Skip to main content

Advertisement

SpringerLink
Log in

Grazing effects on microbial community composition, growth and nutrient cycling in salt marsh and sand dune grasslands

  • Originl Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The effect of grazing by large herbivores on the microbial community and the ecosystem functions they provide are relatively unknown in grassland systems. In this study, the impact of grazing upon the size, composition and activity of the soil microbial community was measured in field experiments in two coastal ecosystems: one salt marsh and one sand dune grassland. Bacterial, fungal and total microbial biomass were not systematically affected by grazing across ecosystems, although, within an ecosystem, differences could be detected. Fungal-to-bacterial ratio did not differ with grazing for either habitat. Redundancy analysis showed that soil moisture, bulk density and root biomass significantly explained the composition of phospholipid fatty acid (PLFA) markers, dominated by the distinction between the two grassland habitats, but where the grazing effect could also be resolved. PLFA markers for Gram-positive bacteria were more proportionally abundant in un-grazed, and markers for Gram-negative bacteria in grazed grasslands. Bacterial growth rate (leucine incorporation) was highest in un-grazed salt marsh but did not vary with grazing intensity in the sand dune grassland. We conclude that grazing consistently affects the composition of the soil microbial community in semi-natural grasslands but that its influence is small (7 % of the total variation in PLFA composition), compared with differences between grassland types (89 %). The relatively small effect of grazing translated to small effects on measurements of soil microbial functions, including N and C mineralisation. This study is an early step toward assessing consequences of land-use change for global nutrient cycles driven by the microbial community.

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

Similar content being viewed by others

References

  • Bååth E (1994) Measurement of protein synthesis by soil bacterial assemblages with the leucine incorporation technique. Biol Fertil Soils 17:147–153

    Article  Google Scholar 

  • Bååth E, Pettersson M, Söderberg KH (2001) Adaptation of a rapid and economical microcentrifugation method to measure thymidine and leucine incorporation by soil bacteria. Soil Biol Biochem 33:1571–1574

    Article  Google Scholar 

  • Bakker JP, Leeuw J, Dijkema KS, Leendertse PC, Prins HHT, Rozema J (1993) Salt marshes along the coast of The Netherlands. Hydrobiologia 265:73–95

    Article  Google Scholar 

  • Ball DF (1964) Loss-on-ignition as an estimate of organic matter and organic carbon in non-calcareous soils. J Soil Sci 15:84–92

    Article  CAS  Google Scholar 

  • Bapiri A, Bååth E, Rousk J (2010) Drying-rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microb Ecol 60:419–428

    Article  PubMed  Google Scholar 

  • Bardgett RD, Jones AC, Jones DL, Kemmitt SJ, Cook R, Hobbs PJ (2001) Soil microbial community patterns related to the history and intensity of grazing in sub-montane ecosystems. Soil Biol Biochem 33:1653–1664

    Article  CAS  Google Scholar 

  • Barret M, Morrissey JP, O’Gara F (2011) Functional genomic analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743

    Article  CAS  Google Scholar 

  • Beare MH, Neely CL, Coleman DC, Hargrove WL (1991) Characterization of a substrate-induced respiration method for measuring fungal, bacterial and total microbial biomass on plant residues. Agric Ecosys Environ 34:65–73

    Article  Google Scholar 

  • Bengtson P, Bengtsson G (2007) Rapid turnover of DOC in temperate forests accounts for increased CO2 production at elevated temperatures. Ecol Lett 10:783–790

    Article  PubMed  Google Scholar 

  • Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725

    Article  CAS  Google Scholar 

  • Clegg CD (2006) Impact of cattle grazing and inorganic fertiliser additions to managed grasslands on the microbial community composition of soils. Appl Soil Ecol 31:73–82

    Article  Google Scholar 

  • Conant RT, Ryan MG, Ågren GI et al (2011) Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob Change Biol 17:3392–3404

    Article  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Curry JP (1994) Grassland invertebrates: ecology, influence on soil fertility and effects on plant growth. Chapman & Hall, London

    Google Scholar 

  • De Vries FT, Hoffland E, van Eekeren N, Brussaard L, Bloem J (2006) Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38:2092–2103

    Article  Google Scholar 

  • R Development Core Team (2011). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Ford H, Garbutt A, Jones L, Jones DL (2012) Grazing management in saltmarsh ecosystems drives invertebrate diversity, abundance and functional group structure. Insect Conserv Diver. doi:10.1111/j.1752-4598.2012.00202.x

  • Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from 2 soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

    PubMed  Google Scholar 

  • Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551

    Article  CAS  Google Scholar 

  • Hatch DJ, Lovell RD, Antil RS, Jarvis SC, Owen PM (2000) Nitrogen mineralization and microbial activity in permanent pastures amended with nitrogen fertilizer or dung. Biol Fertil Soils 30:288–293

    Article  Google Scholar 

  • Holdo M, Holt RD, Coughenour MB, Ritchie ME (2007) Plant productivity and soil nitrogen as a function of grazing, migration and fire in an African savanna. J Ecol 95:115–128

    Article  Google Scholar 

  • Iovieno P, Bååth E (2008) Effect of drying and rewetting on bacterial growth rates in soil. FEMS Microbiol Ecol 65:400–407

    Article  PubMed  CAS  Google Scholar 

  • Janišová M, Bartha S, Kiehl K, Dengler J (2011) Advances in the conservation of dry grasslands: introduction to contributions from the seventh European Dry Grassland Meeting. Plant Biosyst 145:507–513

    Article  Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480

    Article  CAS  Google Scholar 

  • Kirchman D (2001) Measuring bacterial biomass production and growth rates from leucine incorporation in natural aquatic environments. Meth Microbiol 30:227–237

    Article  CAS  Google Scholar 

  • Kirchman D, Knees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49:599–607

    PubMed  CAS  Google Scholar 

  • Kirschbaum MUF (2004) Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? Glob Change Biol 10:1870–1877

    Article  Google Scholar 

  • Klumpp K, Fontaine S, Attard E, Le Roux X, Gleixner G, Soussana JF (2009) Grazing triggers soil carbon loss by altering plant roots and their control on soil microbial community. J Ecol 97:876–885

    Article  CAS  Google Scholar 

  • Lambert R (2000) Practical management of grazed saltmarshes. In: Sherwood BR, Gardiner BG, Harris T (eds) British saltmarshes. Forrest Text, UK, pp 333–340

    Google Scholar 

  • Lopez-Sangil L, Rousk J, Wallander H, Casals P (2011) Microbial growth rate measurements reveal that land-use abandonment promotes a fungal dominance of SOM decomposition in grazed Mediterranean ecosystems. Biol Fertil Soils 47:129–138

    Article  Google Scholar 

  • Lovell RD, Jarvis SC (1996) Effect of cattle dung on soil microbial biomass C and N in a permanent pasture soil. Soil Biol Biochem 28:291–299

    Article  CAS  Google Scholar 

  • Lukac M, Godbold DL (2010) Fine root biomass and turnover in southern taiga estimated by root inclusion nets. Plant Soil 331:505–513

    Article  CAS  Google Scholar 

  • Luo Y, Zhou X (2006) Soil respiration and the environment. Academic, London, Elsevier

    Google Scholar 

  • Mawdsley JL, Bardgett RD (1997) Continuous defoliation of perennial ryegrass (Lolium perenne) and white clover (Trifolium repens) and associated changes in the composition and activity of the microbial population of an upland grassland soil. Biol Fertil Soils 24:52–58

    Article  CAS  Google Scholar 

  • Morris MG (2000) The effects of structure and its dynamics on the ecology and conservation of arthropods in British grasslands. Biol Conserv 95:129–142

    Article  Google Scholar 

  • Nilsson LO, Bååth E, Falkengren-Grerup U, Wallander H (2007) Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153:375–384

    Article  PubMed  Google Scholar 

  • O’leary W, Wilkinson S (1988) Gram-positive bacteria. In: Ratledge C, Wilkinson SC (eds) Microbial lipids. Academic, London, pp 117–202

    Google Scholar 

  • Olsson PA, Johnson NA (2005) Tracking carbon from the atmosphere to the rhizosphere. Ecol Lett 8:1264–1270

    Article  Google Scholar 

  • Piñeiro G, Paruelo JM, Oesterheld M, Jobbagy EG (2010) Pathways of grazing effects on soil organic carbon and nitrogen. Rangeland Ecol Manage 63:109–119

    Article  Google Scholar 

  • Plassmann K, Edwards-Jones G, Jones MLM (2009) The effects of low levels of nitrogen deposition and grazing on dune grassland. Sci Total Environ 407:1391–1404

    Article  PubMed  CAS  Google Scholar 

  • Plassmann K, Edwards-Jones G, Jones MLM (2010) Effects of long-term grazing management on sand dune vegetation of high conservation interest. Appl Veg Sci 13:100–112

    Article  Google Scholar 

  • Pykälä J (2003) Effects of restoration with cattle grazing on plant species composition and richness of semi-natural grasslands. Biodivers Conserv 12:2211–2226

    Article  Google Scholar 

  • Ritz K, McNicol JW, Nunan N, Grayston S, Millard P, Atkinson D, Gollotte A, Habeshaw D, Boag B, Clegg CD, Griffiths BS, Wheatley RE, Glover LA, McCaig AE, Prosser JI (2004) Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiol Ecol 49:191–205

    Article  PubMed  CAS  Google Scholar 

  • Rodwell JS (2000) British plant communities, volume 5. Maritime communities and vegetation of open habitats. Cambridge University Press, UK

    Google Scholar 

  • Rousk J, Bååth E (2007) Fungal and bacterial growth in soil with plant materials of different C/N ratios. FEMS Microbiol Ecol 62:258–267

    Article  PubMed  CAS  Google Scholar 

  • Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30

    Article  PubMed  CAS  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010a) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • Rousk J, Brookes PC, Bååth E (2010b) The microbial PLFA composition as affected by pH in an arable soil. Soil Biol Biochem 42:516–520

    Article  CAS  Google Scholar 

  • Rousk J, Brookes PC, Bååth E (2011a) Fungal and bacterial growth responses to N fertilization and pH in the 150-year ‘Park Grass’ UK grassland experiment. FEMS Microbiol Ecol 76:89–99

    Article  PubMed  CAS  Google Scholar 

  • Rousk J, Brookes PC, Glanville H, Jones DL (2011b) Lack of correlation between turnover of low-molecular weight dissolved organic carbon and differences in microbial community composition or growth across a soil pH gradient. Appl Environ Microbiol 77:2791–2795

    Article  PubMed  CAS  Google Scholar 

  • Rowe EC, Emmett BA, Smart SM, Frogbrook ZL (2011) A new net mineralisable nitrogen assay improves predictions of floristic composition. J Veg Sci 22:251–261

    Article  Google Scholar 

  • Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569

    Article  CAS  Google Scholar 

  • Smith RS, Shiel RS, Bardgett RD, Millward D, Corkhill P, Rolph G, Hobbs PJ, Peacock S (2003) Soil microbial community, fertility, vegetation and diversity as targets in the restoration management of a meadow grassland. J Appl Ecol 40:51–64

    Article  Google Scholar 

  • Söderberg KH, Probanza A, Jumpponen A, Bååth E (2004) The microbial community in the rhizosphere determined by community level physiological profiles (CLPP) and direct soil—and cfu—PLFA techniques. Appl Soil Ecol 25:135–145

    Article  Google Scholar 

  • Steer J, Harris JA (2000) Shifts in the microbial community in rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera. Soil Biol Biochem 32:869–878

    Article  CAS  Google Scholar 

  • Strickland MS, Rousk J (2010) Considering fungal: bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  CAS  Google Scholar 

  • Strijker D (2005) Marginal lands in Europe—causes of decline. Basic Appl Ecol 6:99–106

    Article  Google Scholar 

  • Taylor P (2006) Beyond conservation: shifting the paradigm of upland land use. ESRC trans-disciplinary seminar series: sustaining upland landscapes. Exeter University, UK

    Google Scholar 

  • Ter Braak CJF, Smilauer P (2003) CANOCO for Windows version 4.5. Biometris–Plant Research International, Wageningen

    Google Scholar 

  • Treonis AM, Ostle NJ, Stott AW, Primrose R, Grayston SJ, Ineson P (2004) Identification of groups of metabolically active rhizosphere microorganisms by stable isotope probing. Soil Biol Biochem 36:533–537

    Article  CAS  Google Scholar 

  • Van Groenigen KJ, Bloem J, Bååth E, Boeckx P, Rousk J, Bodé S, Forristal PD, Jones MB (2010) Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol Biochem 42:48–55

    Article  Google Scholar 

  • Vickery JA, Tallowin JR, Feber RE, Asteraki EJ, Atkinson PW, Fuller RJ, Brown VK (2001) The management of lowland neutral grasslands in Britain: effects of agricultural practices on birds and their food resources. J Appl Ecol 38:647–664

    Article  Google Scholar 

  • Waksman SA, Gerretsen FC (1931) Influences of temperature and moisture upon the nature and extent of decomposition of plant residues by micro-organisms. Ecology 12:33–60

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, vad der Putten WH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson SC (1988) Gram-negative bacteria. In: Ratledge C, Wilkinson SC (eds) Microbial lipids. Academic, London, pp 299–488

    Google Scholar 

Download references

Acknowledgments

We thank Inma Robinson for assistance with the respiration analyses. This study was funded as part of a NERC—Centre for Ecology and Hydrology project—NECO3610. JR was supported by grants from the Swedish Research Council (Vetenskapsrådet; Project No. 623-2009-7343 and 621-2011-5719). Thanks to Countryside Council for Wales and Natural England for access to field sites.

Author information

Authors and Affiliations

  1. Centre for Ecology and Hydrology, Environment Centre Wales, Deiniol Road, Bangor, UK

    H. Ford, A. Garbutt & L. Jones

  2. School of Environment, Natural Resources and Geography, Bangor University, Environment Centre Wales, Deiniol Road, Bangor, UK

    J. Rousk & D. L. Jones

  3. Section of Microbial Ecology, Department of Biology, Lund University, 22362, Lund, Sweden

    J. Rousk

Authors
  1. H. Ford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Rousk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Garbutt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. L. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. Ford.

Additional information

H. Ford and J. Rousk contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ford, H., Rousk, J., Garbutt, A. et al. Grazing effects on microbial community composition, growth and nutrient cycling in salt marsh and sand dune grasslands. Biol Fertil Soils 49, 89–98 (2013). https://doi.org/10.1007/s00374-012-0721-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-012-0721-2

Keywords

Search

Navigation