Biological Invasions

, Volume 12, Issue 2, pp 313–324 | Cite as

Introduced ungulate herbivore alters soil processes after fire

  • Michelle L. Stritar
  • Jennifer A. Schweitzer
  • Stephen C. Hart
  • Joseph K. Bailey
Original Paper

Abstract

Ungulate herbivory can have profound effects on ecosystem processes by altering organic inputs of leaves and roots as well as changing soil physical and chemical properties. These effects may be especially important when the herbivore is an introduced species. Utilizing large mammal exclosures to prevent access by introduced elk at multiple sites along a fire chronosequence, we examined the effects of elk herbivory and fire on soil microbial activity and nutrient availability. Using time since fire as a co-variate and herbivore exclosures, paired with areas outside of the exclosures, we hypothesized that reductions in plant biomass due to herbivory would reduce organic inputs to soils and impact soil microbial activities and nutrient storage. We found three major patterns: (1) when elk were excluded, surface mineral soils had higher soil organic carbon (C), total nitrogen (N), microbial N pools, and increased extra-cellular enzyme activity of a C-acquiring enzyme across a gradient of time since fire. (2) When introduced elk are present, the activity of some extracellular enzymes as well as NO3 availability are enhanced in the soil but the post-fire patterns described above with respect to nutrient accrual over time are delayed. (3) Herbivory by an introduced ungulate upsets the trajectory of ecosystem “recovery” after wildfire and delays soil C and N dynamics by an estimated 14.5–21 years, respectively. These results suggest that introduced, browsing herbivores significantly decelerate ecosystem processes but herbivory by exotics may also result in unpredictability in specific soil responses.

Keywords

Aspen Decelerated nutrient cycles Elk Fire Introduced herbivores Populus 

References

  1. Acea MJ, Carballas T (1996) Changes in physiological groups of microorganisms in soil following fire. FEMS Micro Ecol 20:33–39CrossRefGoogle Scholar
  2. Allombert S, Stockton S, Martin J-L (2005a) A natural experiment on the impact of overabundant deer on forest invertebrates. Con Biol 19:1917–1929CrossRefGoogle Scholar
  3. Allombert S, Gaston T, Martin J-L (2005b) A natural experiment on the impact of overabundant deer on songbird populations. Biol Cons 126:1–13CrossRefGoogle Scholar
  4. Anderson CB, Rosemond AD (2007) Ecosystem engineering by invasive exotic beavers reduces in-stream diversity and enhances ecosystem function in Cape Horn, Chile. Oecologia 154:141–153CrossRefPubMedGoogle Scholar
  5. Augustine DJ, Frank DA (2001) Effects of migratory grazers on spatial heterogeneity of soil nitrogen properties in a grassland ecosystem. Ecology 82:3149–3169Google Scholar
  6. Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: Herbivore selectivity and herbivore tolerance. J Wild Man 62:1165–1183CrossRefGoogle Scholar
  7. Bailey JK, Whitham TG (2002) Interactions among fire, aspen, and elk affect insect diversity: reversal of a community response. Ecology 83:1701–1712CrossRefGoogle Scholar
  8. Bailey JK, Irschick DJ, Schweitzer JA, Rehill BJ, Lindroth RL, Whitham TG (2007) Selective herbivory by elk results in rapid shifts in the chemical composition of aspen forests. Biol Invasions 9:715–722CrossRefGoogle Scholar
  9. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268CrossRefGoogle Scholar
  10. Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground interactions: how plant response to foliar herbivory influences soil organisms. Soil Biol Biochem 30:1867–1878CrossRefGoogle Scholar
  11. Binkley D, Singer F, Kaye M, Rochelle R (2003) Influence of elk grazing on soil properties in Rocky Mountain National Park. For Ecol Man 185:239–247CrossRefGoogle Scholar
  12. Choromanska U, DeLuca TH (2002) Microbial activity and nitrogen mineralization in forest mineral soils following heating: evaluation of post-fire effects. Soil Biol Biochem 34:263–271CrossRefGoogle Scholar
  13. Cộte SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM (2004) Ecological impact of deer over-abundance. Annu Rev Ecol Evol Syst 35:113–147CrossRefGoogle Scholar
  14. DeByle NV, Winokur RP (1985) Aspen: ecology and management in the Western United States. Fort Collins, Colo: U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station; WashingtonGoogle Scholar
  15. Ellison AM, Banks MS, Clinton BD et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486CrossRefGoogle Scholar
  16. Ford MA, Grace JB (1998) Effects of vertebrate herbivores on soil processes, plant biomass, litter accumulation and soil elevation changes in a coastal marsh. J Ecol 86:974–982CrossRefGoogle Scholar
  17. Frank DA, Groffman PM (1998) Ungulate vs. landscape control of soil C and N processes in grasslands of Yellowstone National Park. Ecology 79:2229–2241Google Scholar
  18. Frank DA, Groffman PM, Evans DR, Tracy BF (2000) Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grassland. Oecologia 123:116–121CrossRefGoogle Scholar
  19. Frank DA, Kuns MM, Guido DR (2002) Consumer control of grassland plant production. Ecology 83:602–606CrossRefGoogle Scholar
  20. Gee GW, Baker JM (1986) Particle-size analysis. In: Methods of soil analysis part 1, physical and mineralogical methods. Agronomy monograph No. 9 (2nd edn), American Society of Agronomy, Madison, pp 383–411Google Scholar
  21. Hamilton EW, Frank DA (2001) Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass. Ecology 82:2397–2402CrossRefGoogle Scholar
  22. Hamilton EW, Frank DA, Hinchey PM, Murray TR (2008) Defoliation induces root exudation and triggers positive rhizopheric feedbacks in a temperate grassland. Soil Biol Biochem 40:2865–2873CrossRefGoogle Scholar
  23. Harrison KA, Bardgett RD (2004) Browsing by red deer negatively impacts on soil nitrogen availability in regenerating woodland. Soil Biol Biochem 36:115–126CrossRefGoogle Scholar
  24. Harrison KA, Bardgett RD (2008) Impacts of grazing and browsing by large herbivores on soils and soil biological properties. In: Gordon IJ, Prins HHT (eds) The ecology of browsing and grazing. Ecological studies 195. Springer, Berlin, pp 201–216CrossRefGoogle Scholar
  25. Hart SC, Firestone MK (1989) Evaluation of three in situ soil nitrogen availability assays. Can J For Res 19:185–192CrossRefGoogle Scholar
  26. Hart SC, Stark JM, Davidson AE, Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Methods of soil analysis, Part 2, SSSA Book Series, no. 5Google Scholar
  27. Haubensak K, Hart SC, Stark JM (2002) Influences of chloroform exposure time and soil water content on C and N release in forest soils. Soil Biol Biochem 4:1549–1562CrossRefGoogle Scholar
  28. Hendel B, Sinsabaugh RL, Marxsen J (2005) Spectrophotometric determination of Lignin-degrading enzyme activities (Phenoloxidase and Peroxidase). In: Graca MAS, Barlocher F, Gessner M (eds) Methods to study litter decomposition. Springer, BerlinGoogle Scholar
  29. Hendershot WH, Lalande H, Duquette M (1993) Soil reaction and exchangeable acidity. In: Carter MR (ed) Soil sampling and methods of analysis. CRC Press, Boca Raton, pp 141–146Google Scholar
  30. Hierro JL, Eren Ö, Khetsuriani L, Diaconu A, Török K, Montesinos D, Andonian K, Kikodze D et al (2009) Germination responses of an invasive species in native and non-native ranges. Oikos 118:529–538Google Scholar
  31. Hoffmeister DF (1986) Mammals of Arizona. University of AZ Press, TucsonGoogle Scholar
  32. Husheer SW, Coomes DA, Robertson AW (2003) Long-term influences of introduced deer on the composition and structure of New Zealand Nothofagus forests. For Ecol Man 181:99–117CrossRefGoogle Scholar
  33. Kay CE, Bartos DL (2000) Ungulate herbivory on Utah aspen: assesment of long term exclosures. J Range Man 53:145–153CrossRefGoogle Scholar
  34. Kilpatrick S, Clause D, Scott D (2003) Aspen response to prescribed fire, mechanical treatments, and ungulate herbivory. USDA Forest Service Proceedings RMRS-P 29Google Scholar
  35. Martin JL, Stockton SA, Allombert S, Gaston AJ (in press) Top-down and bottom-up consequences of unchecked ungulate browsing on plant and animal diversity in temperate forests: lessons from a deer introduction. Biol Inv. doi:10.1007/s10530-009-9628-8
  36. Maschinski J (2001) Impacts of ungulate herbivores on a rare willow at the southern edge of its range. Biol Conserv 101:119–130CrossRefGoogle Scholar
  37. Mitton JB, Grant MC (1996) Genetic variation and the natural history of quaking aspen. Bioscience 46:25–31CrossRefGoogle Scholar
  38. Pastor J, Cohen Y (1997) Herbivores, the functional diversity of plant species and the cycling of nutrients in ecosystems. Theor Popul Biol 51:165–179CrossRefPubMedGoogle Scholar
  39. Pastor J, Danell K (2003) Moose-vegetation-soil interactions:a dynamic system. Alces 39:177–192Google Scholar
  40. Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y (1993) Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Ecology 74:467–480CrossRefGoogle Scholar
  41. Potvin F, Beaupré P, Laprise G (2003) The eradication of balsam fir stands by white-tailed deer on Anticosti Island, Québec: a 150-year process. Ecoscience 10:487–495Google Scholar
  42. Prieto-Fernández A, Acea MJ, Carballas T (1998) Soil microbial and extractable C and N after wildfire. Biol Fertil Soils 27:132–142CrossRefGoogle Scholar
  43. Rambo JL, Faeth SH (1999) Effects of grazing on plant and insect community structure. Con Biol 13:1047–1054CrossRefGoogle Scholar
  44. Relva MA, Veblen TT (1998) Impacts of introduced large herbivores on Austrocedrus chilensis forests in northern Patagonia, Argentina. For Ecol Manage 108:27–40CrossRefGoogle Scholar
  45. Relva MA, Westerholm CL, Kitzberger T (2008) Effects of introduced ungulates of forest understory communities in northern Patagonia are modified by timing and severity of stand mortality. Plant Ecol 201:11–22CrossRefGoogle Scholar
  46. Relva MA, Nuñez MA, Simberloff D (in press) Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Inv. doi:10.1007/s10530-009-9623-0
  47. Ritchie MA, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177CrossRefGoogle Scholar
  48. Rolf J (2001) Aspen fencing in N. Arizona: A 15 y perspective. Proceedings of the Rocky Mountain Research Station. USDA Forest Service. RMRS-P-18:193–196Google Scholar
  49. Romme WH, Turner MG, Wallace LL, Walker JS (1995) Aspen, elk, and fire in northern Yellowstone National Park. Ecology 76:2097–2106CrossRefGoogle Scholar
  50. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) Effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  51. Sankaran M, Augustine DJ (2004) Large herbivores suppress decomposer abundance in a semi-arid grazing system. Ecology 85:1052–1061CrossRefGoogle Scholar
  52. Schoenecker KA, Singer FJ, Zeingenfuss LC, Binkley D, Menezes RC (2004) Effects of elk herbivory on vegetation and nitrogen processes. J Wildlife Man 68:837–849CrossRefGoogle Scholar
  53. Singer FJ, Hartner MK (1996) Comparative effects of elk herbivory and 1988 fires on northern Yellowstone National Park grasslands. Ecol Appl 6:185–199CrossRefGoogle Scholar
  54. Singer FJ, Schoenecker KA (2003) Do ungulates accelerate or decelerate nitrogen cycling? For Ecol Manage 181:189–204CrossRefGoogle Scholar
  55. Smale MC, Hall GMJ, Gardner RO (1995) Dynamics of Kanuka (Kunzea ericoides) forest on South Kaipara Spit, New Zealand and the impact of fallow deer (Dama dama). NZ J Ecol 19:131–141Google Scholar
  56. Stark S, Strömmer R, Tuomi J (2002) Reindeer grazing and soil microbial processes in two suboceanic and two subcontinental tundra heaths. Oikos 97:69–78CrossRefGoogle Scholar
  57. Tabatabai MA, Dick WA (2002) Enzymes in soil: research and developments in measuring activities. In: Burns RG, Dick RP (eds) Enzymes in the environment. Marcel Dekker, New York, pp 567–596Google Scholar
  58. Treseder KK, Mack MC, Cross A (2004) Relationship among fires, fungi and soil dynamics in Alaskan boreal forests. Ecol Appl 14:1826–1838CrossRefGoogle Scholar
  59. Vázquez DP (2002) Multiple effects of introduced mammalian herbivores in a temperate forest. Biol Invasions 4:175–191CrossRefGoogle Scholar
  60. Vázquez FJ, Acea MJ, Carballas T (1993) Soil microbial populations after wildfire. FEMS Microbiol Ecol 13:93–104Google Scholar
  61. Veblen T, Mermoz M, Martın C, Ramilo E (1989) Effects of exotic deer on forest regeneration and composition in northern Patagonia. J Appl Ecol 26:711–724CrossRefGoogle Scholar
  62. Waldrop MP, Zak DR, Sinsabaugh RL (2004) Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36:1443–1451CrossRefGoogle Scholar
  63. Wallem P, Anderson CB, Martínez Pastur G, Lencinas MV (in press) Using assembly rules to measure the resilience of riparian plant communities to beaver invasion in subantarctic forests. Biol Inv. doi:10.1007/s10530-009-9625-y
  64. Wardle DA, Barker GM, Yeates GW, Bonner KI, Ghani A (2001) Introduced browsing mammals in natural New Zealand forests: aboveground and belowground consequences. Ecol Monogr 71:587–614CrossRefGoogle Scholar
  65. White LL, Zak DR, Barnes BV (2004) Biomass accumulation and soil nitrogen availability across an 87-year-old Populus grandidentata chronosequence. For Ecol Manag 191:121–127CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Michelle L. Stritar
    • 1
  • Jennifer A. Schweitzer
    • 2
  • Stephen C. Hart
    • 3
  • Joseph K. Bailey
    • 2
  1. 1.School of Forestry and Merriam-Powell Center for Environmental ResearchNorthern Arizona UniversityFlagstaffUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of Tennessee, KnoxvilleKnoxvilleUSA
  3. 3.School of Natural Sciences and Sierra Nevada Research InstituteUniversity of CaliforniaMercedUSA

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