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Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles

Published online by Cambridge University Press:  24 July 2007

W.O.C. Symondson ,
S. Cesarini ,
P.W. Dodd ,
G.L. Harper ,
M.W. Bruford ,
D.M. Glen ,
C.W. Wiltshire  and
J.D. Harwood
W.O.C. Symondson*
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
S. Cesarini
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
P.W. Dodd
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
G.L. Harper
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
M.W. Bruford
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
D.M. Glen
Affiliation:
IACR-Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol, BS41 9AF, UK
C.W. Wiltshire
Affiliation:
Arion Ecology, The Brambles, Stinchcombe Hill, Dursley, Gloucestershire, GL11 6AQ, UK
J.D. Harwood
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
*
*Fax: +44 (0)29 20 874 305 E-mail: Symondson@Cardiff.ac.uk
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Abstract

Environment-friendly farming techniques seek to increase invertebrate biodiversity in part with the intention of encouraging greater numbers of predators that will help to control crop pests. However, in theory, this effect may be negated if the availability of a greater abundance and diversity of alternative prey diverts predators away from feeding on pests. The hypothesis that access to alternative prey can lead to reduced pest suppression under semi-field conditions was tested. Alternative prey type and diversity were manipulated in 70 mesocosms over 7+ weeks in the presence of the carabid Pterostichus melanarius (Illiger), a known predator of slugs, and reproducing populations of the slug Deroceras reticulatum (Müller). Significantly fewer slugs survived where no alternative prey were provided. Maximum slug numbers and biomass were found in treatments containing either carabids plus a high diversity of alternative prey (many species of earthworm and three of Diptera larvae) or a single additional prey (blowfly larvae, Calliphora vomitoria Linnaeus). In these treatments slug numbers and biomass were as high as in plots lacking predators. The effects of alternative prey were taxon-specific. Alternative prey strongly affected carabid fitness in terms of biomass and egg load. The fittest predators (those with access to high alternative prey diversity or C. vomitoria larvae) reduced slug numbers the least. The mean individual slug weights were greater in treatments with alternative prey than where no alternative prey were provided to the carabids. These results suggest that pests may survive and reproduce more rapidly in patches where predators have access to alternative prey.

Keywords

CarabidaeDeroceras reticulatumdietgeneralist predatorspredator fitnessPterostichus melanariusslugs

Information

Type
Research Article
Information
Bulletin of Entomological Research , Volume 96 , Issue 6 , December 2006 , pp. 637 - 645
Copyright
Copyright © Cambridge University Press 2006

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References

Agustí, N., Shayler, S., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 3467–3475.CrossRefGoogle ScholarPubMed
Bohan, D.A., Bohan, A.C., Glen, D.M., Symondson, W.O.C., Wiltshire, C.W. & Hughes, L. (2000) Spatial dynamics of predation by carabid beetles on slugs. Journal of Animal Ecology 69, 367–379.CrossRefGoogle Scholar
Bommarco, R. (1998) Reproduction and energy reserves of a predatory carabid beetle relative to agroecosystems complexity. Ecological Applications 8, 846–853.CrossRefGoogle Scholar
Bommarco, R. (1999) Feeding, reproduction and community impact of a predatory carabid in two agricultural habitats. Oikos 87, 89–96.CrossRefGoogle Scholar
Buckland, S.M. & Grime, J.P. (2000) The effects of trophic structure and soil fertility on the assembly of plant communities. Oikos 91, 336–352.CrossRefGoogle Scholar
Chang, G.C. & Kareiva, P. (1999) The case for indigenous generalists in biological control. pp. 103–115 in Hawkins, B.A. & Cornell, H.V. (Eds) Theoretical approaches to biological control. Cambridge, Cambridge University Press.CrossRefGoogle Scholar
Cornic, J.F. (1973) Etude du régime alimentaire de trois espèces de Carabiques et de ses variations en verger de pommiers. Annales Société Entomologique de France 9, 69–87.CrossRefGoogle Scholar
Chiverton, P.A. (1987) Predation of Rhopalosiphum padi (Homoptera: Aphididae) by polyphagous predatory arthropods during the aphids' pre-peak period in spring barley. Annals of Applied Biology 111, 257–269.CrossRefGoogle Scholar
Dodd, C.S., Bruford, M.W., Symondson, W.O.C. & Glen, D.M. (2003) Detection of slug DNA within carabid predators using prey-specific PCR primers. pp. 13–20 in Slug and snail pests: agricultural, veterinary and environmental perspectives. Alton, British Crop Protection Council.Google Scholar
El Titi, A. (2003) Effects of tillage on invertebrates in agroecosystems. pp. 261–296 in El Titi, A. (Ed.) Soil tillage in agroecosystems. London, CRC Press.Google Scholar
Finch, S. (1996) Effect of beetle size on predation of cabbage root fly eggs by ground beetles. Entomologia Experimentalis et Applicata 81, 199–206.CrossRefGoogle Scholar
Finke, D.L. & Denno, R.F. (2004) Predator diversity dampens trophic cascades. Nature 429, 407–410.CrossRefGoogle ScholarPubMed
Fisker, E.N. & Toft, S. (2004) Effects of chronic exposure to a toxic prey in a generalist predator. Physiological Entomology 29, 129–138.CrossRefGoogle Scholar
Fry, J.C. (1993) Biological data analysis: a practical approach. Oxford, IRL Press.CrossRefGoogle Scholar
Glen, D.M. & Symondson, W.O.C. (2003) Influence of soil tillage on slugs and their natural enemies. pp. 207–227 in El Titi, A. (Ed.) Soil tillage in agroecosystems. London, CRC Press.Google Scholar
Glen, D.M., Wiltshire, C.W. & Milsom, N.F. (1988) Effects of straw disposal on slug problems in cereals. Aspects of Applied Biology 17, 173–179.Google Scholar
Glen, D.M., Milsom, N.F. & Wiltshire, C.W. (1989) Effects of seed-bed conditions on slug numbers and damage to winter wheat in a clay soil. Annals of Applied Biology 115, 177–190.CrossRefGoogle Scholar
Greene, A. (1975) Biology of five species of Cychrini (Coleoptera: Carabidae) in the steppe region of south-eastern Washington. Melanderia 19, 1–43.Google Scholar
Greenstone, M.H. (1979) Spider behaviour optimises dietary essential amino acid composition. Nature 282, 501–503.CrossRefGoogle Scholar
Halaj, J. & Wise, D.H. (2002) Impact of a detrital subsidy on trophic cascades in a terrestrial grazing food web. Ecology 83, 3141–3151.CrossRefGoogle Scholar
Harmon, J.P. & Andow, D.A. (2004) Indirect effects between shared prey: predictions for biological control. BioControl 49, 605–626.CrossRefGoogle Scholar
Harper, G.L., King, R.A., Dodd, C.S., Harwood, J.D., Glen, D.M., Bruford, M.W. & Symondson, W.O.C. (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology 14, 819–827.CrossRefGoogle ScholarPubMed
Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2004) Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. Molecular Ecology 13, 3549–3560.CrossRefGoogle ScholarPubMed
Holland, J.M. (2004) The environmental consequences of adopting conservation tillage in Europe: reviewing the evidence. Agriculture, Ecosystems and Environment 103, 1–25.CrossRefGoogle Scholar
Holland, J.M. & Reynolds, C.J.M. (2003) The impact of soil cultivation on arthropod (Coleoptera and Araneae) emergence on arable land. Pedobiologia 47, 181–191.CrossRefGoogle Scholar
Holt, R.D. & Lawton, J.H. (1994) The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25, 495–520.CrossRefGoogle Scholar
Jones, A.A. & Selman, B.J. (1985) Microsporidium novacastriensis n. sp., a mircosporidian parasite of the grey field slug, Deroceras reticulatum. Journal of Protozoology 34, 581–586.CrossRefGoogle Scholar
Kendall, D.A., Chinn, N.E., Glen, D.M., Wiltshire, C.W., Winstone, L. & Tidbold, C. (1995) Effects of soil management on cereal pests and their natural enemies. pp. 83–102 in Glen, D.M., Greaves, M.P. & Anderson, H.M. (Eds) Ecology and integrated farming systems. Chichester, John Wiley & Sons.Google Scholar
Kladivko, E.J. (2001) Tillage systems and soil ecology. Soil and Tillage Research 61, 61–76.CrossRefGoogle Scholar
Köller, K. (2003) Techniques of soil tillage. pp. 1–25 in El Titi, A. (Ed.) Soil tillage in agroecosystems. London, CRC Press.Google Scholar
Koss, A.M. & Snyder, W.E. (2005) Alternative prey disrupt biocontrol by a guild of generalist predators. Biological Control 32, 243–251.CrossRefGoogle Scholar
Mayntz, D., Raubenheimer, D., Salomon, M., Toft, S. & Simpson, S.J. (2005) Nutrient-specific foraging in invertebrate predators. Science 307, 111–113.CrossRefGoogle ScholarPubMed
McCann, K.S., Hastings, A. & Huxel, G.R. (1998) Weak trophic interactions and the balance of nature. Nature 395, 794–798.CrossRefGoogle Scholar
McKemey, A., Symondson, W.O.C., Glen, D.M. & Brain, P. (2001) Effects of slug size on predation by Pterostichus melanarius (Coleoptera: Carabidae). Biocontrol Science and Technology 11, 83–93.CrossRefGoogle Scholar
McKemey, A., Symondson, W.O.C. & Glen, D.M. (2003) Predation and prey size choice by the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae): the dangers of extrapolating from laboratory to field. Bulletin of Entomological Research 93, 227–234.CrossRefGoogle ScholarPubMed
Moran, M.D. (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100, 403–405.CrossRefGoogle Scholar
Murdoch, W.W., Chesson, J. & Chesson, P.L. (1985) Biological control in theory and practice. American Naturalist 125, 344–366.CrossRefGoogle Scholar
Oberholzer, F. & Frank, T. (2003) Predation by the carabid beetles Pterostichus melanarius and Poecilus cupreus on slugs and slug eggs. Biocontrol Science and Technology 13, 99–110.CrossRefGoogle Scholar
Oberholzer, F., Escher, N. & Frank, T. (2003) The potential of carabid beetles (Coleoptera) to reduce slug damage to oilseed rape in the laboratory. European Journal of Entomology 100, 81–85.CrossRefGoogle Scholar
Oelbermann, K. & Scheu, S. (2002) Effects of prey type and mixed diets on survival, growth and development of a generalist predator, Pardosa lugubris. Basic and Applied Ecology 3, 285–291.CrossRefGoogle Scholar
Perneger, T.V. (1998) What's wrong with Bonferroni adjustments? British Medical Journal 316, 1236–1238.CrossRefGoogle ScholarPubMed
Polis, G.A., Myers, C.A. & Holt, R.D. (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology and Systematics 20, 297–330.CrossRefGoogle Scholar
Pyke, G.H. (1984) Optimal foraging theory: a critical review. Annual Review of Ecology and Systematics 15, 523–575.CrossRefGoogle Scholar
Rypstra, A.L. & Marshall, S.D. (2005) Augmentation of soil detritus affects the spider community and herbivory in a soybean agroecosystem. Entomologia Experimentalis et Applicata 116, 149–157.CrossRefGoogle Scholar
Settle, W.H., Ariawan, H., Astuti, E.T., Cahyana, W., Hakim, A.L., Hindayana, D., Lestari, A.S. & Sartanto, P. (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77, 1975–1988.CrossRefGoogle Scholar
Sheppard, S.K. & Harwood, J.D. (2005) Advances in molecular ecology: tracking trophic links through predator–prey food webs. Functional Ecology 19, 751–762.CrossRefGoogle Scholar
Sims, R.W. & Gerard, B.M. (1985) Earthworms. London, E.J. Brill/Dr W. Backhuys.CrossRefGoogle Scholar
Stephens, D.W. & Krebs, J.R. (1986) Foraging theory. Princeton, Princeton University Press.Google Scholar
Stinner, B.R. & House, G.J. (1990) Arthropods and other invertebrates in conservation tillage agriculture. Annual Review of Entomology 35, 299–318.CrossRefGoogle Scholar
Sunderland, K.D. (1975) The diet of some predatory arthropods in cereal crops. Journal of Applied Ecology 17, 389–396.CrossRefGoogle Scholar
Sunderland, K.D. (2002) Invertebrate pest control by carabids. pp. 165–214 in Holland, J.M. (Ed.) The agroecology of carabid beetles. Andover, Intercept.Google Scholar
Sunderland, K.D., Powell, W. & Symondson, W.O.C. (2005) Populations and communities. pp. 299–434 in Jervis, M.A. (Ed.) Insects as natural enemies: a practical perspective. Berlin, Springer.CrossRefGoogle Scholar
Symondson, W.O.C. (1993) Chemical confinement of slugs: an alternative to electric fences. Journal of Molluscan Studies 59, 259–261.CrossRefGoogle Scholar
Symondson, W.O.C. (1997) Does Tandonia budapestensis (Mollusca: Pulmonata) contain toxins? Evidence from feeding trials with the slug predator Pterostichus melanarius (Coleoptera: Carabidae). Journal of Molluscan Studies 7, 457–465.Google Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.CrossRefGoogle ScholarPubMed
Symondson, W.O.C. (2004) Coleoptera (Carabidae, Drilidae, Lampyridae and Staphylinidae) as predators of terrestrial gastropods. pp. 37–84 in Barker, G.M. (Ed.) Natural enemies of terrestrial molluscs. Wallingford, Oxon, CAB International.CrossRefGoogle Scholar
Symondson, W.O.C., Glen, D.M.Wiltshire, C.WLangdon, C.J. & Liddell, J.E. (1996) Effects of cultivation techniques and methods of straw disposal on predation by Pterostichus melanarius (Coleoptera: Carabidae) upon slugs (Gastropoda: Pulmonata) in an arable field. Journal of Applied Ecology 33, 741–753.CrossRefGoogle Scholar
Symondson, W.O.C., Glen, D.M., Erickson, M.L., Liddell, J.E. & Langdon, C.J. (2000) Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera: Carabidae) within crops? Investigations using a monoclonal antibody-based detection system. Molecular Ecology 9, 1279–1292.CrossRefGoogle Scholar
Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002a) Can generalist predators be effective biocontrol agents? Annual Review of Entomology 47, 561–594.CrossRefGoogle ScholarPubMed
Symondson, W.O.C., Glen, D.M., Ives, A.R., Langdon, C.J. & Wiltshire, C.W. (2002b) Dynamics of the relationship between a generalist predator and slugs over five years. Ecology 83, 137–147.CrossRefGoogle Scholar
Thomas, C.F.G., Parkinson, L. & Marshall, E.J.P. (1998) Isolating the components of activity-density for the carabid beetle Pterostichus melanarius in farmland. Oecologia 116, 103–112.CrossRefGoogle ScholarPubMed
Thomas, R.S. (2002) An immunological and behavioural study of the role of carabid beetle larvae as pest control agents in cereal crops. PhD thesis, Cardiff University, Cardiff, UK.Google Scholar
Thorbeck, P. & Bilde, T. (2004) Reduced numbers of generalist arthropod predators after crop management. Journal of Applied Ecology 41, 526–538.CrossRefGoogle Scholar
Tod, M.E. (1973) Notes on beetle predators of molluscs. Entomologist 106, 196–201.Google Scholar
Toft, S. & Wise, D.H. (1999) Growth, development and survival of a generalist predators fed single- and mixed-species diets of different quality. Oecologia 119, 191–197.CrossRefGoogle ScholarPubMed
Wilson, M.J., Glen, D.M. & George, S.K. (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Science and Technology 3, 503–511.CrossRefGoogle Scholar
Winder, L., Alexander, C.J., Holland, J.M., Woolley, C. & Perry, J. (2005a) Modelling the dynamic spatio-temporal response of predators to transient prey patches in the field. Ecology Letters 4, 568–576.CrossRefGoogle Scholar
Winder, L., Alexander, C.J., Holland, J.M., Symondson, W.O.C., Perry, J. & Woolley, C. (2005b) Predatory activity and spatial pattern: the response of generalist carabids to their aphid prey. Journal of Animal Ecology 74, 443–454.CrossRefGoogle Scholar