Björk M, Duarte C, Lovelock CE, Schlesingers WH, Silliman BR. 2011. A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front Ecol Environ 7:362–70.CrossRefGoogle Scholar
  58. Morel JL, Habib L, Plantureux S. 1991. Influence of maize root mucilage on soil aggregate stability. Plant Soil 136:111–19.CrossRefGoogle Scholar
  59. Neubauer SC. 2008. Contributions of mineral and organic components of tidal freshwater marsh accretion. Estuar Coast Shelf Sci 78:78–88.CrossRefGoogle Scholar
  60. Oades JM, Waters AG. 1991. Aggregate hierarchy in soils. Aust J Soil Res 29:815–28.CrossRefGoogle Scholar
  61. Qin P, Zhong CX. 1992. Applied studies on Spartina. London: Ocean Press.Google Scholar
  62. Roulet NT. 2000. Peatlands, carbon storage, greenhouse gases, and the Kyoto Protocol: prospects, and significance for Canada. Wetlands 20:605–15.CrossRefGoogle Scholar
  63. Rovira P, Vallejo VR. 2002. Labile and recalcitrant pools of carbon and nitrogen in organic matter decomposing at different depths in soil: an acid hydrolysis approach. Geoderma 107:109–41.CrossRefGoogle Scholar
  64. Salome C, Nunan N, Poteau R, Lerch TZ, Chenu C. 2010. Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob Change Biol 16:416–26.CrossRefGoogle Scholar
  65. Six J, Jastrow JD. 2002. Organic matter turnover. In: Lal T, Ed. Encyclopedia of soil science. New York: Marcel Dekker. p 936–42.Google Scholar
  66. Six J, Elliott ET, Paustian K, Doran JW. 1998. Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62:1367–76.CrossRefGoogle Scholar
  67. Six J, Paustian K, Elliott ET, Combrink C. 2000a. Soil structure and organic matter: I. Distribution of aggregate-size classes and aggregate-associated carbon. Soil Sci Soc Am J 64:681–9.CrossRefGoogle Scholar
  68. Six J, Elliott ET, Paustian K. 2000b. Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–103.CrossRefGoogle Scholar
  69. Six J, Conant RT, Paul EA, Paustian K. 2002. Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–76.CrossRefGoogle Scholar
  70. Six J, Bossuyt H, Degryze S, Denef K. 2004. A history of research on the link between (micro) aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31.CrossRefGoogle Scholar
  71. Sun T, Chen Q, Chen Y, Cruse R, Li X, Song C, Kravchenko Y, Zhang X. 2014. A novel soil wetting technique for measuring wet stable aggregates. Soil Tillage Res 141:19–24.CrossRefGoogle Scholar
  72. Tisdall JM, Oades JM. 1982. Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–63.CrossRefGoogle Scholar
  73. Wang Q, An SQ, Ma ZJ, Zhao B, Chen JK, Li B. 2006. Invasive Spartina alterniflora: biology, ecology, and management. Acta Phytotaxon Sin 44:559–88.CrossRefGoogle Scholar
  74. Wang D, Zhang R, Xiong J, Guo HQ, Zhao B. 2015. Contribution of invasive species Spartina alterniflora to soil organic carbon pool in coastal wetland: stable isotope approach. Chin J Plant Ecol 39:941–9 (in Chinese, with English abstract).CrossRefGoogle Scholar
  75. Wilson GWT, Rice CW, Rillig MC, Springer A, Hartnett DC. 2009. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–61.CrossRefPubMedGoogle Scholar
  76. Windham L, Ehrenfeld JG. 2003. Net impact of a plant invasion on nitrogen-cycling processes within a brackish tidal marsh. Ecol Appl 13:883–97.CrossRefGoogle Scholar
  77. Wooller M, Smallwood B, Jacobson M, Fogel M. 2003. Carbon and nitrogen stable isotopic in Laguncularia racemosa (L.) (white mangrove) from Florida and Belize: implications for trophic level studies. Hydrobiologia 499:13–23.CrossRefGoogle Scholar
  78. Yang SG, Li JH, Zheng Z, Meng Z. 2009. Characterization of Spartina alterniflora as feedstock for anaerobic digestion. Biomass Bioenergy 33:597–602.CrossRefGoogle Scholar
  79. Yang W, Jeelani N, Leng X, Cheng XL, An XQ. 2016. Spartina alterniflora invasion alters soil microbial community composition and microbial respiration following invasion chronosequence in a coastal wetland of China. Sci Rep 6:26880.  https://doi.org/10.1038/srep26880.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Zhang YH, Ding WX, Luo JF, Donnison A. 2010. Changes in soil organic carbon dynamics in an Eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora. Soil Biol Biochem 42:1712–20.CrossRefGoogle Scholar
  81. Zhao B, Yan Y, Guo HQ, He MM, Gu YJ, Li B. 2009. Monitoring rapid vegetation succession in estuarine wetland using time series MODIS-based indicators: an application in the Yangtze River Delta area. Ecol Indic 9:346–56.CrossRefGoogle Scholar
  82. Zuazo VHD, Pleguezuelo CRR. 2008. Soil-erosion and runoff prevention by plant covers: a review. Agron Sustain Dev 28:65–86.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Yanghui He
    • 1
    • 2
    • 3
  • Xuhui Zhou
    • 1
    • 4
    Email author
  • Weisong Cheng
    • 1
  • Lingyan Zhou
    • 1
  • Guodong Zhang
    • 2
  • Guiyao Zhou
    • 1
  • Ruiqiang Liu
    • 1
  • Junjiong Shao
    • 1
  • Kai Zhu
    • 3
  • Weixin Cheng
    • 3
  1. 1.Center for Global Change and Ecological Forecasting, Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration, School of Ecological and Environmental SciencesEast China Normal UniversityShanghaiChina
  2. 2.Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, The Institute of Biodiversity Science, School of Life SciencesFudan UniversityShanghaiChina
  3. 3.Environmental Studies DepartmentUniversity of CaliforniaSanta CruzUSA
  4. 4.Shanghai Institute of Pollution Control and Ecological SecurityShanghaiChina

Personalised recommendations