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Effects of shrub encroachment on vertical changes in soil organic carbon in Mongolian grasslands: using a multi-biomarker approach

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Abstract

Aims

In recent decades, ecologists have investigated the effects of shrub encroachment on regional carbon cycling in semi-arid and arid regions. Although differences in carbon sequestration and stocks have been recognized in different soil layers, the vertical changes in soil organic carbon (SOC) at the molecular level following shrub encroachment remain unexplored. In this study, we used biomarkers to assess the impacts of shrub encroachment on SOC composition.

Methods

We collected soil samples along the 1-m profile within shrub patches and grassy matrix in three typical shrub-encroached grassland (SEG) sites in Inner Mongolia, and quantified the vertical distribution of the biomarkers, including free lipids, bound lipids and lignin-derived phenols.

Results

The principal component analysis (PCA) of the biomarker data showed that samples in the grassy matrix had strong positive loadings along the first two components (PCs); in contrast, samples in the upper 50 cm of the shrub patches had negative loadings along the first component (PC1) as well as a narrower range. The acid to aldehyde ratios of the vanillyl and syringyl type monomers increased simultaneously along the 1-m profile in the grassy matrix; however, this trend was not observed in the shrub patches. In addition, the vanillyls to syringyls to cinnamyls ratio was approximately 3:2:1 in the shrub patches and 3:2:1 or 2:2:1 in the grassy matrix.

Conclusions

Shrub encroachment altered the vertical patterns in SOC composition, especially in the upper 50 cm, as well as the oxidation status of lignin-derived phenols along the entire 1-m profile. Further, shrub encroachment influenced the soil carbon composition under the shrub canopy as well as in the grassy matrix due to the sprawling canopies and the horizontal extension of the root systems of the encroaching shrubs. These results provided new insights into the vertical patterns of SOC changes after shrub encroachment at the molecular level and have important implications for understanding the mechanisms of soil carbon dynamics with changes in vegetation structure and composition.

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References

  • Andersson RA, Kuhry P, Meyers P, Zebühr Y (2011) Impacts of paleohydrological changes on n-alkane biomarker compositions of a holocene peat sequence in the eastern European Russian Arctic. Org Geochem 42:1065–1075

    Article  CAS  Google Scholar 

  • Angst G, John S, Mueller CW, Kögel-Knabner I, Rethemeyer J (2016) Tracing the sources and spatial distribution of organic carbon in subsoils. Sci Rep 6. https://doi.org/10.1038/srep28974

  • Armas-Herrera CM, Dignac M, Rumpel C, Arbelo AD, Chabbi A (2016) Management effects on composition and dynamics of cutin and suberin in topsoil under agricultural use. Eur J Soil Sci 67:360–373

    Article  CAS  Google Scholar 

  • Bao H, Kao S, Lee T, Zehetner F, Huang J, Chang Y, Lu J, Lee J (2017) Distribution of organic carbon and lignin in soils in a subtropical small mountainous river basin. Geoderma 306:81–88

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blaser WJ, Shanungu GK, Edwards PJ, Olde Venterink H (2014) Woody encroachment reduces nutrient limitation and promotes soil carbon sequestration. Ecol Evol 4:1423–1438

    Article  PubMed  PubMed Central  Google Scholar 

  • Briske DD (2017) Rangeland systems: processes, management and challenges. Springer. https://doi.org/10.1007/978-3-319-46709-2

    Google Scholar 

  • Bull ID, Nott CJ, van Bergen PF, Poulton PR, Evershed RP (2000) Organic geochemical studies of soils from the rothamsted classical experiments-VI. The occurrence of organic acids in an experimental grassland soil. Soil Biol Biochem 32:1367–1376

    Article  CAS  Google Scholar 

  • Cai Y, Tang Z, Xiong G, Xie Z, Liu Z, Feng X (2017) Different composition and distribution patterns of mineral-protected versus hydrolysable lipids in shrubland soils. J Geophys Res Biogeosci 122:2206–2218

    Article  CAS  Google Scholar 

  • Chen L, Li H, Zhang P, Zhao X, Zhou L, Liu T, Hu H, Bai Y, Shen H, Fang J (2015) Climate and native grassland vegetation as drivers of the community structures of shrub-encroached grasslands in Inner Mongolia, China. Landsc Ecol 30:1627–1641

    Article  Google Scholar 

  • Crow SE, Lajtha K, Filley TR, Swanston CW, Bowden RD, Caldwell BA (2009) Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Glob Chang Biol 15:2003–2019

    Article  Google Scholar 

  • Doetterl S, Stevens A, Six J, Merckx R, Oost KV, Pinto MC, Casanova-Katny A, Muñoz C, Boudin M, Venegas EZ, Boeckx P (2015) Soil carbon storage controlled by interactions between geochemistry and climate. Nat Geosci 8:780–783

    Article  CAS  Google Scholar 

  • Eldridge DJ, Bowker MA, Maestre FT, Roger E, Reynolds JF, Whitford WG (2011) Impacts of shrub encroachment on ecosystem structure and functioning: towards a global synthesis. Ecol Lett 14:709–722

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng X, Simpson MJ (2007) The distribution and degradation of biomarkers in Alberta grassland soil profiles. Org Geochem 38:1558–1570

    Article  CAS  Google Scholar 

  • Feng X, Simpson MJ (2011) Molecular-level methods for monitoring soil organic matter responses to global climate change. J Environ Monit 13:1246–1254

    Article  CAS  PubMed  Google Scholar 

  • Feng X, Simpson AJ, Schlesinger WH, Simpson MJ (2010) Altered microbial community structure and organic matter composition under elevated CO2 and n fertilization in the Duke forest. Glob Chang Biol 16:2104–2116

    Article  Google Scholar 

  • Filley TR, Boutton TW, Liao JD, Jastrow JD, Gamblin DE (2008) Chemical changes to nonaggregated particulate soil organic matter following grassland-to-woodland transition in a subtropical savanna. J Geophys Res 113:G03009

    Google Scholar 

  • Han L, Sun K, Jin J, Xing B (2016) Some concepts of soil organic carbon characteristics and mineral interaction from a review of literature. Soil Biol Biochem 94:107–121

    Article  CAS  Google Scholar 

  • Hedges JI, Mann DC (1979) The characterization of plant tissues by their lignin oxidation products. Geochim Cosmochim Ac 43:1803–1807

    Article  CAS  Google Scholar 

  • Hedges JI, Blanchette RA, Weliky K, Devol AH (1988) Effects of fungal degradation on the CuO oxidation products of lignin: a controlled laboratory study. Geochim Cosmochim Ac 52:2717–2726

    Article  CAS  Google Scholar 

  • Hughes RF, Archer SR, Asner GP, Wessman CA, McMurtry C, Nelson JIM, Ansley RJ (2006) Changes in aboveground primary production and carbon and nitrogen pools accompanying woody plant encroachment in a temperate savanna. Glob Chang Biol 12:1733–1747

    Article  Google Scholar 

  • IUSS Working Group WRB (2015) World reference base for soil resources 2014, update 2015 international soil classification system for naming soils and creating legends for soil maps. World Soil resources Reports No. 106. FAO, Rome

  • Jackson RB, Banner JL, Jobbágy EG, Pockman WT, Wall DH (2002) Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–626

    Article  CAS  PubMed  Google Scholar 

  • Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436

    Article  Google Scholar 

  • Knapp AK, Briggs JM, Collins SL, Archer SR, Bret-Harte MS, Ewers BE, Peters DP, Young DR, Shaver GR, Pendall E, Cleary MB (2008) Shrub encroachment in north American grasslands: shifts in growth form dominance rapidly alters control of ecosystem carbon inputs. Glob Chang Biol 14:615–623

    Article  Google Scholar 

  • Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162

    Article  Google Scholar 

  • Kögel-Knabner I (2017) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter: fourteen years on. Soil Biol Biochem 105:A3–A8

    Article  CAS  Google Scholar 

  • Lam TBT, Kadoya K, Iiyama K (2001) Bonding of hydroxycinnamic acids to lignin: Ferulic and p-coumaric acids are predominantly linked at the benzyl position of lignin, not the β-position, in grass cell walls. Phytochemistry 57:987–992

    Article  CAS  PubMed  Google Scholar 

  • Li H (2015) Effects of shrub encroachment on soil organic carbon pool in Inner-Mongolia, China. PhD thesis, Institute of Botany, Chinese Academy of Sciences, Beijing

  • Li H, Shen H, Chen L, Liu T, Hu H, Zhao X, Zhou L, Zhang P, Fang J (2016) Effects of shrub encroachment on soil organic carbon in global grasslands. Sci Rep 6:28974

    Article  PubMed  PubMed Central  Google Scholar 

  • Maestre FT, Bowker MA, Puche MD, Belén Hinojosa M, Martínez I, García-Palacios P, Castillo AP, Soliveres S, Luzuriaga AL, Sánchez AM (2009) Shrub encroachment can reverse desertification in semi-arid Mediterranean grasslands. Ecol Lett 12:930–941

    Article  PubMed  Google Scholar 

  • National soil survey office (1994) A database of soil types in China. China Agriculture Press, Beijing

    Google Scholar 

  • Nguyen Tu TT, Egasse C, Zeller B, Bardoux G, Biron P, Ponge J, David B, Derenne S (2011) Early degradation of plant alkanes in soils: a litterbag experiment using C-13-labelled leaves. Soil Biol Biochem 43:2222–2228

    Article  CAS  Google Scholar 

  • Nierop KGJ (1998) Origin of aliphatic compounds in a forest soil. Org Geochem 29:1009–1016

    Article  CAS  Google Scholar 

  • Nierop KGJ, Naafs DFW, Verstraten JM (2003) Occurrence and distribution of ester-bound lipids in dutch coastal dune soils along a pH gradient. Org Geochem 34:719–729

    Article  CAS  Google Scholar 

  • Niu C, Alamusa ZQ, Luo Y, Toshio O, Sun G, Liu Q (2013) Allocation patterns of above- and below-ground biomass of Caragana microphylla in Horqin Sandy land, North China. China J Eco 32:1980–1986

    Google Scholar 

  • Oelofse M, Birch-Thomsen T, Magid J, de Neergaard A, van Deventer R, Bruun S, Hill T (2016) The impact of black wattle encroachment of indigenous grasslands on soil carbon, eastern Sape, South Africa. Biol Invasions 18:445–456

    Article  Google Scholar 

  • Otto A, Simpson MJ (2005) Degradation and preservation of vascular plant-derived biomarkers in grassland and forest soils from Western Canada. Biogeochemistry 74:377–409

    Article  CAS  Google Scholar 

  • Otto A, Simpson MJ (2006) Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry 80:121–142

    Article  CAS  Google Scholar 

  • Otto A, Shunthirasingham C, Simpson MJ (2005) A comparison of plant and microbial biomarkers in grassland soils from the prairie ecozone of Canada. Org Geochem 36:425–448

    Article  CAS  Google Scholar 

  • Peng H, Li X, Jiang Z, Ma Y, Li G, Zhang Z, Zhang S, Li L, Zhao G (2013) Shrub encroachment with increasing anthropogenic disturbance in the semiarid Inner Mongolian grasslands of China. Catena 109:39–48

    Article  Google Scholar 

  • Peterson GG, Neill C (2003) Using soil 13C to detect the historic presence of Schizachyrium scoparium (little bluestem) grasslands on Martha’s vineyard. Restor Ecol 11:116–122

    Article  Google Scholar 

  • Pisani O, Frey SD, Simpson AJ, Simpson MJ (2015) Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level. Biogeochemistry 123:391–409

    Article  CAS  Google Scholar 

  • Pisani O, Haddix ML, Conant RT, Paul EA, Simpson MJ (2016) Molecular composition of soil organic matter with land-use change along a bi-continental mean annual temperature gradient. Sci Total Environ 573:470–480

    Article  CAS  PubMed  Google Scholar 

  • Rumpel C, Eusterhues K, Kögel-Knabner I (2004) Location and chemical composition of stabilized organic carbon in topsoil and subsoil horizons of two acid forest soils. Soil Biol Biochem 36:177–190

    Article  CAS  Google Scholar 

  • Rumpel C, Kögel-Knabner I (2011) Deep soil organic matter-a key but poorly understood component of terrestrial C cycle. Plant Soil 338:143–158

    Article  CAS  Google Scholar 

  • Saixiyala, Yang D, Zhang S, Liu G, Yang X, Huang Z, Ye X (2017) Facilitation by a spiny shrub on a rhizomatous clonal herbaceous in thicketization-grassland in northern China: Increased soil resources or shelter from herbivores. Front Plant Sci 8:809

  • Salomé C, Nunan N, Pouteau V, Lerch TZ, Chenu C (2010) Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob Chang Biol 16:416–426

    Article  Google Scholar 

  • Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DA, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    Article  CAS  PubMed  Google Scholar 

  • Steffens M, Kölbl A, Schörk E, Gschrey B, Kögel-Knabner I (2011) Distribution of soil organic matter between fractions and aggregate size classes in grazed semiarid steppe soil profiles. Plant Soil 338:63–81

    Article  CAS  Google Scholar 

  • Tamura M, Tharayil N (2014) Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystems. New Phytol 203:110–124

    Article  CAS  PubMed  Google Scholar 

  • Toriyama J, Kato T, Siregar CA, Siringoringo HH, Ohta S, Kiyono Y (2011) Comparison of depth- and mass-based approaches for estimating changes in forest soil carbon stocks: a case study in young plantations and secondary forests in west Java, Indonesia. Forest Ecol Manag 262:1659–1667

    Article  Google Scholar 

  • Van Auken OW (2009) Causes and consequences of woody plant encroachment into Western North American grasslands. J Environ Manag 90:2931–2942

    Article  Google Scholar 

  • Wang J, Guo Y, Yao Y, Tang J, Zhang M (2017) Distribution characteristics of root system and carbon stock of Caragana microphylla Lam, in Aohan sandificational area. Nat Sci Ed 45:103–110

    CAS  Google Scholar 

  • Wu M, Zhang Y, Song Y, Zhao B (2016) Study on soil texture of typical steppen in Central Inner Mongolia. Environ Dev 28:12–15

    Google Scholar 

  • Xiong X, Han X (2005) Spatial heterogeneity in soil carbon and nitrogen resources, caused by Caragana microphylla, in the thicketization of semiarid grassland, Inner Mongolia. Acta Ecolog ica Sinica 25:1678–1683

    CAS  Google Scholar 

  • Zhang L, Wang X, Zhang W, Hu E, Hai L (2013) Study on population structure and spatial distribution characteristic of Amygdalus pedunculata in two habitats. J Arid Land Resour Environ 27:124–129

    Google Scholar 

  • Zhao L, Wu W, Xu X, Xu Y (2014) Soil organic matter dynamics under different land use in grasslands in Inner Mongolia (northern China). Biogeosciences 11:5103–5113

    Article  Google Scholar 

  • Zhou L, Li H, Shen H, Xu Y, Wang Y, Xing A, Fang J (2017a) Shrub-encroachment induced alterations in input chemistry and soil microbial community affect topsoil organic carbon in an inner Mongolian grassland. Biogeochemistry 136:311–324

    Article  CAS  Google Scholar 

  • Zhou Y, Boutton TW, Wu XB, McCulley R (2017b) Soil carbon response to woody plant encroachment: importance of spatial heterogeneity and deep soil storage. J Ecology 105:1738–1749

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by the National Natural Science Foundation of China (31330012, 31470525), the National Basic Research Program of China on Global Change (2014CB954001), the Key Research Program of Frontier Sciences, CAS, (QYZDY-SSW-SMC011).

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Authors and Affiliations

  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Luhong Zhou, He Li, Haihua Shen, Aijun Xing, Yankun Zhu & Jingyun Fang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Luhong Zhou, Haihua Shen, Aijun Xing, Yankun Zhu & Jingyun Fang

  3. Shanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China

    Yunping Xu

  4. College of Urban and Environmental Sciences, and Key Laboratory of Earth Surface Processes of the Ministry of Education, Peking University, Beijing, 100871, China

    Yinghui Wang, Shangzhe Zhou & Jingyun Fang

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  1. Luhong Zhou
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  2. He Li
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  3. Haihua Shen
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Correspondence to Jingyun Fang.

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Zhou, L., Li, H., Shen, H. et al. Effects of shrub encroachment on vertical changes in soil organic carbon in Mongolian grasslands: using a multi-biomarker approach. Plant Soil 431, 217–230 (2018). https://doi.org/10.1007/s11104-018-3761-z

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