Skip to main content

Advertisement

Log in

Does the Aboveground Herbivore Assemblage Influence Soil Bacterial Community Composition and Richness in Subalpine Grasslands?

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Grassland ecosystems support large communities of aboveground herbivores that are known to directly and indirectly affect belowground properties such as the microbial community composition, richness, or biomass. Even though multiple species of functionally different herbivores coexist in grassland ecosystems, most studies have only considered the impact of a single group, i.e., large ungulates (mostly domestic livestock) on microbial communities. Thus, we investigated how the exclusion of four groups of functionally different herbivores affects bacterial community composition, richness, and biomass in two vegetation types with different grazing histories. We progressively excluded large, medium, and small mammals as well as invertebrate herbivores using exclosures at 18 subalpine grassland sites (9 per vegetation type). We assessed the bacterial community composition using terminal restriction fragment length polymorphism (T-RFLP) at each site and exclosure type during three consecutive growing seasons (2009–2011) for rhizosphere and mineral soil separately. In addition, we determined microbial biomass carbon (MBC), root biomass, plant carbon:nitrogen ratio, soil temperature, and soil moisture. Even though several of these variables were affected by herbivore exclusion and vegetation type, against our expectations, bacterial community composition, richness, or MBC were not. Yet, bacterial communities strongly differed between the three growing seasons as well as to some extent between our study sites. Thus, our study indicates that the spatiotemporal variability in soil microclimate has much stronger effects on the soil bacterial communities than the grazing regime or the composition of the vegetation in this high-elevation ecosystem.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Lieth H (1978) Pattern of primary productivity in the biosphere. Hutchinson & Ross, Stroudsberg

    Google Scholar 

  2. White RS, Murray S, Rohweder M (2000) Pilot analysis of global ecosystems: grassland ecosystems technical report. World Resources Institute, Washington

    Google Scholar 

  3. Wardle DA, Barker GM, Yeates GW, Bonner KI, Ghani A (2001) Introduced browsing mammals in New Zealand natural forests: aboveground and belowground consequences. Ecol Monogr 71:587–614

    Article  Google Scholar 

  4. Del-Val E, Crawley MJ (2005) What limits herb biomass in grasslands: competition or herbivory? Oecologia 142:202–211

    Article  PubMed  Google Scholar 

  5. Bakker ES, Ritchie ME, Olff H, Milchunas DG, Knops JMH (2006) Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecol Lett 9:780–788

    Article  PubMed  Google Scholar 

  6. Austrheim G, Mysterud A, Pedersen B, Halvoresen R, Hassel K, Evju M (2008) Large scale experimental effects of three levels of sheep densities on an alpine ecosystem. Oikos 117:837–846

    Article  Google Scholar 

  7. Zhou X, Wang J, Wang Y (2010) Intermediate grazing intensities by sheep increase soil bacterial diversities in an inner Mongolian steppe. Biol Fert Soils 46:817–824

    Article  Google Scholar 

  8. Binkley D, Singer F, Kaye M, Rochelle R (2003) Influence of elk grazing on soil properties in rocky mountain national park. For Ecol Manag 185:239–247

    Article  Google Scholar 

  9. Stark S, Wardle DA, Ohtonen R, Helle T, Yeates GW (2000) The effect of reindeer grazing on decomposition, mineralization and soil biota in a dry oligotrophic Scots pine forest. Oikos 90:301–310

    Article  Google Scholar 

  10. Bardgett RD, Leemans DK, Cook R, Hobbs PJ (1997) Seasonality of the soil biota of grazed and ungrazed hill grasslands. Soil Biol Biochem 29:1285–1294

    Article  CAS  Google Scholar 

  11. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268

    Article  Google Scholar 

  12. Holland JN, Cheng W, Crossley DA (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107:87–94

    Article  Google Scholar 

  13. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402

    Article  Google Scholar 

  14. Tracy BF, Frank DA (1998) Herbivore influence on soil microbial biomass and nitrogen mineralization in a northern grassland ecosystem: Yellowstone National Park. Oecologia 114:556–562

    Article  Google Scholar 

  15. Bakker ES, Olff H, Boekhoff M, Gleichmann JM, Berendse F (2004) Impact of herbivores on nitrogen cycling: contrasting effects of small and large species. Oecologia 138:91–101

    Article  CAS  PubMed  Google Scholar 

  16. Wang KH, McSorley R, Bohlen B, Gathumbi SM (2006) Cattle grazing increases microbial biomass and alters soil nematode communities in subtropical pastures. Soil Biol Biochem 38:1956–1965

    Article  CAS  Google Scholar 

  17. Bardgett RD, Hobbs PJ, Frostegård Å (1996) Changes in fungal:bacterial biomass ratios following reductions in the intensity of management on an upland grassland. Biol Fertil Soils 22:261–264

    Article  Google Scholar 

  18. 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 

  19. Klumpp K, Fontaine S, Attard E, Le Roux X, Gleixner G, Soussana J (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 

  20. Patra AK, Abbadie L, Clays-Josserand A, Degrange V, Grayston SJ, Loiseau P, Loualt F, Mahmood S, Nazaret S, Philippot L, Poly F, Prosser JI, Richaume A, Le Roux X (2005) Effects of grazing on microbial functional groups involved in soil dynamics. Ecol Monogr 75:65–80

    Article  Google Scholar 

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

    Article  Google Scholar 

  22. Orwin KH, Bertram JE, Clough TJ, Condron LM, Sherlock RR, O’Callaghan M, Ray J, Baird DB (2010) Impact of bovine urine deposition on soil microbial activity, biomass, and community structure. Appl Soil Ecol 44:89–100

    Article  Google Scholar 

  23. Holland JN (1995) Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems. Appl Soil Ecol 2:275–279

    Article  Google Scholar 

  24. MeteoSchweiz (2011) IDAWEB weather data portal. https://gate.meteoswiss.ch/idaweb/login.do?language = en. Accessed 10 Jan 2012

  25. Schütz M, Risch AC, Leuzinger E, Krüsi BO, Achermann G (2003) Impact of herbivory by red deer (Cervus elaphus L.) on patterns and processes in subalpine grasslands in the swiss national park. For Ecol Manag 181:177–88

    Article  Google Scholar 

  26. Schütz M, Risch AC, Achermann G, Thiel-Egenter C, Page-Dumroese DS, Jurgensen MF, Edwards PJ (2006) Phosphorus translocation by red deer on a subalpine grassland in the central European Alps. Ecosystems 9:624–633

    Article  Google Scholar 

  27. Haynes AG (2013) Trophic cascades in two contrasting plant communities: the effects of herbivore exclusion on grassland ecosystems. PhD thesis 21497, ETH Zurich

  28. Risch AC, Haynes AG, Busse MD, Filli F, Schütz M (2013) The response of soil CO2 fluxes to progressively excluding vertebrate and invertebrate herbivores depends on ecosystem type. Ecosystems 16:1192–1202

    Article  CAS  Google Scholar 

  29. Haynes AG, Schuetz M, Buchmann N, Page-Dumroese DS, Busse MD, Risch AC (2014) Linkages between grazing history and herbivore exclusion on decomposition rates in mineral soils of subalpine grasslands. Plant Soil 374:579–591

    Article  CAS  Google Scholar 

  30. Risch AC, Jurgensen MF, Page-Dumroese DS, Wildi O, Schütz M (2008) Long-term development of above- and belowground carbon stocks following land-use change in subalpine ecosystems of the Swiss National Park. Can J For Res 38:1590–1602

    Article  CAS  Google Scholar 

  31. Frey B, Kremer J, Rüdt A, Sciacca S, Matthies D, Lüscher P (2009) Compaction of forest soils with heavy logging machinery affects soil bacterial community structure. Eur J Soil Biol 45:312–320

    Article  Google Scholar 

  32. Hartmann M, Frey B, Kölliker R, Widmer F (2005) Semi-automated genetic analyses of soil microbial communities: comparison of T-RFLP and RISA based on descriptive and discriminative statistical approaches. J Microbiol Methods 61:349–360

    Article  CAS  PubMed  Google Scholar 

  33. Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biol Biochem 10:215–221

    Article  CAS  Google Scholar 

  34. Attard E, Degrange V, Klumpp K, Richaume A, Soussana JF, Le Roux X (2008) How do grassland management history and bacterial micro-localisation affect the response of bacterial community structure to changes in aboveground grazing regime? Soil Biol Biochem 40:1244–1252

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  36. Waldrop MP, Firestone MK (2006) Seasonal dynamics of microbial community composition and function in oak canopy and open grassland soils. Microl Ecol 52:470–479

    Article  CAS  Google Scholar 

  37. Grime JP (1977) Evidence fort he existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194

    Article  Google Scholar 

  38. Bardgett RD, Lovell RD, Hobbs PJ, Jarvis SC (1999) Seasonal changes in soil microbial communities along a fertility gradient of temperate grasslands. Soil Biol Biochem 31:1021–1030

    Article  CAS  Google Scholar 

  39. Bardgett RD, Leemans DK (1995) The short-term effects of cessation of fertilizer applications, liming and grazing on microbial biomass and activity in a reseeded upland grassland soil. Biol Fert Soils 19:148–154

    Article  Google Scholar 

  40. Bell C, McIntyre N, Cox S, Tissue D, Zak J (2008) Soil microbial responses to temporal variations of moisture and temperature in a Chihuahuan desert grassland. Microb Ecol 56:153–167

    Article  PubMed  Google Scholar 

  41. Liu W, Xu W, Hong J, Wan S (2010) Interannual variability of soil microbial biomass and respiration in response to topography, annual burning and N addition in a semiarid temperate steppe. Geoderma 158:259–267

    Article  CAS  Google Scholar 

  42. Garcia FO, Rice CW (1994) Microbial biomass dynamics in tall-grass prairie. Soil Sci Soc Am J 58:816–823

    Article  Google Scholar 

  43. Frank D, Esper J (2005) Characterization and climate response of high-elevation, multi-species tree-ring network in the European Alps. Dendrochronologia 22:107–121

    Article  Google Scholar 

  44. Cannone N, Sgorbati S, Guglielmin M (2007) Unexpected impacts of climate change on alpine vegetation. Front Ecology Environ 5:360–364

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank numerous interns and volunteers for their help with fence construction, data collection and laboratory work. Our special thanks go to Bigna Stoffel, Vera Baptista, Anna Schweiger, and Annatina Zingg for sorting the roots. We are grateful to the Swiss National Park for administrative support of our research. This study was funded by the Swiss National Science Foundation, SNF grant-no 31003A_122009/1 and SNF grant-no 31003A_140939/1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anita C. Risch.

Appendix

Appendix

Table 4 Average number of ungulate pellet groups 100 m−2, number of marmots counted, and average number of grasshoppers m−2 at each site for summer 2009 and 2010
Table 5 Interannual differences in bacterial community richness for both the mineral soil and the rhizosphere. Interannual differences in environmental variables microbial biomass (MBC; mg/kg), soil temperature in °C; soil moisture (%), plant material C:N ratio and root biomass (g/m2); values represent mean ± standard error. F = F value, p = p value; different letters indicate significantly different values

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hodel, M., Schütz, M., Vandegehuchte, M.L. et al. Does the Aboveground Herbivore Assemblage Influence Soil Bacterial Community Composition and Richness in Subalpine Grasslands?. Microb Ecol 68, 584–595 (2014). https://doi.org/10.1007/s00248-014-0435-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0435-0

Keywords

Navigation