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Plant and Soil

, Volume 366, Issue 1–2, pp 671–682 | Cite as

Response of soil microbial activity to grazing, nitrogen deposition, and exotic cover in a serpentine grassland

  • Ellen H. EschEmail author
  • Daniel L. Hernández
  • Jae R. Pasari
  • Rose S. G. Kantor
  • Paul C. Selmants
Regular Article

Abstract

Background and aims

Exotic species, nitrogen (N) deposition, and grazing are major drivers of change in grasslands. However little is known about the interactive effects of these factors on below-ground microbial communities.

Methods

We simulated realistic N deposition increases with low-level fertilization and manipulated grazing with fencing in a split-plot experiment in California’s largest serpentine grassland. We also monitored grazing intensity using camera traps and measured total available N to assess grazing and nutrient enrichment effects on microbial extracellular enzyme activity (EEA), microbial N mineralization, and respiration rates in soil.

Results

Continuous measures of grazing intensity and N availability showed that increased grazing and N were correlated with increased microbial activity and were stronger predictors than the categorical grazing and fertilization measures. Exotic cover was also generally correlated with increased microbial activity resulting from exotic-driven nutrient cycling alterations. Seasonal effects, on abiotic factors and plant phenology, were also an important factor in EEA with lower activity occurring at peak plant biomass.

Conclusions

In combination with previous studies from this serpentine grassland, our results suggest that grazing intensity and soil N availability may affect the soil microbial community indirectly via effects on exotic cover and associated changes in nutrient cycling while grazing directly impacts soil community function.

Keywords

California Cattle Extracellular enzyme activity Fertilization Festuca perennis Invasive species 

Abbreviations

CBH

Cellobiohydrolase

EEA

Extracellular enzyme assay

LAP

L-leucine aminopeptidase

NAG

β-1,4-N-acetylglucosaminidase

PHOS

Phosphatase

XYL

β-xylopyranoside

Notes

Acknowledgements

This research was supported by funding from the Kearney Foundation for Soil Science. We thank Christal Niederer for her assistance with fieldwork and Bonnie Keeler for her useful comments on this manuscript.

References

  1. Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems - hypotheses revisited. Bioscience 48(11):921–934CrossRefGoogle Scholar
  2. Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai'i. Oecologia 141(4):612–619. doi: 10.1007/S00442-004-1679-Z PubMedCrossRefGoogle Scholar
  3. Allison SD, Nielsen C, Hughes RF (2006) Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana. Soil Biol Biochem 38(7):1537–1544. doi: 10.1016/J.Soilbio.2005.11.008 CrossRefGoogle Scholar
  4. 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(2–3):148–154CrossRefGoogle Scholar
  5. Bardgett RD, Leemans DK, Cook R, Hobbs PJ (1997) Seasonality of the soil biota of grazed and ungrazed hill grasslands. Soil Biol Biochem 29(8):1285–1294CrossRefGoogle Scholar
  6. Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30(14):1867–1878CrossRefGoogle Scholar
  7. Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8(2):217–230. doi: 10.1007/s10530-004-3856-8 CrossRefGoogle Scholar
  8. Batten KM, Scow KM, Espeland EK (2008) Soil microbial community associated with an invasive grass differentially impacts native plant performance. Microb Ecol 55(2):220–228. doi: 10.1007/s00248-007-9269-3 PubMedCrossRefGoogle Scholar
  9. Bell TH, Klironomos JN, Henry HAL (2010) Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc Am J 74(3):820–828. doi: 10.2136/sssaj2009.0036 CrossRefGoogle Scholar
  10. Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40(2):344–353. doi: 10.1046/j.1365-2664.2003.00789.x CrossRefGoogle Scholar
  11. Carreiro M, Sinsabaugh R, Repert D, Parkhurst D (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81(9):2359–2365CrossRefGoogle Scholar
  12. Carson WP, Barrett GW (1988) Succession in old-field plant-communities - effects of contrasting types of nutrient enrichment. Ecology 69(4):984–994CrossRefGoogle Scholar
  13. Chen H, Liu J, Zhang YL, Wang Q, Ge XL, Wei YH, Wang RQ (2011) Influence of invasive plant Coreopsis grandiflora on functional diversity of soil microbial communities. J Environ Biol 32(5):567–572Google Scholar
  14. 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(1–2):73–82. doi: 10.1016/j.apsoil.2005.04.003 CrossRefGoogle Scholar
  15. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14(4):135–139PubMedCrossRefGoogle Scholar
  16. Dukes JS, Chiariello NR, Loarie SR, Field CB (2011) Strong response of an invasive plant species (Centaurea solstitialis L.) to global environmental changes. Ecol Appl 21(6):1887–1894PubMedCrossRefGoogle Scholar
  17. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6(6):503–523. doi: 10.1007/S10021-002-0151-3 CrossRefGoogle Scholar
  18. Ehrenfeld JG, Kourtev P, Huang WZ (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11(5):1287–1300CrossRefGoogle Scholar
  19. Elam DR, Wright DH, Goettle B (1998) Recovery plan for serpentine soil species of the San Francisco Bay area. Portland, OregonGoogle Scholar
  20. Fenn ME, Allen EB, Weiss SB, Jovan S, Geiser LH, Tonnesen GS, Johnson RF, Rao LE, Gimeno BS, Yuan F, Meixner T, Bytnerowicz A (2010) Nitrogen critical loads and management alternatives for N-impacted ecosystems in California. J Environ Manage 91(12):2404–2423. doi: 10.1016/J.Jenvman.2010.07.034 PubMedCrossRefGoogle Scholar
  21. Foreman CM, Franchini P, Sinsabaugh RL (1998) The trophic dynamics of riverine bacterioplankton: Relationships among substrate availability, ectoenzyme kinetics, and growth. Limnol Oceanogr 43(6):1344–1352CrossRefGoogle Scholar
  22. Franck VM, Hungate BA, Chapin FS, Field CB (1997) Decomposition of litter produced under elevated CO2: Dependence on plant species and nutrient supply. Biogeochemistry 36(3):223–237CrossRefGoogle Scholar
  23. Gelbard JL, Harrison S (2003) Roadless habitats as refuges for native grasslands: interactions with soil, aspect, and grazing. Ecol Appl 13(2):404–415CrossRefGoogle Scholar
  24. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43(7):1387–1397. doi: 10.1016/j.soilbio.2011.03.017 CrossRefGoogle Scholar
  25. Gutknecht JLM, Henry HAL, Balser TC (2010) Inter-annual variation in soil extra-cellular enzyme activity in response to simulated global change and fire disturbance. Pedobiologia 53(5):283–293. doi: 10.1016/j.pedobi.2010.02.001 CrossRefGoogle Scholar
  26. Henry HAL, Juarez JD, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Glob Change Biol 11(10):1808–1815CrossRefGoogle Scholar
  27. Hernandez DL, Hobbie SE (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335(1–2):397–411. doi: 10.1007/s11104-010-0428-9 CrossRefGoogle Scholar
  28. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion - implications for conservation. Conserv Biol 6(3):324–337CrossRefGoogle Scholar
  29. Hobbs RJ, Gulmon SL, Hobbs VJ, Mooney HA (1988) Effects of fertilizer addition and subsequent gopher disturbance on a serpentine annual grassland community. Oecologia 75(2):291–295CrossRefGoogle Scholar
  30. Holland EA, Detling JK (1990) Plant-response to herbivory and belowground nitrogen cycling. Ecology 71(3):1040–1049CrossRefGoogle Scholar
  31. Holly DC, Ervin GN, Jackson CR, Diehl SV, Kirker GT (2009) Effect of an invasive grass on ambient rates of decomposition and microbial community structure: A search for causality. Biol Invasions 11(8):1855–1868. doi: 10.1007/s10530-008-9364-5 CrossRefGoogle Scholar
  32. Holmes TH, Rice KJ (1996) Patterns of growth and soil-water utilization in some exotic annuals and native perennial bunchgrasses of California. Ann Bot-London 78(2):233–243CrossRefGoogle Scholar
  33. Holt JA (1997) Grazing pressure and soil carbon, microbial biomass and enzyme activities in semi-arid northeastern Australia. Appl Soil Ecol 5(2):143–149CrossRefGoogle Scholar
  34. Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71(2):478–491CrossRefGoogle Scholar
  35. ICF International (2010) Draft Santa Clara Valley habitat plan. Santa Clara CountyGoogle Scholar
  36. Jones JM, Evans RA (1960) Botanical composition changes in annual grassland as affected by ferlization and grazing. Agron J 52:459–461CrossRefGoogle Scholar
  37. Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: Implications for litter and soil organic matter decomposition. Ecosystems 12(1):1–15. doi: 10.1007/s10021-008-9199-z CrossRefGoogle Scholar
  38. Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83(11):3152–3166CrossRefGoogle Scholar
  39. Kourtev PS, Ehrenfeld JG, Haggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35(7):895–905. doi: 10.1016/s0038-0717(03)00120-2 CrossRefGoogle Scholar
  40. Liao CZ, Peng RH, Luo YQ, Zhou XH, Wu XW, Fang CM, Chen JK, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytol 177(3):706–714. doi: 10.1111/J.1469-8137.2007.02290.X PubMedCrossRefGoogle Scholar
  41. Maly MS, Barrett GW (1984) Effects of two types of nutrient enrichment on the structure and function of contrasting old-field communities. Am Midl Nat 111(2):342–357CrossRefGoogle Scholar
  42. Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA (1991) Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72(1):242–253CrossRefGoogle Scholar
  43. O'Dell RE, Claassen VP (2006) Relative performance of native and exotic grass species in response to amendment of drastically disturbed serpentine substrates. J Appl Ecol 43(5):898–908. doi: 10.1111/J.1365-2664.2006.01193.X CrossRefGoogle Scholar
  44. Ostertag R, Verville JH (2002) Fertilization with nitrogen and phosphorus increases abundance of non-native species in Hawaiian montane forests. Plant Ecol 162(1):77–90CrossRefGoogle Scholar
  45. Pasari JR (2011) Grassland invasion, management, and multifunctionality. Dissertation, University of California, Santa Cruz, Santa Cruz, CAGoogle Scholar
  46. Pasari JR, Selmants PC, Young H, O'Leary J, Zavaleta ES (2011) Nitrogen enrichment. In: Rejmanek M, Simberloff D (eds) The encyclopedia of invasive species. University of California Press, pp 488–492Google Scholar
  47. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2011) nlme: Linear and nonlinear mixed effects models. R package version 3.1–101Google Scholar
  48. Prieto LH, Bertiller MB, Carrera AL, Olivera NL (2011) Soil enzyme and microbial activities in a grazing ecosystem of Patagonian Monte, Argentina. Geoderma 162(3–4):281–287. doi: 10.1016/J.Geoderma.2011.02.011 CrossRefGoogle Scholar
  49. Safford HD, Harrison SP (2001) Grazing and substrate interact to affect native vs. exotic diversity in roadside grasslands. Ecol Appl 11(4):1112–1122CrossRefGoogle Scholar
  50. Saiya-Cork KR, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  51. Shariff AR, Biondini ME, Grygiel CE (1994) Grazing intensity effects on litter decomposition and soil-nitrogen mineralization. J Range Manage 47(6):444–449CrossRefGoogle Scholar
  52. Sinsabaugh RL (1994) Enzymatic analysis of microbial pattern and process. Biol Fert Soils 17(1):69–74CrossRefGoogle Scholar
  53. Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60(1):1–24CrossRefGoogle Scholar
  54. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11(11):1252–1264. doi: 10.1111/j.1461-0248.2008.01245.x PubMedGoogle Scholar
  55. Skopp J, Jawson MD, Doran JW (1990) Steady-state aerobic microbial activity as a function of soil-water content. Soil Sci Soc Am J 54(6):1619–1625CrossRefGoogle Scholar
  56. Stromberg MR, Corbin JD, D'Antonio CM (2007) California grasslands: ecology and management. University of California Press, Berkeley, CaliforniaGoogle Scholar
  57. Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microb Ecol 51(1):90–98. doi: 10.1007/s00248-005-5156-y PubMedCrossRefGoogle Scholar
  58. Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57(3):189–214CrossRefGoogle Scholar
  59. Treseder KK (2008) Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecol Lett 11(10):1111–1120. doi: 10.1111/J.1461-0248.2008.01230.X PubMedCrossRefGoogle Scholar
  60. Turitzin SN (1982) Nutrient limitations to plant growth in a California serpentine grassland. Am Midl Nat 107(1):95–99CrossRefGoogle Scholar
  61. Venables WN, Ripley BD (2002) Modern applied statistics with S, Fourthth edn. Springer, New YorkCrossRefGoogle Scholar
  62. Weiss SB (1999) Cars, cows, and checkerspot butterflies: nitrogen deposition and management of nutrient-poor grasslands for a threatened species. Conserv Biol 13(6):1476–1486CrossRefGoogle Scholar
  63. Weiss SB, Wright DH, Niederer C (2007) Serpentine vegetation management project. United States Fish and Wildlife ServiceGoogle Scholar
  64. Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55(6):477–487CrossRefGoogle Scholar
  65. Xu YQ, Li LH, Wang QB, Chen QS, Cheng WX (2007) The pattern between nitrogen mineralization and grazing intensities in an inner Mongolian typical steppe. Plant Soil 300(1–2):289–300. doi: 10.1007/S11104-007-9416-0 CrossRefGoogle Scholar
  66. Zeglin LH, Stursova M, Sinsabaugh RL, Collins SL (2007) Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia 154(2):349–359. doi: 10.1007/s00442-007-0836-6 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Ellen H. Esch
    • 1
    Email author
  • Daniel L. Hernández
    • 1
  • Jae R. Pasari
    • 2
  • Rose S. G. Kantor
    • 3
  • Paul C. Selmants
    • 4
  1. 1.Biology DepartmentCarleton CollegeNorthfieldUSA
  2. 2.Bodega Marine LaboratoryUniversity of California, DavisBodega BayUSA
  3. 3.Plant and Microbial BiologyUniversity of California, BerkeleyBerkeleyUSA
  4. 4.Department of Natural Resources and Environmental ManagementUniversity of Hawaii at ManoaHonoluluUSA

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