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Statistical models to evaluate invertebrate–plant trophic interactions in arable systems

Published online by Cambridge University Press:  24 May 2007

D.A. Bohan ,
C. Hawes ,
A.J. Haughton ,
I. Denholm ,
G.T. Champion ,
J.N. Perry  and
S.J. Clark
D.A. Bohan*
Affiliation:
Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK
C. Hawes
Affiliation:
Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK
A.J. Haughton
Affiliation:
Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK
I. Denholm
Affiliation:
Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK
G.T. Champion
Affiliation:
Broom's Barn Research Station, Bury St Edmunds, Suffolk, 1P28 6NP, UK
J.N. Perry
Affiliation:
Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK
S.J. Clark
Affiliation:
Rothamsted Research, Harpenden, Herts, AL5 2JQ, UK
*
*Fax: +44 (0)1582 760981 E-mail: [email protected]
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Abstract

Over the past 40 years there have been marked shifts in arable farmland management that are widely believed to have had a considerable impact on flowering plants and invertebrates and the small mammals and birds that rely upon them. It is not yet possible to predict the dynamics of plants and invertebrates either with past or future changes in farmland management. This study investigates whether a basic invertebrate classification, formed of broad trophic groups, can be used to describe interactions between invertebrates and their resource plants and evaluate management impacts for genetically modified, herbicide-tolerant (GMHT) and conventional herbicide management in both spring- and winter-sown oilseed rape. It is argued that the analyses validate trophic-based approaches for describing the dynamics of invertebrates in farmland and that linear models might be used to describe the changes in invertebrate trophic group abundance in farmland when driven by primary producer abundance or biomass and interactions between invertebrates themselves. The analyses indicate that invertebrate dynamics under GMHT management are not unique, but similar to conventional management occurring over different resource ranges, and that dynamics differed considerably between spring- and winter-sown oilseed rape. Thus, herbicide management was of much lower impact on trophic relationships than sowing date. Results indicate that invertebrate dynamics in oilseed rape are regulated by a combination of top-down and bottom-up trophic processes.

Type
Research Article
Information
Bulletin of Entomological Research , Volume 97 , Issue 3 , June 2007 , pp. 265 - 280
Copyright
Copyright © Cambridge University Press 2007

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References

Abrams, P.A. (1993) Effect of increased productivity on the abundance of trophic levels. American Naturalist 141, 351–371.CrossRefGoogle Scholar
Aebischer, N.J. (1991) Twenty years of monitoring invertebrates and weeds in cereal fields in Sussex. pp. 305–331in Firbank, L.G.Carter, N.Derbyshire, J.F. & Potts, G.R. (Eds) The ecology of temperate cereal fields. Oxford, Blackwell.Google Scholar
Bohan, D.A., Boffey, C.W.H., Brooks, D.R., Clark, S.J., Dewar, A.M., Firbank, L.G., Haughton, A.J., Hawes, C., Heard, M.S., May, M.J., Osborne, J.L., Perry, J.N., Rothery, P., Roy, D.B., Scott, R.J., Squire, G.R., Woiwod, I.P. & Champion, G.T. (2005) Effects on weed and invertebrate abundance and diversity of herbicide management in genetically modified herbicide-tolerant winter-sown oilseed rape. Proceedings of the Royal Society of London, B 272, 463–474.Google Scholar
Brooks, D.R., Bohan, D.A., Champion, G.T., Haughton, A.J., Hawes, C., Heard, M.S., Clark, S.J., Dewar, A.M., Firbank, L.G., Perry, J.N., Rothery, P., Scott, R.J., Woiwod, I.P., Birchall, C., Skellern, M.P., Walker, J.H., Baker, P., Bell, D., Browne, E.L., Dewar, A.J.G., Fairfax, C.M., Garner, B.H., Haylock, L.A., Horne, S.L., Hulmes, S.E., Mason, N.S., Norton, L.R., Nuttall, P., Randle, Z., Rossall, M.J., Sands, R.J.N., Singer, E.J. & Walker, M.J. (2003) Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. I. Soil-surface-active invertebrates. Philosophical Transactions of the Royal Society of London, B 358, 1847–1862.Google Scholar
Candolfi, M., Bigler, F., Campbell, P., Heimbach, U., Schmuck, R., Angeli, G., Bakker, F., Brown, K., Carli, G., Dinter, A., Forti, D., Forster, R., Gathmann, A., Hassan, S., Mead-Briggs, M., Melandri, M., Neumann, P., Pasqualini, E., Powell, W., Reboulet, J.N., Romijn, K., Sechser, B., Thieme, T., Ufer, A., Vergnet, C. & Vogt, H. (2000) Principles for regulatory testing and interpretation of semifield and field studies with non-target arthropods. Journal of Pesticide Science 73, 141–147.CrossRefGoogle Scholar
Carpenter, S.R. & Kitchell, J.F. (1988) Consumer control of lake productivity. BioScience 38, 764–769.CrossRefGoogle Scholar
Carpenter, S.R., Kitchell, J.F. & Hodgson, J.R. (1985) Cascading trophic interactions and lake productivity. BioScience 35, 634–639.CrossRefGoogle Scholar
Carpenter, S.R., Kitchell, J.F., Hodgson, J.R., Cochran, P.A., Elser, J.J., Elser, M.M., Lodge, D.M., Kretchmer, D., He, X. & von Ende, C.N. (1987) Regulation of lake primary productivity by food web structure. Ecology 68, 1863–1876.CrossRefGoogle ScholarPubMed
Chamberlain, D.E., Fuller, R.J., Bunce, R.G.H., Duckworth, J.C. & Shrubb, M. (2000) Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. Journal of Applied Ecology 37, 771–788.CrossRefGoogle Scholar
Champion, G.T., May, M.J., Bennett, S., Brooks, D.R., Clark, S.J., Daniels, R.E., Firbank, L.G., Haughton, A.J., Hawes, C., Heard, M.S., Perry, J.N., Randle, Z., Rossall, M.J., Rothery, P., Skellern, M.P., Scott, R.J., Squire, G.R. & Thomas, M.R. (2003) Crop management and agronomic context of the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of the Royal Society of London, B 358, 1801–1818.Google ScholarPubMed
Cromartie, W.J. (1975) The effect of stand size and vegetational background on the colonization of cruciferous plants by herbivorous insects. Journal of Applied Ecology 12, 517–533.Google Scholar
De Feo, O. & Rinaldi, S. (1997) Yield and dynamics of tritrophic food chains. American Naturalist 150, 328–345.CrossRefGoogle ScholarPubMed
Donald, P.F. (1998) Changes in the abundance of invertebrates and plants on British farmland. British Wildlife 9, 279–289.Google Scholar
Donald, P.F. & Vickery, J.A. (2001) The ecology and conservation of skylarks Alauda arvensis. Sandy, Beds, Royal Society for the Protection of Birds.Google Scholar
Firbank, L.G., Heard, M.S., Woiwod, I.P., Hawes, C., Haughton, A.J., Champion, G.T., Scott, R.J., Hill, M.O., Dewar, A.M., Squire, G.R., May, M.J., Brooks, D.R., Bohan, D.A., Daniels, R.E., Osborne, J.L., Roy, D.B., Black, H.I.J., Rothery, P. & Perry, J.N. (2003a) An introduction to the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Journal of Applied Ecology 40, 2–16.CrossRefGoogle Scholar
Firbank, L.G., Perry, J.N., Squire, G.R., Bohan, D.A., Brooks, D.R., Champion, G.T., Clark, S.J., Daniels, R.E., Dewar, A.M., Haughton, A.J., Hawes, C., Heard, M.S., Hill, M.O., May, M.J., Osborne, J.L., Rothery, P., Roy, D.B., Scott, R.J. & Woiwod, I.P. (2003b) The implications of spring-sown genetically modified herbicide-tolerant crops for farmland biodiversity: a commentary on the Farm Scale Evaluations of spring sown crops http://www.defra.gov.uk/environment/gm/fse/results/fse-commentary.pdfGoogle Scholar
Fretwell, S.D. (1977) The regulation of plant communities by the food chains exploiting them. Perspectives in Biology and Medicine 20, 169–185.CrossRefGoogle Scholar
Fretwell, S.D. (1987) Food chain dynamics: the central theory of ecology? Oikos 50, 291–301.CrossRefGoogle Scholar
Fuller, R.J., Gregory, R.D., Gibbons, D.W., Marchant, J.H., Wilson, J.D., Baillie, S.R. & Carter, N. (1995) Population declines and range contractions among lowland farmland birds in Britain. Conservation Biology 9, 1425–1441.CrossRefGoogle Scholar
Gibbons, D.W., Avery, M.I. & Brown, A.F. (1996) Population trends of breeding birds in the United Kingdom since 1800. British Birds 89, 291–305.Google Scholar
GM Science Review (2003) http://www.gmsciencedebate.org.uk/Google Scholar
Godfray, H.C.J. (1994) Parasitoids: behavioural and evolutionary ecology. Princeton, New Jessey, Princeton University Press.CrossRefGoogle Scholar
Gomez, J.M. & Zamora, R. (1994) Top-down effects in a tritrophic system: parasitoids enhance plant fitness. Ecology 75, 1023–1030.CrossRefGoogle Scholar
Haddad, N.M., Tilman, D., Haarstad, J., Ritchie, M. & Knops, J.M.H. (2001) Contrasting effects of plant richness and composition on insect communities: a field experiment. American Naturalist 158, 17–35.CrossRefGoogle ScholarPubMed
Hairston, N.G. Jr. & Hairston, N.G. Sr. (1993) Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. American Naturalist 142, 379–411.CrossRefGoogle Scholar
Hairston, N.G., Smith, F.E. & Slobodkin, L.B. (1960) Community structure, population control, and competition. American Naturalist 94, 421–425.CrossRefGoogle Scholar
Hald, A.B. (1999) Weed vegetation (wild flora) of long established organic versus conventional cereal fields in Denmark. Annals of Applied Biology 134, 307–314.CrossRefGoogle Scholar
Hassell, M.P., Southwood, T.R.E. & Reader, P.M. (1987) The dynamics of the viburnum whitefly (Aleurotrachelus jelinekii): a case study of population regulation. Journal of Animal Ecology 56, 283–300.CrossRefGoogle Scholar
Haughton, A.J., Champion, G.T., Hawes, C., Heard, M.S., Brooks, D.R., Bohan, D.A., Clark, S.J., Dewar, A.M., Firbank, L.G., Osborne, J.L., Perry, J.N., Rothery, P., Roy, D.B., Scott, R.J., Woiwod, I.P., Birchall, C., Skellern, M.P., Walker, J.H., Baker, P., Browne, E.L., Dewar, A.J.G., Garner, B.H., Haylock, L.A., Horne, S.L., Mason, N.S., Sands, R.J.N. & Walker, M.J. (2003) Invertebrate responses to the management of genetically modified herbicide-tolerant and conventional spring crops. II. Within-field epigeal and aerial arthropods. Philosophical Transactions of the Royal Society of London, B 358, 1863–1877.Google Scholar
Hawes, C., Haughton, A.J., Osborne, J.L., Roy, D.B., Clark, S.J., Perry, J.N., Rothery, P., Bohan, D.A., Brooks, D.R., Champion, G.T., Dewar, A.M., Heard, M.S., Woiwod, I.P., Daniels, R.E., Young, M.W., Parish, A.M., Scott, R.J., Firbank, L.G. & Squire, G.R. (2003) Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of The Royal Society of London, B 358, 1899–1913.Google ScholarPubMed
Heard, M.S., Hawes, C., Champion, G.T., Clark, S.J., Firbank, L.G., Haughton, A.J., Parish, A.M., Perry, J.N., Rothery, P., Scott, R.J., Skellern, M.P., Squire, G.R. & Hill, M.O. (2003) Weeds in fields with contrasting conventional and genetically modified herbicide-tolerant crops. I. Effects on abundance and diversity. Philosophical Transactions of the Royal Society of London, B 358, 1819–1833.Google ScholarPubMed
Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724–732.CrossRefGoogle Scholar
Jones, C.G. & Lawton, J.H. (1995) Linking species and ecosystems. London, Chapman and Hall.CrossRefGoogle Scholar
Koricheva, J., Mulder, C.P.H., Schmid, B., Joshi, J. & Huss-Danell, K. (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125, 271–282.CrossRefGoogle ScholarPubMed
Krebs, J.R., Wilson, J.D., Bradbury, R.B. & Siriwardena, G.M. (1999) The second silent spring? Nature 400, 611–612.CrossRefGoogle Scholar
Lavorel, S. & Garnier, E. (2002) Predicting changes in community composition and ecosystem functioning from plant traits; revisiting the Holy Grail. Functional Ecology 16, 545–556.CrossRefGoogle Scholar
Lavorel, S., McIntyre, S., Landsberg, J. & Forbes, T.D.A. (1997) Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends in Ecology and Evolution 12, 474–478.CrossRefGoogle ScholarPubMed
Leibold, M.A. (1989) Resource edibility and the effects of predators and productivity on the outcome of trophic interactions. American Naturalist 134, 922–949.CrossRefGoogle Scholar
Lewis, P.A., Klemm, D.J. & Lazorchack, J.M. (1992) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms. EPA/600/4-91/022. Environmental Monitoring Systems Laboratory Cincinnati, Ohio.Google Scholar
Lindeman, R.L. (1942) The trophic-dynamic aspect of ecology. Ecology 23, 399–418.CrossRefGoogle Scholar
Marquis, R.J. & Whelan, C.J. (1994) Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology 75, 2007–2014.CrossRefGoogle Scholar
Marshall, E.J.P. & Moonen, A.C. (2002) Field margins in northern Europe: their functions and interactions with agriculture. Agriculture, Ecosystems and Environment 89, 5–21.CrossRefGoogle Scholar
McNaughton, S.J. (1985) Ecology of a grazing ecosystem: the Serengeti. Ecological Mongraphs 55, 259–294.CrossRefGoogle Scholar
McNaughton, S.J., Oesterheld, M., Frank, D.A. & Williams, K.J. (1989) Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats. Nature 341, 142–144.CrossRefGoogle ScholarPubMed
McQueen, D.J., Post, J.R. & Mills, E.L. (1986) Trophic relationships in freshwater pelagic ecosystems. Canadian Journal of Fisheries and Aquatic Science 43, 1571–1581.CrossRefGoogle Scholar
McQueen, D.J., Johannes, M.R.S., Post, J.R., Stewart, T.J. & Lean, D.R.S. (1989) Bottom-up and top-down impacts on freshwater pelagic community structure. Ecological Mongraphs 59, 289–309.CrossRefGoogle Scholar
Mikola, J. & Setälä, H. (1998) No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79, 153–164.CrossRefGoogle Scholar
Moriarty, F. (1999) Ecotoxicology: the study of pollutants in ecosystems. 3rd edn. Academic Press.Google Scholar
Oksanen, L. (1983) Trophic exploitation and arctic phytomass patterns. American Naturalist 122, 45–52.CrossRefGoogle Scholar
Oksanen, L., Fretwell, S.D., Arruda, J. & Niemela, P. (1981) Exploitation ecosystems in gradients of primary productivity. American Naturalist 118, 240–261.CrossRefGoogle Scholar
Osenberg, C.W. & Mittelbach, G.G. (1996) The relative importance of resource limitation and predator limitation in food chains. pp. 134–148in Polis, G.A. & Winemiller, K.O. (Eds) Food webs: integration of patterns and dynamics. New York, Chapman and Hall.CrossRefGoogle Scholar
Perry, J.N. (1982) Fitting split-lines to ecological data. Ecological Entomology 7, 421–435.CrossRefGoogle Scholar
Perry, J.N., Rothery, P., Clark, S.J., Heard, M.S. & Hawes, C. (2003) Design, analysis and statistical power of the Farm-Scale Evaluations of genetically modified herbicide-tolerant crops. Journal of Applied Ecology 40, 17–31.CrossRefGoogle Scholar
Persson, L., Diehl, S., Johansson, L., Andersson, G. & Hamrin, S.F. (1992) Trophic interactions in temperate lake ecosystems: a test of food chain theory. American Naturalist 140, 59–84.CrossRefGoogle Scholar
Polis, G.A. & Holt, R.D. (1992) Intraguild predation: the dynamics of complex trophic interactions. Trends in Ecology and Evolution 7, 151–154.CrossRefGoogle ScholarPubMed
Power, M.E. (1990) Effects of fish in river food webs. Science 250, 811–814.CrossRefGoogle ScholarPubMed
Power, M.E. (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73, 733–746.CrossRefGoogle Scholar
Price, P.W., Bouton, C.E., Gross, B.A., McPheron, J.N., Thompson, J.N. & Weis, A.E. (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11, 41–65.CrossRefGoogle Scholar
Robinson, R.A. & Sutherland, W.J. (2002) Post-war changes in arable farming and biodiversity in Great Britain. Journal of Applied Ecology 39, 157–176.CrossRefGoogle Scholar
Root, R. (1973) Organisation of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecological Mongraphs 43, 95–124.CrossRefGoogle Scholar
Rosenzweig, M.L. (1971) Paradox of enrichment: destabilisation of exploitation ecosystems in ecological time. Science 171, 385–387.CrossRefGoogle Scholar
Roy, D.B., Bohan, D.A., Haughton, A.J., Hill, M.O., Osborne, J.L., Clark, S.J., Perry, J.N., Rothery, P., Scott, R.J., Brooks, D.R., Champion, G.T., Hawes, C., Heard, M.S. & Firbank, L.G. (2003) Invertebrates and vegetation of field margins adjacent to crops subject to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of the Royal Society of London, B 358, 1879–1898.Google ScholarPubMed
Siemann, E., Tilman, D., Haarstad, J. & Ritchie, M. (1998) Experimental tests of the dependence of arthropod diversity on plant diversity. American Naturalist 152, 738–750.CrossRefGoogle ScholarPubMed
Siriwardena, G.M., Baillie, S.R., Buckland, S.T., Fewster, R.M., Marchant, J.H. & Wilson, J.D. (1998) Trends in the abundance of farmland birds: a quantitative comparison of smoothed Common Bird Census indices. Journal of Applied Ecology 35, 24–43.CrossRefGoogle Scholar
Sokal, R.R. & Rohlf, F.J. (1981) Biometry. 2nd edn. New YorkW.H. Freeman and Company.Google Scholar
Spiller, D.A. & Schoener, T.W. (1994) Effects of top and intermediate predators in a terrestrial food web. Ecology 75, 182–196.CrossRefGoogle Scholar
Squire, G.R., Brooks, D.R., Bohan, D.A., Champion, G.T., Daniels, R.E., Haughton, A.J., Hawes, C., Heard, M.S., Hill, M.O., May, M.J., Osborne, J.L., Perry, J.N., Roy, D.B., Woiwod, I.P. & Firbank, L.G. (2003) On the rationale and interpretation of the Farm Scale Evaluations of genetically modified herbicide-tolerant crops. Philosophical Transactions of the Royal Society of London, B 358, 1779–1799.Google ScholarPubMed
Stinson, C.S.A. & Brown, V.K. (1983) Seasonal changes in the architecture of natural plant communities and its relevance to insect herbivores. Oecologia 56, 67–69.CrossRefGoogle ScholarPubMed
Strong, D.R. (1992) Are trophic cascades all wet? Differentation and donor-control in speciose ecosystems. Ecology 73, 747–754.CrossRefGoogle Scholar
Williams, P.H. (1986) Environmental change and the distributions of British bumble bees (Bombus latr). Bee World 67, 50–61.CrossRefGoogle Scholar
Wilson, J.B. (1999) Guilds, functional types and ecological groups. Oikos 86, 507–522.CrossRefGoogle Scholar
Woiwod, I.P. & Harrington, R. (1994) Flying in the face change: the Rothamsted Insect Survey. pp. 321–337in Leigh, R.A. & Johnston, A.E. (Eds) Long-term experiments in agricultural and ecological sciences. Wallingford, Oxon, CAB International.Google Scholar