Advertisement

Indirect Effects of Invertebrate Herbivory on the Decomposer Subsystem

  • D. A. Wardle
  • R. D. Bardgett
Part of the Ecological Studies book series (ECOLSTUD, volume 173)

Summary

Invertebrate herbivores can exert important effects on the decomposer subsystem through a range of mechanisms. In this chapter, we review the mechanistic bases through which invertebrate herbivory may affect the quantity and quality of plant-derived resources entering the soil. We identify four main types of mechanisms through which this may occur: (1) herbivores can influence resource quantity, both in the short term through promoting rhizosphere exudation and in the long term through optimizing or reducing net primary productivity (NPP); (2) herbivores may affect litter quality, either positively through causing greater tissue nutrient concentrations or negatively through inducing plants to produce secondary defence compounds; (3) herbivores sometimes return a significant proportion of NPP to the soil as fecal material, which can have very different consequences to plant litter for decomposers; (4) in the longer term herbivores can significantly alter the functional composition of vegetation which can in turn determine the quality of litter returned to the soil. There are therefore numerous ways in which invertebrate herbivores can affect decomposers either positively or negatively, and these can exert important aboveground feedbacks. Some of the most significant effects of invertebrate herbivores in ecosystems occur during periodic population outbreaks, and the likely consequences of this for the decomposer subsystem are discussed. Usually, herbivores occur in multiple species communities, which leads to the question of how herbivore diversity affects decomposer processes; while there is a dearth of information available on the topic, there are plausible mechanisms whereby such effects could theoretically occur. It is concluded that, since all ecosystems depend upon both the producer and decomposer subsystems, a more complete understanding of ecosystem-level consequences of invertebrate herbivory can only be gained through the application of approaches that explicitly consider both subsystems, as well as the feedbacks between them.

Keywords

Soil Microbial Biomass Root Herbivory Invertebrate Herbivore Population Outbreak Vertebrate Herbivore 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agrawal AA (1998) Induced responses to herbivory and increased plant performance. Science 279: 1201–1202CrossRefPubMedGoogle Scholar
  2. Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manage 62: 1165–1183CrossRefGoogle Scholar
  3. Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84: 2258–2268CrossRefGoogle Scholar
  4. Bardgett RD, Wardle DA, Yeates GW (1998) Linking above-ground and below-ground food webs: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30: 1867–1878CrossRefGoogle Scholar
  5. Bardgett RD, Denton CS, Cook R (1999) Below-ground herbivory promotes soil nutrient transfer and root growth in grassland. Ecol Lett 2: 357–360CrossRefGoogle Scholar
  6. Belovsky GE, Slade JB (2000) Insect herbivory accelerates nutrient cycling and increases plant production. Proc Nat Acad Sci USA 97: 14412–14417CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bonkowski M, Geoghegan IE, Birch ANE, Griffiths BS (2001) Effects of soil decomposer invertebrates (protozoa and earthworms) on an above-ground phytophagous insect (cereal aphid) mediated through changes in the host plant. Oikos 95: 441–450CrossRefGoogle Scholar
  8. Brown VK, Gange AC (1990) Insect herbivory below ground. Adv Ecol Res 20: 1–58Google Scholar
  9. Brown VK, Gange AC (1992) Secondary plant succession: how is it modified by insect herbivory? Vegetatio 101: 3–13CrossRefGoogle Scholar
  10. Buckland SM, Grime JP (2000) The effects of trophic structure and soil fertility on the assembly of plant communities: a microcosm experiment. Oikos 91: 336–352CrossRefGoogle Scholar
  11. Cates RG, Orians GH (1975) Successional status and the palatability of plants to generalized herbivores. Ecology 56: 410–418CrossRefGoogle Scholar
  12. Cebrian J (1999) Patterns in the fate of production in plant communities. Am Nat 154: 449–468CrossRefPubMedGoogle Scholar
  13. Cebrian J, Williams M, McLelland J, Valeila I (1998) The dependence of heterotrophic consumption and C accumulation on autotrophic nutrient content in ecosystems. Ecol Lett 1: 165–170CrossRefGoogle Scholar
  14. Davidson DW (1993) The effect of herbivory and granivory on terrestrial plant succession.Oikos 68: 23–35Google Scholar
  15. De Mazancourt C, Loreau M (2000) Effects of herbivory on primary production, and plant species replacement.Am Nat 155: 734–754Google Scholar
  16. De Ruiter PC, Neutel A, Moore JC (1995) Energetics, patterns of interaction strength, and stability in real ecosystems. Science 269: 1257–1260CrossRefPubMedGoogle Scholar
  17. Díaz S, Cadibo M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16: 646–655CrossRefGoogle Scholar
  18. Dighton J (1978) Effects of synthetic lime aphid honeydew on populations of soil organisms. Soil Biol Biochem 10: 369–376CrossRefGoogle Scholar
  19. Duffy JE, Macdonald KS, Rohde JM, Parker JD (2001) Grazer diversity, functional redundancy and productivity in seagrass beds: an experimental test. Ecology 82: 2417–2434CrossRefGoogle Scholar
  20. Dyer MI, Acra MA, Wang GM, Coleman DC, Freckman DW, McNaughton SJ, Strain BR (1991) Source-sink carbon relations in two Panicum coloratum ecotypes in response to herbivory. Ecology 72: 1472–1483CrossRefGoogle Scholar
  21. Findlay S, Carreiro M, Krishik V, Jones CJ (1996). Effects of damage to living plants on leaf litter quality. Ecol Appl 6: 269–275CrossRefGoogle Scholar
  22. Grime JP (2001) Plant strategies, vegetation processes and ecosystem properties. Wiley, ChichesterGoogle Scholar
  23. Grime JP, Cornelissen JHC, Thompson K, Hodgson JG (1996) Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos 77: 489–494CrossRefGoogle Scholar
  24. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control and competition.Am Nat 94: 421–425Google Scholar
  25. Haukioja E, Neuvonen S, Hanhimäki S, Niemelä P (1988) The autumnal moth in Fennoscandia. In: Berryman AA (ed) Dynamics of forest insect populations. Plenum Press, New York, pp 163–178CrossRefGoogle Scholar
  26. Holland EA, Parton WJ, Detling JK, Coppock DL (1992) Physiological responses of plant populations to herbivory and their consequences for ecosystem nutrient flow.Am Nat 140: 685–706Google Scholar
  27. Holland JN (1995) Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems.Appl Soil Ecol 2: 275–279Google Scholar
  28. 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– 94Google Scholar
  29. Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804–808CrossRefPubMedGoogle Scholar
  30. Lovett GM, Ruesink AE (1995) Carbon and nitrogen mineralization from decomposing gypsy moth frass. Oecologia 104: 133–138CrossRefGoogle Scholar
  31. Lovett GM, Christenson LM, Groffman PM, Jones CJ, Hart JE, Mitchell MJ (2002) Insect defoliation and nitrogen cycling in forests. BioScience 52: 335–341CrossRefGoogle Scholar
  32. Masters GJ, Brown VK, Gange AC (1993). Plant mediated interactions between above-and below-ground insect herbivores. Oikos 66: 148–151CrossRefGoogle Scholar
  33. Mawdsley JL, Bardgett RD (1997) Continuous defoliation of perennial ryegrass (Lolium perenne) and white clover (Trifolium repens) and associated changes in the microbial population of an upland soil. Biol Fertil Soils 24: 52–58CrossRefGoogle Scholar
  34. McNaughton SJ (1985) Ecology of a grazing system: the Serengeti. Ecol Monogr 55: 259–294CrossRefGoogle Scholar
  35. McNaughton SJ, Osterheld M, Frank DA, Williams KJ (1989) Ecosystem level patterns of primary productivity and herbivory in terrestrial habitats. Nature 341: 142–144CrossRefPubMedGoogle Scholar
  36. Mikola J, Yeates GW, Wardle DA, Barker GM, Bonner KI (2001b) Response of soil food web structure to defoliation of different plant species combinations in an experimental grassland community. Soil Biol Biochem 33: 205–214CrossRefGoogle Scholar
  37. Northup RA,Yu Z, Dahlgren RA, Vogt KA (1995) Polyphenol control of nitrogen release from pine litter. Nature 377: 227–229Google Scholar
  38. Oksanen L, Fretwell SD, Arruda J, Niemelä P (1981) Exploitation ecosystems in gradients of primary productivity.Am Nat 118: 240–261Google Scholar
  39. Pastor J, Naiman RJ, Dewey B, McInnes P (1988) Moose, microbes and the boreal forest. BioScience 38: 770–777CrossRefGoogle Scholar
  40. Polis GA, Hurd SD, Jackson CT, Pinero FS (1997) El Niño effects on the dynamics and control of an island ecosystem in the Gulf of California. Ecology 78: 1884–1897Google Scholar
  41. Rhoades DF (1985) Offensive–defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. Am Nat 125: 205–238CrossRefGoogle Scholar
  42. Riedell WE (1989) Western corn rootworm damage in maize: greenhouse technique and plant response. Crop Sci 29: 412–415CrossRefGoogle Scholar
  43. Root RB (1973) Organisation of a plant–arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43: 95–124CrossRefGoogle Scholar
  44. Schädler M, Jung G, Auge H, Brandl R (2003) Does the Fretwell–Oksanen model apply to invertebrates? Oikos 100: 203–207CrossRefGoogle Scholar
  45. Scheu S, Theenhaus A, Jones TH (1999) Links between the detritivore and herbivore system: effects of earthworms and Collembola on plant growth and aphid development. Oecologia 119: 541–551CrossRefGoogle Scholar
  46. Seastedt TR, Ramundo RA, Hayes DC (1988) Maximization of densities of soil animals by foliage herbivory: empirical evidence, graphical and conceptual models. Oikos 51: 243–248CrossRefGoogle Scholar
  47. Selas V, Hogstad O, Andersson G, von Proschwitz T (2001) Population cycles of autumnal moth, Epirrita autumnata, in relation to birch mast seeding. Oecologia 129: 213–219CrossRefGoogle Scholar
  48. Siemann E (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79: 2057–2070CrossRefGoogle Scholar
  49. Southwood TRE, Brown VK, Reader PM (1979) The relationships of plant and insect diversities in succession. Biol J Linn Soc 12: 327–348CrossRefGoogle Scholar
  50. Stadler B, Michalzik B (1998) Linking aphid honeydew, throughfall, and forest floor solution chemistry of Norway spruce. Ecol Lett 1: 13–16CrossRefGoogle Scholar
  51. Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above-and below-ground multitrophic interactions of plants, herbivores, pathogens and their antagonists. Trends Ecol Evol 16: 547–554CrossRefGoogle Scholar
  52. Wardle DA (2002) Communities and ecosystems: linking the aboveground and below-ground components. Princeton University Press, PrincetonGoogle Scholar
  53. Wardle DA (2004) Hidden effects: the belowground consequences of introduced browsing mammals in New Zealand forests. In: Allen RB, Lee WG (eds) Biological invasions in New Zealand. Ecological studies, vol 10. Springer, Berlin Heidelberg New York (in press)Google Scholar
  54. Wardle DA, Barker GM (1997) Competition and herbivory in establishing grassland communities: implications for plant biomass, species diversity and soil microbial activity. Oikos 80: 470–480CrossRefGoogle Scholar
  55. Wardle DA, Zackrisson O, Hörnberg G, Gallet C (1997) The influence of island area on ecosystem properties. Science 277: 1296–1299CrossRefGoogle Scholar
  56. Wardle DA, Barker GM, Bonner KI, Nicholson KS (1998) Can comparative approaches based on plant ecophysiological traits predict the nature of biotic interactions and plant species effects in ecosystems? J Ecol 86: 405–420CrossRefGoogle Scholar
  57. Wardle DA, Bonner KI, Barker GM (2000) Stability of ecosystem properties in response to above-ground functional group richness and composition. Oikos 89: 11–23CrossRefGoogle Scholar
  58. White TRC (1978) The importance of relative shortage of food in animal ecology. Oecologia 33: 71–86CrossRefGoogle Scholar
  59. Yeates GW, Saggar S, Denton CS, Mercer CF (1998) Impact of clover cyst nematode (Heterodera trifolii) infection on soil microbial activity in the rhizosphere of white clover (Trifolium repens)–a pulse labelling experiment. Nematologica 44: 81–90CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • D. A. Wardle
  • R. D. Bardgett

There are no affiliations available

Personalised recommendations