Skip to main content
SpringerLink
Log in

Ground bryophytes regulate net soil carbon efflux: evidence from two subalpine ecosystems on the east edge of the Tibet Plateau

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Given the broad distribution of bryophytes and their prominence in alpine and high latitude ecosystems, to generate a better understanding of how bryophyte communities influence soil CO2 efflux is essential for increasing our comprehension of the global C cycle.

Methods

We measured CO2 efflux from bryophyte-covered and bryophyte-removed soil surface in two subalpine ecosystems: a conifer dominated forest and an ericaceous dominated shrubland, on the east edge of Tibetan Plateau. In addition, soil temperature (T soil), soil water content (SWC), total soil organic C (SOC), dissolved organic C (DOC) and microbial community structure were measured as possible drivers of the bryophyte-effects.

Results

Bryophyte removal resulted in reduced floor (bryophyte + soil) and mineral soil CO2 efflux, SOC, DOC, microbial biomass C (MBC) and phospholipid fatty acid (PLFA) concentrations, and caused a change in soil microbial community in the two ecosystems. The higher soil CO2 emissions from the bryophyte-covered, relative to the bare soil, was not caused by the changes in T soil and SWC, rather, it was consistent with the higher SOC, DOC, MBC and/or the PLFAs contents in the plots with bryophytes.

Conclusion

Our results highlight bryophytes are regulators of soil C efflux in subalpine ecosystems. Incorporating the effects of bryophytes will help improve the accuracy of current ecosystem C cycling models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

C:

carbon

CO2 :

carbon dioxide

T soil :

soil temperature

SWC:

soil water content

SOC:

total soil organic carbon

DOC:

dissolved organic carbon

MBC:

microbial biomass carbon

PLFA:

phospholipid fatty acid

References

  • Bergeron O, Margolis HA, Coursolle C (2009) Forest floor carbon exchange of a boreal black spruce forest in eastern North America. Biogeosciences 6:1849–1864

    Article  CAS  Google Scholar 

  • Beringer J, Lynch AH, Chapin FS, Mack M, Bonan GB (2001) The representation of arctic soils in the land surface model: the importance of mosses. J Clim 14:3324–3335

    Article  Google Scholar 

  • Bona KA, Fyles JW, Shaw C, Kurz WA (2013) Are mosses required to accurately predict upland black spruce forest soil carbon in national-scale forest C accounting models? Ecosystems 16:1071–1086

    Article  CAS  Google Scholar 

  • Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12

    Article  CAS  PubMed  Google Scholar 

  • Botting RS, Fredeen AL (2006) Net ecosystem CO2 exchange for moss and lichen dominated forest floors of old-growth sub-boreal spruce forests in central British Columbia, Canada. For Ecol Manag 235:240–251

    Article  Google Scholar 

  • Budge K, Leifeld J, Egli M, Fuhrer J (2011) Soil microbial communities in (sub)alpine grasslands indicate a moderate shift towards new environmental conditions 11 years after soil translocation. Soil Biol Biochem 43:1148–1154

    Article  CAS  Google Scholar 

  • Cannone N, Binelli G, Worland R, Convey P, Guglielmin M (2012) CO2 fluxes among different vegetation types during the growing season in Marguerite Bay (Antarctic peninsula). Geoderma 189-190:595–605

    Article  CAS  Google Scholar 

  • Carleton TJ, Read DJ (1991) Ectomycorrhizas and nutrient transfer in conifer feather moss ecosystems. Can J Bot 69:778–785

    Article  Google Scholar 

  • Chapin FS III, Shaver GR (1988) Differences in carbon and nutrient fractions among arctic growth forms. Oecologia 77:506–514

    Article  PubMed  Google Scholar 

  • Coxson DS (1991) Nutrient release from epiphytic bryophytes in tropical montane rain forest (Guadeloupe). Can J Bot 69:2122–2129

    Article  Google Scholar 

  • Coxson DS, Mcintyre DD, Vogel HJ (1992) Pulse release of sugars and polyols from canopy bryophytes in tropical montane rain forest Guadeloupe French West Indies. Biotropica 24:121–133

    Article  Google Scholar 

  • Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621–632

    Article  PubMed  Google Scholar 

  • Davey MC, Rothery P (1997) Interspecific variation in respiratory and photosynthetic parameters in Antarctic bryophytes. New Phytol 137:231–240

    Article  Google Scholar 

  • De Long JR, Dorrepaal E, Kardol P, Nilsson M, Teuber LM, Wardle DA (2016) Understory plant functional groups and litter species identity are stronger drivers of litter decomposition than warming along a boreal forest post-fire successional gradient. Soil Biol Biochem 98:159–170

    Article  CAS  Google Scholar 

  • De Sá Mendonça E, La Scala JN, Panosso AR, Simas FNB, Schaefer CEGR (2011) Spatial variability models of CO2 emissions from soils colonized by grass (Deschampsia antarctica) and moss (Sanionia uncinata) in Admiralty Bay, king George Island. Antarct Sci 23:27–33

    Article  Google Scholar 

  • Delucia EH, Turnbull MH, Walcroft A, Griffin K, Tissue D, Glenny D, Mcseveny TM, Whitehead D (2003) The contribution of bryophytes to the carbon exchange for a temperate rainforest. Glob Chang Biol 9:1158–1170

    Article  Google Scholar 

  • Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462

    Article  CAS  Google Scholar 

  • Federle TW (1986) Microbial distribution in the soil–new techniques. In: Megusar F, Gantar M (eds) Perspectives in microbial Ecology. Slovene Society for Microbiology, Ljubljana, pp 493–498

    Google Scholar 

  • Fenton NJ, Bergeron Y, Paré D (2010) Decomposition rates of bryophytes in managed boreal forests: influence of bryophyte species and forest harvesting. Plant Soil 336:499–508

    Article  CAS  Google Scholar 

  • Flanagan LB, Kubien DS, Ehleringer JR (1999) Spatial and temporal variation in the carbon and oxygen stable isotope ratio of respired CO2 in a boreal forest ecosystem. Tellus 51B:367–384

    Article  CAS  Google Scholar 

  • Frostegård Å, Tunlidb A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

    PubMed  PubMed Central  Google Scholar 

  • Garcia-Pichel F, Johnson SL, Youngkin D, Belnap J (2003) Small scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado Plateau. Microb Ecol 46:312–321

    Article  CAS  PubMed  Google Scholar 

  • Gaumont-Guay D, Black TA, Barr AG, Jassal RS, Nesic Z (2008) Biophysical controls on rhizospheric and heterotrophic components of soil respiration in a boreal black spruce stand. Tree Physiol 28:161–171

    Article  CAS  PubMed  Google Scholar 

  • Gaumont-Guay D, Black TA, Barr AG, Griffis TJ, Jassal RS, Krishnan P, Grant N, Nesic Z (2014) Eight years of forest–floor CO2 exchange in a boreal black spruce forest: Spatial integration and long–term temporal trends. Agric For Meteorol 184:25–35

    Article  Google Scholar 

  • Gornall JL, Jónsdóttir IS, Woodin SJ, Van der Wal R (2007) Arctic mosses govern below–ground environment and ecosystem processes. Oecologia 153:931–941

    Article  CAS  PubMed  Google Scholar 

  • Gornall JL, Woodin SJ, Jónsdóttir IS, Van der Wal R (2009) Herbivore impacts to the moss layer determine tundra ecosystem response to grazing and warming. Oecologia 161:747–758

    Article  PubMed  Google Scholar 

  • Goulden ML, Crill PM (1997) Automated measurements of CO2 exchange at the moss surface of a black spruce forest. Tree Physiol 17:537–542

    Article  CAS  PubMed  Google Scholar 

  • Gupta RK (1977) A study of photosynthesis and leakage of solutes in relation to the desiccation effects in bryophytes. Can J Bot 55:1186–1194

    Article  CAS  Google Scholar 

  • Gurlevik N, Kelting DL, Allen HL (2004) Nitrogen mineralization following vegetation control and fertilization in a 14–year–old loblolly pine plantation. Soil Sci Soc Am J 68:272–281

    Article  CAS  Google Scholar 

  • Hagemann U, Moroni M, Glibner J, Makeschine F (2010) Accumulation and preservation of dead wood upon burial by bryophytes. Ecosystems 13:600–611

    Article  CAS  Google Scholar 

  • Harden JW, O’Neill KP, Trumbore SE, Veldhuis H, Stocks BJ (1997) Moss and soil contributions to the annual net carbon flux of a maturing boreal forest. J Geophys Res 102:28805–28816

    Article  CAS  Google Scholar 

  • Hebel CL, Smith JE, Cromack K (2009) Invasive plant species and soil microbial response to wildfire burn severity in the Cascade range of Oregon. Appl Soil Ecol 42:150–159

    Article  Google Scholar 

  • Hinzman LD, Kane DL, Gieck RE, Everett KR (1991) Hydrologic and thermal–properties of the active layer in the Alaskan Arctic. Cold Reg Sci Tech 19:95–110

    Article  Google Scholar 

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522

    Article  Google Scholar 

  • Hobbie SE, Schimel JP, Trumbore SE, Randerson JR (2000) Controls over carbon storage and turnover in high–latitude soils. Global Chang Biol 6:196–210

    Article  Google Scholar 

  • Jackson BG, Nilsson MC, Wardle DA (2013) The effects of the moss layer on the decomposition of intercepted vascular plant litter across a post-fire boreal forest chronosequence. Plant Soil 367:199–214

    Article  CAS  Google Scholar 

  • Kanerva T, Palojärvi A, Rämö K, Manninen S (2008) Changes in soil microbial community structure under elevated tropospheric O3 and CO2. Soil Biol Biochem 40:2502–2510

    Article  CAS  Google Scholar 

  • Laganière J, Paré D, Bergeron Y, Chen HYH (2012) The effect of boreal forest composition on soil respiration is mediated through variations in soil temperature and C quality. Soil Biol Biochem 53:18–27

    Article  Google Scholar 

  • Leckie SE, Prescott CE, Grayston SJ, Neufeld JD, Mohn WW (2004) Comparison of chloroform fumigation–extraction, phospholipid fatty acid, and DNA methods to determine microbial biomass in forest humus. Soil Biol Biochem 36:529–532

    Article  CAS  Google Scholar 

  • Lindo Z, Gonzalez A (2010) The bryosphere: an integral and influential component of the earth’s biosphere. Ecosystems 13:612–627

    Article  Google Scholar 

  • Lindo Z, Nilsson MC, Gundale MJ (2013) Bryophyte-cyanobacteria associations as regulators of the northern latitude carbon balance in response to global change. Glob Chang Biol 19:2022–2035

    Article  PubMed  Google Scholar 

  • Longton RE (1992) The role of bryophytes and lichens in terrestrial systems. In: Bates JW, Farmer AM (eds) Bryophytes and lichens in a changing environment. Oxford University Press, New York, pp 32–76

    Google Scholar 

  • Luthin JN, Guymon GL (1974) Soil moisture–vegetation–temperature relationships in central Alaska. J Hydrol 23:233–246

    Article  Google Scholar 

  • Mauclaire L, Pelz O, Thullner M, Abraham W, Zeyer J (2003) Assimilation of toluene carbon along a bacteria–protist food chain determined by 13C–enrichment of biomarker fatty acids. J Microbiol Meth 55:635–649

    Article  CAS  Google Scholar 

  • Moore TR, Bubier JL, Bledzki L (2007) Litter decomposition in temperate peatland ecosystems: the effect of substrate and site. Ecosystems 10:949–963

    Article  Google Scholar 

  • Nakane K, Kohno T, Horikoshi T, Nakatsubo T (1997) Soil carbon cycling at black spruce (Picea mariana) forest stands in Saskatchewan, Canada. J Geophys Res 102:28785–28793

    Article  CAS  Google Scholar 

  • Novak M, Zemanova L, Buzek F, Jackova I, Adamova M, Komarek A, Vile MA, Kelman WR, Stepanova M (2010) The effect of a reciprocal peat transplant between two contrasting central European sites on C cycling and C isotope ratios. Biogeosciences 7:921–932

    Article  CAS  Google Scholar 

  • O'Leary WM, Wilkinson SG (1988) Gram–positive bacteria C. In: Ratledge WM, Wilkinson SG (eds) Microbial Lipids, vol 1. Academic, London, pp 117–202

    Google Scholar 

  • Orwin KH, Ostle NJ (2012) Moss species effects on peatland carbon cycling after fire. Funct Ecol 26:829–836

    Article  Google Scholar 

  • Proctor MCF (2000) Physiological Ecology. In: Shaw AJ, Goffinet B (eds) Bryophyte biology. Cambridge University Press, Cambridge, pp 225–247

    Chapter  Google Scholar 

  • Pypker TG, Unsworth MH, Bond BJ (2006) The role of epiphytes in rainfall interception by forests in the Pacific northwest. II. Field measurements at the branch and canopy scale. Can J For Res 36:819–832

    Article  Google Scholar 

  • Royer-Tardif S, Bradley RL, Parsons WFJ (2010) Evidence that plant diversity and site productivity confer stability to forest floor microbial biomass. Soil Biol Biochem 42:813–821

    Article  CAS  Google Scholar 

  • Schindlbacher A, Rodler A, Kuffner M, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitt A, Glaser B (2011) Organic matter dynamics in a temperate forest soil following enhanced drying. Soil Biol Biochem 43:478–489

    Article  CAS  Google Scholar 

  • Sedia EG, Ehrenfeld JG (2005) Differential effects of lichens, mosses and grasses on respiration and nitrogen mineralization in soils of the New Jersey pinelands. Oecologia 144:137–147

    Article  PubMed  Google Scholar 

  • Sharratt BS (1997) Thermal conductivity and water retention of a black spruce forest floor. Soil Sci 162:576–582

    Article  CAS  Google Scholar 

  • Skre O, Oechel WC (1981) Moss functioning in different taiga ecosystems in interior Alaska I. Seasonal, phenotypic, and drought effects on photosynthesis and response patterns. Oecologia 48:50–59

    Article  CAS  PubMed  Google Scholar 

  • Smithwick EAH, Turner MG, Metzger KL, Balser TC (2005) Variation in NH4 + mineralization and microbial communities with stand age in lodgepole pine (Pinus contorta) forests, Yellowstone National Park (USA). Soil Biol Biochem 37:1546–1559

    Article  CAS  Google Scholar 

  • Street LE, Subke JA, Sommerkorn M, Sloan V, Ducrotoy H, Phoenix GK, Williams M (2013) The role of mosses in carbon uptake and partitioning in arctic vegetation. New Phytol 199:163–175

    Article  CAS  PubMed  Google Scholar 

  • Sun SQ, Wu YH, Wang GX, Zhou J, Yu D, Bing HJ, Luo J (2013) Bryophyte species richness and composition along an altitudinal gradient in Gongga Mountain, China. PLoS One 8:e58131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swanson RV, Flanagan LB (2001) Environmental regulation of carbon dioxide exchange at the forest floor in a boreal black spruce ecosystem. Agr For Meteorol 108:165–181

    Article  Google Scholar 

  • Thoms C, Gleixner G (2013) Seasonal differences in tree species’ influence on soil microbial communities. Soil Biol Biochem 66:239–248

    Article  CAS  Google Scholar 

  • Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106:395–409

    Article  Google Scholar 

  • Van Cleve K, Yarie J (1986) Interaction of temperature, moisture and soil chemistry in controlling nutrient cycling and ecosystem development in the taiga of Alaska. In: Van Cleve K, Chapin FS III, Flanagan PW, Viereck LA, Dyrness CT (eds) Forest ecosystems in the Alaskan taiga. A synthesis of structure and function. Springer, New York, pp 160–189

    Chapter  Google Scholar 

  • Vance E, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Waldrop MP, Zak DR, Sinsabaugh RL (2004) Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36:1443–1451

    Article  CAS  Google Scholar 

  • Wang YS, Wang YH (2003) Quick measurement of CH4, CO2 and N2O emissions from a short-plant ecosystem. Adv Atmos Sci 20:842–844

    Article  Google Scholar 

  • Wang C, Bond Lamberty B, Gower ST (2003) Carbon distribution of a well–and poorly–drained black spruce fire chronosequence. Glob Chang Biol 9:1066–1079

    Article  Google Scholar 

  • White DC, Stair JO, Ringelberg DB (1996) Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol Biotech 17:185–196

    Article  CAS  Google Scholar 

  • Wickland KP, Neff JC (2008) Decomposition of soil organic matter from boreal black spruce forest: environmental and chemical controls. Biogeochemistry 87:29–47

    Article  Google Scholar 

  • Williams TG, Flanagan LB (1998) Measuring and modeling environmental influences on photosynthetic gas exchange in sphagnum and Pleurozium. Plant Cell Environ 21:555–564

    Article  CAS  Google Scholar 

  • Wilson JA, Coxson DS (1999) Carbon flux in a subalpine spruce-fir forest: pulse release from Hylocomium splendens feather–moss mats. Can J Bot 77:564–569

    Google Scholar 

  • Woodin SJ, van der Wal R, Sommerkorn M, Gornall JL (2009) Differential allocation of carbon in mosses and grasses governs ecosystem sequestration: a 13C tracer study in the high Arctic. New Phytol 184:944–949

    Article  CAS  PubMed  Google Scholar 

  • Wu YP, Ding N, Wang G, Xu JM, Wu JJ, Brookes PC (2009) Effects of different soil weights, storage times and extraction methods on soil phospholipid fatty acid analyses. Geoderma 150:171–178

    Article  CAS  Google Scholar 

  • Yuan W, Liu S, Dong W, Liang S, Zhao S, Chen J, Xu W, Li X, Barr X, Black TA, Yan W, Goulden ML, Kulmala L, Lindroth A, Margolis HA, Matsuura Y, Moors E, van der Molen M, Ohta T, Pilegaard K, Varlagin A, Vesala T (2014) Differentiating moss from higher plants is critical in studying the carbon cycle of the boreal biome. Nat Commun 5:4270

    CAS  PubMed  Google Scholar 

  • Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294

    Article  CAS  PubMed  Google Scholar 

  • Zelles L (1999) Fatty acids patterns of phospholipids and lipopolysacharides in the characterisation of microbial communities in soil: a review. Biol Fert Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zimov SA, Chuprynin VI, Oreshko AP, Chapin FS, Reynolds JF, Chapin MC (1995) Steppe–tundra transition—a herbivore driven biome shift at the end of the Pleistocene. Am Nat 146:765–794

    Article  Google Scholar 

  • Zogg GP, Donald RZ, David BR, Neil WM, Kurt SP, David CW (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Biol Biochem 61:475–481

    CAS  Google Scholar 

Download references

Acknowledgements

The authors appreciate the support of the Alpine Ecosystem Observation and Experiment Station of Mt. Gongga and the Yanting Agro-ecological Experimental Station of Purple Soil, institute of mountain hazards and environment, CAS. This work was supported by the National Natural Science Foundation of China (grant numbers. 41473078, 41273096); the Key Laboratory of Mountain Surface Processes and Ecological Regulation, CAS.

Author information

Authors and Affiliations

  1. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, No. 9, Block 4, South Renmin Rd, Chengdu, 610041, China

    Shou-Qin Sun, Tao Liu, Yan-Hong Wu, Gen-Xu Wang, Bo Zhu, Yan-Qiang Wang & Ji Luo

  2. School of Environment and Forest Sciences, University of Washington, Box 352100, Seattle, WA, 98195-2100, USA

    Thomas Henry DeLuca

Authors
  1. Shou-Qin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan-Hong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gen-Xu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bo Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Thomas Henry DeLuca
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yan-Qiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ji Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shou-Qin Sun.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Hans Lambers.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, SQ., Liu, T., Wu, YH. et al. Ground bryophytes regulate net soil carbon efflux: evidence from two subalpine ecosystems on the east edge of the Tibet Plateau. Plant Soil 417, 363–375 (2017). https://doi.org/10.1007/s11104-017-3264-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3264-3

Keywords

Search

Navigation