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Biological Invasions

, Volume 12, Issue 8, pp 2619–2638 | Cite as

Determining the impact of scale insect honeydew, and invasive wasps and rodents, on the decomposer subsystem in a New Zealand beech forest

  • David A. Wardle
  • Brian J. Karl
  • Jacqueline R. Beggs
  • Gregor W. Yeates
  • Wendy M. Williamson
  • Karen I. Bonner
Original Paper

Abstract

Relatively few studies have considered how aboveground invasive consumers influence decomposer communities. We investigated the potential effects of three types of animals on the decomposer subsystem in a floristically simple New Zealand Nothofagus forest. These animals are the native beech honeydew scale insect (Ultracoelostoma spp.) that secretes large amounts of sugar-rich honeydew that washes to the soil, invasive social wasps (Vespula spp.) that remove honeydew and prevent it from reaching the ground, and invasive rodents (the house mouse (Mus musculus) and ship rat (Rattus rattus)) that are predators of litter invertebrates. We performed a 4 years manipulative experiment involving addition of synthetic honeydew to the soil surface at amounts equal to that washed to the soil both in the absence and presence of wasps. All treatments were subjected to both exclusion and non-exclusion of rodents. Full honeydew addition influenced several components of the belowground community (both positively and negatively), and promoted fungi and fungal feeding fauna at the expense of bacteria and bacterial-feeders. The reduced addition of honeydew (representing effects of wasps) reversed some (but not all) effects of full honeydew addition. Rodents also influenced some belowground organisms, often reversing the effects of honeydew addition. The honeydew levels simulating wasp effects and the presence of rodents both greatly promoted humus carbon and nutrient storage relative to all other treatments, highlighting that invaders can alter soil carbon sequestration and nutrient capital. Our study points to invasive animals modifying the effects of a native animal on multiple components of the decomposer subsystem.

Keywords

Beech forest Decomposition Honeydew House mouse Nothofagus Ship rat Social wasps Soil food web 

Notes

Acknowledgments

We thank Gaye Rattray for technical assistance, Richard Bardgett, Tad Fukami and Anna Lagerström for help with field sampling, Richard Toft and John Dugdale for assistance with invertebrate identifications, the New Zealand Department of Conservation (notably Ann Brow and Grant Harper) for discussion and access to data on rodent densities and beech mast seeding in the study area, and two anonymous reviewers for constructive comments. This work was supported by the New Zealand Foundation of Research, Science and Technology.

Supplementary material

10530_2009_9670_MOESM1_ESM.doc (228 kb)
(DOC 228 kb)

References

  1. Abrams PA (2009) When does greater mortality increase population size? The long history and diverse mechanisms underlying the hydra effect. Ecol Lett 12:462–474CrossRefPubMedGoogle Scholar
  2. Allen RB, Lee WG (eds) (2006) Biological invasions in New Zealand. Ecological Studies 186. Springer, HeidelbergGoogle Scholar
  3. Alley JC, Berben PH, Dugdale JS, Fitzgerald BM, Knightbridge PI, Meads MJ, Webster RA (2001) Responses of litter dwelling arthropods and house mice to beech seeding in the Orongorongo Velley of New Zealand. J Roy Soc NZ 31:425–452Google Scholar
  4. Anderson JPE, Domsch KH (1978) A physiologically active method for the quantification of microbial biomass in soil. Soil Biol Biochem 10:215–221CrossRefGoogle Scholar
  5. Angel A, Wanless RM, Cooper J (2009) Review of impacts of the introduced house mouse on islands in the Southern Ocean: are mice equivalent to rats? Biol Inv 11:1743–1754CrossRefGoogle Scholar
  6. Bardgett RD (2005) The biology of soils—a community and ecosystem approach. Oxford University Press, OxfordGoogle Scholar
  7. Bardgett RD, Wardle DA (2003) Herbivore mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268CrossRefGoogle Scholar
  8. Bardgett RD, Hobbs PJ, Frostegård Å (1996) Changes in the structure of microbial communities following reductions in the intensity and management of an upland grassland. Biol Fertil Soils 22:261–264CrossRefGoogle Scholar
  9. Beggs JR (2001) The ecological consequences of social wasps (Vespula spp) invading an ecosystem that has an abundant carbohydrate source. Biol Conserv 99:17–28CrossRefGoogle Scholar
  10. Beggs JR, Wardle DA (2006) Competition for honeydew among exotic and indigenous species. In: Allen RB, Lee WG (eds) Biological Invasions in New Zealand. Ecological Studies 186. Springer, Heidelberg, pp 281–294CrossRefGoogle Scholar
  11. Beggs JR, Karl BJ, Wardle DA, Bonner KI (2005) Soluble carbon production by honeydew scale insects in a New Zealand beech forest. NZ J Ecol 29:105–115Google Scholar
  12. Bligh EG, Dyer WG (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedGoogle Scholar
  13. Boag B (2000) The impact of the New Zealand flatworm on earthworms and moles in agricultural land in western Scotland. Aspects Appl Biol 62:79–84Google Scholar
  14. Boag B, Yeates GW (2001) The potential impact of the New Zealand flatworm, a predator of earthworms, in western Europe. Ecol Applic 11:1276–1286CrossRefGoogle Scholar
  15. Brow AK, Bruce TA, Chisnall DT, Gasson PA, Leggett SA, Paton BR, Hawes M (2008) Rotoiti nature recovery project annual report 2006–2007—Nelson Lakes Mainland Island, Nelson Lakes National Park. Department of Conservation, NelsonGoogle Scholar
  16. Chown SL, McGeoch MA, Marshall DJ (2002) Diversity and conservation of invertebrates on the Subarctic Prince Edward Islands. Afr Entomol 10:67–82Google Scholar
  17. Coleman DC, Reid CPP, Cole CV (1983) Biological strategies of nutrient cycling in soil systems. Adv Ecol Res 13:1–51CrossRefGoogle Scholar
  18. Crafford JE (1990) The role of feral house mice in ecosystem functioning on Marion Island. In: Kerry KR, Hempel G (eds) Antarctic ecosystems: ecological change and conservation. Springer, Berlin, pp 359–364Google Scholar
  19. Croll DA, Maron JL, Estes JA, Danner EM, Byrd GV (2005) Introduced predators transform subarctic islands from grassland to tundra. Science 307:1959–1961CrossRefPubMedGoogle Scholar
  20. Degens BP (1998) Microbial functional diversity can be influenced by the addition of simple organic substrates to soil. Soil Biol Biochem 30:1981–1988CrossRefGoogle Scholar
  21. Degens BP, Harris JA (1997) Development of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1302–1320CrossRefGoogle Scholar
  22. Dighton J (1978) In vitro experiments simulating the possible fate of honeydew sugars in soil. Soil Biol Biochem 10:53–57CrossRefGoogle Scholar
  23. Dugdale JS (1996) Natural history and identification of litter-feeding Lepidoptera larvae (Insecta) in beech forests, Orongorongo Valley, New Zealand with especial reference to the diet of mice (Mus musculus). J Royal Soc NZ 26:252–275Google Scholar
  24. Dungan RJ, Beggs JR, Wardle DA (2004) A simple gravimetric technique for estimating honeydew or nectar production. NZ J Ecol 28:283–288Google Scholar
  25. Dungan RJ, Turnbull MH, Kelly D (2007) The carbon costs for host trees of a phloem-feeding herbivore. J Ecol 95:603–613CrossRefGoogle Scholar
  26. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  27. Ettema CH, Lowrance R, Coleman DC (1999) Riparian soil response to surface nitrogen input: the indicator potential of free living soil nematode populations. Soil Biol Biochem 31:1625–1638CrossRefGoogle Scholar
  28. Fitzgerald BM, Gibb JA (2001) Introduced mammals in a New Zealand forest: long-term research in the Orongorongo Valley. Biol Conserv 99:97–108CrossRefGoogle Scholar
  29. Fitzgerald BM, Efford MG, Karl BJ (2004) Breeding of house mice and the mast seeding of southern beeches in the Orongorongo Valley, New Zealand. NZ J Zool 31:167–184Google Scholar
  30. Fukami T, Wardle DA, Bellingham PJ, Mulder CPH, Towns DR, Yeates GW, Bonner KI, Durrett MS, Grant-Hoffman MN, Williamson WM (2006) Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett 9:1299–1307CrossRefPubMedGoogle Scholar
  31. Grant WD, Beggs JR (1989) Carbohydrate analysis of beech honeydew. NZ J Ecol 16:283–288Google Scholar
  32. Jackson ML (1958) Soil chemical analysis. Constable, LondonGoogle Scholar
  33. Jackson RB, Banner JL, Jobbagy EG, Pockman WT, Wall DH (2002) Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418:623–626CrossRefPubMedGoogle Scholar
  34. Lavelle P (1997) Faunal activities and soil processes: adaptive strategies that determine ecosystem function. Adv Ecol Res 27:93–132CrossRefGoogle Scholar
  35. Lee WG, Allen RB, Tompkins DM (2006) Paradise lost–the last major colonization. In: Allen RB, Lee WG (eds) Biological Invasions in New Zealand. Ecological Studies 186. Springer, Heidelberg, pp 1–13CrossRefGoogle Scholar
  36. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405CrossRefGoogle Scholar
  37. Maron JL, Estes JA, Croll DA, Danner EM, Elmendorf SC, Buckalew S (2006) An introduced predator alters Aleutian Island plant communities by thwarting nutrient subsidies. Ecol Monogr 76:3–24CrossRefGoogle Scholar
  38. Matsuoka T, Seno H (2008) Ecological balance in the native population dynamics may cause the paradox of pest control with harvesting. J Theor Biol 252:87–97CrossRefPubMedGoogle Scholar
  39. Moller H, Tilley JAV, Thomas BW, Gaze PD (1991) Effect of introduced social wasps on the standing crop of honeydew in New Zealand beech forests. NZ J Zool 18:171–179Google Scholar
  40. Moore JC, Hunt HW (1988) Resource compartmentation and the stability of real ecosystems. Nature 333:261–263CrossRefGoogle Scholar
  41. Mulder CPH, Grant-Hoffman MN, Towns DR, Bellingham PJ, Wardle DA, Durrett MS, Fukami T, Bonner KI (2009) Direct and indirect effects of rats: will their eradication restore ecosystem functioning of New Zealand seabird islands? Biol Invas 11:1671–1688CrossRefGoogle Scholar
  42. O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817CrossRefGoogle Scholar
  43. Paine PT (1966) Food web complexity and species diversity. Am Nat 100:65–75CrossRefGoogle Scholar
  44. Parekh NR, Bardgett RD (2002) The characterisation of microbial communities in environmental samples. In: Keith-Roach MJ, Livens FR (eds), Interactions of microorganisms with radionucleides, vol 2. Radioactivity in the environment. Elsevier, Amsterdam, pp 37–60Google Scholar
  45. Peltzer DA, Bellingham PJ, Kurokawa H, Walker LR, Wardle DA, Yeates GW (2009) Punching above their weight: low-biomass non-native plant species alter soil ecosystem properties during primary succession. Oikos 11:1001–1014CrossRefGoogle Scholar
  46. Peltzer DA, Allen RB, Lovett GM, Whitehead D, Wardle DA (2009) Effects of biological invasions on forest carbon sequestration. Glob Change Biol. doi:  10.1111/j.1365-2486.2009.02038.x
  47. Rutherford PM, Juma NG (1992) Effect of glucose amendment on microbial biomass, fertilizer 15N-recovery and distribution in a barley-soil system. Biol Fertil Soils 12:228–232CrossRefGoogle Scholar
  48. Schoener TW, Spiller DA (1996) Devastation of prey by experimental introduction of predators in the field. Nature 381:691–694CrossRefGoogle Scholar
  49. Seeger J, Filser J (2008) Bottom-up down from the top: honeydew as a carbon source for soil organisms. Eur J Soil Biol 44:483–490CrossRefGoogle Scholar
  50. Simberloff D (1990) Community effects of biological introductions and their implications for restoration. In: Towns DR, Daugherty CH, Atkinson IAE (eds) Ecological restoration of New Zealand islands. Department of Conservation, Wellington, pp 128–136Google Scholar
  51. Stadler B, Michalzik B (1998) Linking aphid honeydew, throughfall and forest floor solution chemistry of Norway spruce. Ecol Lett 1:13–16CrossRefGoogle Scholar
  52. Stadler B, Michalzik B, Müller T (1998) Linking aphid ecology with nutrient fluxes in a coniferous forest. Ecology 79:1514–1525CrossRefGoogle Scholar
  53. Towns DR, Wardle DA, Mulder CPH, Yeates GW, Fitzgerald BM, Parrish GR, Bellingham PJ, Bonner KI (2009) Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118:420–430CrossRefGoogle Scholar
  54. Tunlid A, Hoitink HA, Low C (1989) Characterisation of bacteria that suppress Rhizoctonia damping-off in bark compost media by analysis of fatty acid biomarkers. Appl Environ Microbiol 55:1368–1374PubMedGoogle Scholar
  55. Van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37CrossRefPubMedGoogle Scholar
  56. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  57. Wardhaugh CW, Didham RK (2005) Preliminary evidence suggests that beech scale insect honeydew has a negative effect on terrestrial litter decomposition rates in Nothofagus forests of New Zealand. N Z J Ecol 30:279–284Google Scholar
  58. Wardle DA (1992) A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soils. Biol Rev 67:321–358CrossRefGoogle Scholar
  59. Wardle DA (1993) Changes in the microbial biomass and metabolic quotient during leaf litter succession in some New Zealand forest and scrubland ecosystems. Funct Ecol 7:346–355CrossRefGoogle Scholar
  60. Wardle DA (2002) Communities and ecosystems - linking the aboveground and belowground components. Princeton University Press, PrincetonGoogle Scholar
  61. Wardle DA, Bardgett RD (2004) Human-induced changes in densities of large herbivorous mammals: consequences for the decomposer subsystem. Frontiers Ecol Environ 2:145–153CrossRefGoogle Scholar
  62. 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
  63. Wardle DA, Yeates GW, Barker GM, Bellingham PJ, Bonner KI, Williamson W (2003) Island biology and ecosystem functioning in epiphytic soil communities. Science 301:1717–1720CrossRefPubMedGoogle Scholar
  64. Wardle DA, Bellingham PJ, Mulder CPH, Fukami T (2007) Promotion of ecosystem carbon sequestration by invasive predators. Biology Letters 3:479–482CrossRefPubMedGoogle Scholar
  65. Wardle DA, Bellingham PJ, Bonner KI, Mulder CPH (2009) Indirect effects of invasive predators on plant litter quality, decomposition and nutrient resorption on seabird-dominated islands. Ecology 90:452–464CrossRefPubMedGoogle Scholar
  66. White DC, Davis WM, Nikels JS (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62CrossRefGoogle Scholar
  67. Wilmshurst JM, Anderson AJ, Higham TFG, Worthy TH (2008) Dating the late prehistoric dispersal of polynesians to New Zealand using the commensal Pacific rat. Proc Nat Acad Sciences USA 105:7676–7680CrossRefGoogle Scholar
  68. Yarie J, Van Cleve K (1996) Effects of carbon, fertilizer and drought on foliar chemistry of tree species in interior Alaska. Ecol Applic 6:815–827CrossRefGoogle Scholar
  69. Yeates GW (1978) Populations of nematode genera in soils under pasture. I. Seasonal dynamics in dryland and irrigated pasture on a southern yellow-grey earth. NZ J Agric Res 21:321–330Google Scholar
  70. Yeates GW, Bongers T, de Goede RGM (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • David A. Wardle
    • 1
    • 2
  • Brian J. Karl
    • 3
  • Jacqueline R. Beggs
    • 4
  • Gregor W. Yeates
    • 5
    • 7
  • Wendy M. Williamson
    • 6
  • Karen I. Bonner
    • 2
  1. 1.Department of Forest Ecology and ManagementSwedish University of Agricultural SciencesUmeåSweden
  2. 2.Landcare ResearchLincolnNew Zealand
  3. 3.Landcare ResearchNelsonNew Zealand
  4. 4.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  5. 5.Landcare ResearchPalmerston NorthNew Zealand
  6. 6.ESR, Christchurch Science CentreChristchurchNew Zealand
  7. 7.Palmerston NorthNew Zealand

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