Skip to main content
Log in

Season mediates herbivore effects on litter and soil microbial abundance and activity in a semi-arid woodland

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

Abstract

Herbivores can directly impact ecosystem function by altering litter quality of an ecosystem or indirectly by shifting the composition of microbial communities that mediate nutrient processes. We examined the effects of tree susceptibility and resistance to herbivory on litter microarthropod and soil microbial communities to test the general hypothesis that herbivore driven changes in litter inputs and soil microclimate will feedback to the microbial community. Our study population consisted of individual piñon pine trees that were either susceptible or resistant to the stem-boring moth (Dioryctria albovittella) and susceptible piñon pine trees from which the moth herbivores have been manually removed since 1982. Moth herbivory increased piñon litter nitrogen concentrations (16%) and decreased canopy precipitation interception (28%), both potentially significant factors influencing litter and soil microbial communities. Our research resulted in three major findings: (1) In spite of an apparent increase in litter quality, herbivory did not change litter microarthropod abundance or species richness. (2) However, susceptibility to herbivores strongly influenced bulk soil microbial communities (i.e., 52% greater abundance beneath herbivore-resistant and herbivore-removal trees than susceptible trees) and alkaline phosphatase activity (i.e., 412% increase beneath susceptible trees relative to other groups). (3) Season had a strong influence on microbial communities (i.e., microbial biomass and alkaline phosphatase activity increased after the summer rains), and their response to herbivore inputs, in this semi-arid ecosystem. Thus, during the dry season plant resistance and susceptibility to a common insect herbivore had little or no observable effects on the belowground organisms and processes we studied, but after the rains, some pronounced effects emerged.

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

  • Bailey JK, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic-level interactions. Ecol Lett 9:78–85

    PubMed  Google Scholar 

  • Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biol 8:1–16

    Article  Google Scholar 

  • 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 30:1867–1878

    Article  CAS  Google Scholar 

  • Bergmeyer HU (1983) Enzymes. In: Bergmeyer HU (ed) Samples, reagents, assessment of results. Methods of Enzymatic Analysis, Verlag-Chemie, Weinheim Deerfield Beach Basel, pp 126–327

  • Boerner RE, Decker K, Sutherland E (2000) Prescribed burning effects on soil enzyme activity in a southern Ohio hardwood forest: a landscape-scale analysis. Soil Biol Biochem 32:899–908

    Article  CAS  Google Scholar 

  • Boyle SI, Hart SC, Kaye JP, Waldrop MP (2005) Restoration and canopy type influence soil microflora in a ponderosa pine forest. Soil Sci Soc Am J 69:1627–1638

    Article  CAS  Google Scholar 

  • Breshears DD (2006) The grassland-forest continuum: trends in ecosystem properties for woody plant mosaics? Front Ecol Environ 4:96–104

    Article  Google Scholar 

  • Brown DG (1994) Beetle folivory increases resource availability and alters plant invasion in monocultures of goldenrod. Ecology 75:1673–1683

    Article  Google Scholar 

  • Brown JH, Whitham TG, Ernest SKM, Gehring CA (2001) Complex species interactions and the dynamics of ecological systems: long-term experiments. Science 293:643–650

    Article  PubMed  CAS  Google Scholar 

  • Camann MA, Lamoncha KL, Plant NJ (2001) Acari and Collembola at Black mountain experimental forest: and interim report on community structure and prescribed fire effects. USDA Forest Service PSW Research Station Rep

  • Chapman SK, Hart SC, Cobb NS, Whitham TG, Koch GW (2003) Insect herbivory increases litter quality and decomposition: An extension of the acceleration hypothesis. Ecology 84:2867–2876

    Article  Google Scholar 

  • Classen AT, Boyle SI, Haskins KE, Overby ST, Hart SC (2003) Community-level physiological profiles of bacteria and fungi: Plate type and incubation temperature influences on contrasting soils. FEMS Microbiol Ecol 44:319–328

    Article  CAS  PubMed  Google Scholar 

  • Classen AT, Hart SC, Whitham TG, Cobb NS, Koch GW (2005) Insect infestations linked to shifts in microclimate: Important climate change implications. Soil Sci Soc Am J 69:2049–2057

    Article  CAS  Google Scholar 

  • Classen AT, DeMarco J, Hart SC, Whitham TG, Cobb NS, Koch GW (2006) Impacts of herbivorous insects on decomposer communities during the early stages of primary succession in a semi-arid woodland. Soil Biol Biochem 38:972–982

    Article  CAS  Google Scholar 

  • Cobb NS, Whitham TG (1993) Herbivore deme formation on individual trees: A test-case. Oecologia 94:496–502

    Article  Google Scholar 

  • Cobb NS, Trotter III RT, Whitham TG (2002) Long-term sexual allocation in herbivore resistant and susceptible pinyon pine (Pinus edulis). Oecologia 130:78–87

    Google Scholar 

  • Dale VH, Joyce LA, McNulty S, Neilson RP, Ayers MP, Flannigan MD, Hanson PJ, Irland LC, Lugo AE, Peterson CJ, Simberloff D, Swanson FJ, Stocks BJ, Wooton BM (2001) Climate change and forest disturbances. BioScience 51:723–734

    Article  Google Scholar 

  • Davidson EA, Eckert RW, Hart SC, Firestone MK (1989) Direct extraction of microbial biomass nitrogen from forest and grassland soils of California. Soil Biol Biochem 21:773–779

    Article  Google Scholar 

  • Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:162–172

    Article  Google Scholar 

  • Eivazi F, Bayan M (1996) Effects of long-term prescribed burning on the activity of select soil enzymes in an oak-hickory forest. Can J Forest Res 26:1799–1804

    Article  CAS  Google Scholar 

  • Ganeshamurthy AN, Nielsen NE (1990) Arylsulfatase and the biochemical mineralization of soil organic sulfur. Soil Biol Biochem 22:1163–1165

    Article  CAS  Google Scholar 

  • Garland J, Mills A (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source-utilization. Appl Environ Microbiol 57:2351–2359

    PubMed  Google Scholar 

  • Garland J 1996 Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28:213–221

    Article  CAS  Google Scholar 

  • Gehring CA, Whitham TG (1991) Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine. Nature 353:556–557

    Article  Google Scholar 

  • Gehring CA, Cobb NS, Whitham TG (1997) Three-way interactions among ectomycorrhizal mutualists, scale insects and resistant and susceptible pinyon pines. American Naturalist 149:824–841

    Article  CAS  PubMed  Google Scholar 

  • Hansen RA (1999) Red oak litter promotes a microarthropod functional group that accelerates its decomposition. Plant Soil 209:37–45

    Article  CAS  Google Scholar 

  • Hansen RA, Coleman DC (1998) Litter complexity and composition are determinants of the diversity and species composition of oribatid mites (Acari: Oribatida) in litterbags. Appl Soil Ecol 9:7–23

    Article  Google Scholar 

  • Hart SC (1988) Carbon and nitrogen accretion and dynamics in volcanic ash deposits from different subarctic habitats. Biol Fertility Soils 7:79–87

    Article  Google Scholar 

  • Haubensak KA, 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 34:1549–1562

    Article  CAS  Google Scholar 

  • Hooten JA, Ort MA, Eslon MD (2001) Origin of cinders in Wupatki National Monument, Technical Report 2001-12. Desert Archaeology, Inc, Tucson, AZ

    Google Scholar 

  • Hungate BA, Jaeger CH, Gamara G, Chapin FS, Field CB (2000) Soil microbiota in two annual grasslands: responses to elevated atmospheric CO2. Oecologia 124:589–598

    Article  Google Scholar 

  • Karl TR, Knight RW (1998) Comments on “Secular trends of precipitation amount, frequency, and intensify in the United States” - Reply. Bull Am Meteorol Soc 79:2552–2554

    Article  Google Scholar 

  • Krämer S, Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biology and Biochemistry 32:179–188

    Article  Google Scholar 

  • Kuske CR, Ticknor LO, Busch JD, Gehring CA, Whitham TG (2003) The pinyon rhizosphere, plant stress, and herbivory affect the abundance of microbial decomposers in soils. Microbial Ecol 45:340–352

    Article  CAS  Google Scholar 

  • Maraun M, Alphei J, Beste P, Bonkowski M, Buryn R, Migge S, Peter M, Schaefer M, Scheu S (2001) Indirect effects of carbon and nutrient amendments on the soil meso- and micro-fauna of a beechwood. Biol Fertility Soils 34:222–229

    CAS  Google Scholar 

  • McLean EO (1992) Soil pH and lime requirement. In: Page AL (ed) Methods of soil analysis. Chemical and microbiological properties. American Society of Agronomy and Soil Science Society of America, Madison, WI, pp 199–224

    Google Scholar 

  • Mopper S, Maschinski J, Cobb NS, Whitham TG (1991) A new look at habitat structure: consequences of herbivore-modified plant architecture. In: Bell SS, McCoy ED, Mushinsky HR (eds) Habitat structure: the physical arrangement of objects in space. Chapman and Hall Ltd., London, pp 260–280

    Google Scholar 

  • Mopper S, Mitton JB, Whitham TG, Cobb NS, Christensen KM (1991) Genetic differentiation and heterozygosity in pinyon pine associated with resistance to herbivory and environmental. Evolution 45:989–999

    Article  Google Scholar 

  • New M, Todd M, Hulme M, Jones P (2001) Precipitation measurements and trends in the twentieth century. Int J Climatol 21:1899–1922

    Article  Google Scholar 

  • O’Connell AM (1987) Litter decomposition, soil respiration and soil chemical and biochemical properties at three contrasting sites in Karri (Eucalyptus diversicolor F. Muell.) forests of south-western Australia. Aust J Ecol 12:31–40

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190

    Article  CAS  Google Scholar 

  • Osler GHR, Gauci CS, Abbott LK (2004) Limited evidence for short-term succession of microarthropods during early phases of surface litter decomposition. Pedobiologia 48:37–49

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Reynolds BC, Crossley DA, Hunter MD (2003) Response of soil invertebrates to forest canopy inputs along a productivity gradient. Pedobiologia 47:127–139

    Article  Google Scholar 

  • Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177

    Google Scholar 

  • Ruel J, Whitham TG (2002) Fast-growing juvenile pinyons suffer greater herbivory when mature. Ecology 83:2691–2699

    Article  Google Scholar 

  • Rustad LE, Campbell JL, Marion GM, Norby R, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562

    Article  Google Scholar 

  • Santos PF, Depree E, Whitford WG (1978) Spatial distributions of litter and microarthropods in a Chihuahuan desert ecosystem. J Arid Environ 1:41–48

    Google Scholar 

  • Schowalter TD, Sabin TE (1991) Litter microarthropod responses to canopy herbivory, season and decomposition in litterbags in a regenerating conifer ecosystem in Western Oregon. Biol Fertility Soils 11:93–96

    Article  Google Scholar 

  • Seastedt TR, Crossley Jr. DA, Hargrove WW (1983) The effects of low-level consumption by canopy arthropods on the growth and nutrient dynamics of black locust and red maple trees in the southern Appalachians. Ecology 64:1040–1048

    Article  Google Scholar 

  • Shaw JD, Steed BE, DeBlander LT (2005) Forest Inventory and Analysis (FIA) annual inventory answers the question: What is happening to pinyon-juniper woodlands? J For 103:280–285

    Google Scholar 

  • Shuster SM, Lonsdorf EV, Wimp GM, Bailey JK, Whitham TG (2006) Community heritability measures the evolutionary consequences of indirect genetic effects on community structure. Evolution 60:991–1003

    PubMed  CAS  Google Scholar 

  • Sinsabaugh A (1994) Enzymatic analysis of microbial pattern and process. Biol Fertility Soils 17:69–74

    Article  CAS  Google Scholar 

  • Swaty RL, Gehring CA, Van Ert M, Theimer TC, Keim P, Whitham TG (1998) Temporal variation in temperature and rainfall differentially affects ectomycorrhizal colonization at two contrasting sites. New Phytol 139:733–739

    Article  Google Scholar 

  • Tabatabai MA, Bremmer JM (1970) Arylsulfatase activity of soils. Soil Sci Soc Am J 34:225–229

    CAS  Google Scholar 

  • Tarafdar J, Kiran B, Rao A (1989) Phosphatase activity and distribution of phosphorous in arid soil profiles under different land use patterns. J Arid Environ 16:29–34

    Google Scholar 

  • Taylor AR, Wolters V (2005) Responses of oribatid mite communities to summer drought: The influence of litter type and quality. Soil Biol Biochem 37:2117–2130

    Article  CAS  Google Scholar 

  • White TCR (1969) An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50:905–909

    Article  Google Scholar 

  • White TCR (1993) The inadequate environment. Springer, Berlin Heidelberg, New York

    Google Scholar 

  • Whitford WG (1996) The importance of the biodiversity of soil biota in arid ecosystems. Biodiv Conserv 5:185–195

    Article  Google Scholar 

  • Whitford WG (1996) The importance of the biodiversity of soil biota in arid environments. Biodiv Conserv 5:185–195

    Article  Google Scholar 

  • Whitham TG, Mopper S (1985) Chronic herbivory: Impacts on architecture and sex expression of pinyon pine. Science 228:1089–1091

    Article  PubMed  Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, Leroy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Dickerson and J. DeMarco, who helped with sample collection and analysis. S. Boyle and D. Guido assisted with enzyme analysis. S. Chapman assisted with field and laboratory work. G. Crutsinger gave insightful comments on the manuscript. G. Newman and P. Selmants gave useful soil information. NSF grants (DEB9816001, DEB0236204), a NAU undergraduate Hooper fellowship awarded to J. Demarco and M. Dickerson, fellowships awarded to A.T. Classen from the Merriam-Powell Center for Environmental Research and the American Association of University Women, and the U.S. Department of Energy, Office of Science, Biological and Environmental Research Program funded this work. ORNL is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aimée T. Classen.

Additional information

Responsible Editor: Angela Hodge.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Classen, A.T., Overby, S.T., Hart, S.C. et al. Season mediates herbivore effects on litter and soil microbial abundance and activity in a semi-arid woodland. Plant Soil 295, 217–227 (2007). https://doi.org/10.1007/s11104-007-9277-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-007-9277-6

Keywords

Navigation