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Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Published online by Cambridge University Press:  10 October 2011

M. Traugott*
Affiliation:
Cardiff School of Biosciences, Biomedical Sciences Building, Cardiff University, Museum Avenue, Cardiff CF10 3AX, UK Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria
J.R. Bell
Affiliation:
Warwick HRI, University of Warwick, Wellesbourne, Warwick, CV35 9EF, UK
L. Raso
Affiliation:
Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria
D. Sint
Affiliation:
Mountain Agriculture Research Unit, Institute of Ecology, University of Innsbruck, Technikerstrasse 25, 6020 Innsbruck, Austria
W.O.C. Symondson
Affiliation:
Cardiff School of Biosciences, Biomedical Sciences Building, Cardiff University, Museum Avenue, Cardiff CF10 3AX, UK
*
*Author for correspondence Fax: +43 512 507 6190 E-mail: Michael.Traugott@uibk.ac.at

Abstract

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

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References

Agustí, N., Shayler, S.P., 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, 34673475.Google Scholar
Bell, J.R., Traugott, M., Sunderland, K.D., Skirvin, D.J., Mead, A., Kravar-Garde, L., Reynolds, K., Fenlon, J. & Symondson, W.O.C. (2008a) Beneficial links for the control of aphids: the effects of compost applications on predators and prey. Journal of Applied Ecology 45, 12661273.Google Scholar
Bell, J.R., Mead, A., Skirvin, D.J., Sunderland, K.D., Fenlon, J. & Symondson, W.O.C. (2008b) Do functional traits improve prediction of predation rates for a disparate group of aphid predators? Bulletin of Entomological Research 98, 587597.CrossRefGoogle ScholarPubMed
Bell, J.R., King, R.A., Bohan, D.A. & Symondson, W.O.C. (2010) Spatial co-occurrence networks predict the feeding histories of polyphagous arthropod predators at field scales. Ecography 33, 6472.Google Scholar
Brodeur, J. & Rosenheim, J.A. (2000) Intraguild interactions in aphid parasitoids. Entomologia Experimentalis et Applicata 97, 93108.CrossRefGoogle Scholar
Cardinale, B.J., Harvey, C.T., Gross, K. & Ives, A.R. (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecology Letters 6, 857865.Google Scholar
Chacon, J.M. & Heimpel, G.E. (2010) Density-dependent intraguild predation of an aphid parasitoid. Oecologia 164, 213220.CrossRefGoogle ScholarPubMed
Chambers, R.J., Sunderland, K.D., Stacey, D.L. & Wyatt, I.J. (1986) Control of cereal aphids by natural enemies – aphid-specific predators, parasitoids and pathogenic fungi. Annals of Applied Biology 108, 219231.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 109, 4960.Google Scholar
Edwards, C.A., Sunderland, K.D. & George, K.S. (1979) Studies on polyphagous predators of cereal aphids. Journal of Applied Ecology 16, 811823.CrossRefGoogle Scholar
Eitzinger, B. & Traugott, M. (2011) Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut content analysis. Journal of Applied Ecology 48, 591599.Google Scholar
Greenstone, M.H., Rowley, D.L., Weber, D.C., Payton, M.E. & Hawthorne, D.J. (2007) Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. Bulletin of Entomological Research 97, 201209.Google Scholar
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, 35493560.Google Scholar
Harwood, J.D., Desneux, N., Yoo, H.J.S., Rowley, D.L., Greenstone, M.H., Obrycki, J.J. & O'Neil, R.J. (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Molecular Ecology 16, 43904400.CrossRefGoogle ScholarPubMed
Hesterberg, T., Moore, D.S., Monaghan, S., Clipson, A. & Epstein, R. (2003) Bootstrap methods and permutation tests. pp. 14.114.70in Moore, D.S. & McCabe, G.P. (Eds) Introduction to the Practice of Statistics. New York, USA, W H Freeman & Co.Google Scholar
Juen, A. & Traugott, M. (2007) Revealing species-specific trophic links in soil food webs: Molecular identification of scarab predators. Molecular Ecology 16, 15451557.Google Scholar
King, R.A., Read, D.S., Traugott, M. & Symondson, W.O.C. (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17, 947963.CrossRefGoogle ScholarPubMed
King, R.A., Vaughan, I.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010) Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers. Molecular Ecology 19, 17211732.Google Scholar
Kuusk, A.-K. & Ekbom, B. (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biological Control 55, 2026.CrossRefGoogle Scholar
Kuusk, A.-K., Cassel-Lundhagen, A., Kvarnheden, A. & Ekbom, B. (2008) Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis. Basic and Applied Ecology 9, 718725.Google Scholar
Macfadyen, S., Gibson, R., Polaszek, A., Morris, R.J., Craze, P.G., Planque, R., Symondson, W.O.C. & Memmott, J. (2009) Do differences in food web structure between organic and conventional farms affect the ecosystem service of pest control? Ecology Letters 12, 229238.Google Scholar
Müller, C.B., Adriaanse, I.C.T., Belshaw, R. & Godfray, H.C.J. (1999) The structure of an aphid-parasitoid community. Journal of Animal Ecology 68, 346370.CrossRefGoogle Scholar
Nakamura, M. & Nakamura, K. (1977) Population dynamics of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). V. Estimation of the effect of predation by spiders on the mortality of imaginal wasps based on the precipitin test. Oecologia 27, 97116.Google Scholar
Östman, Ö., Ekbom, B. & Bengtsson, J. (2003) Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecological Economics 45, 149158.Google Scholar
Polis, G.A., Myers, C.A. & Holt, R.D. (1989) The ecology an evolution of intraguild predation: potential competitors that eat each other. Annual Review of Ecology and Systematics 20, 297330.CrossRefGoogle Scholar
Ruggle, P. & Holst, N. (1994) Life history parameters of parasitoids attacking cereal aphids. Norwegian Journal of Agricultural Sciences 16, 8388.Google Scholar
Schmidt, M.H., Lauer, A., Purtauf, T., Thies, C., Schaefer, M. & Tscharntke, T. (2003) Relative importance of predators and parasitoids for cereal aphid control. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, 19051909.Google Scholar
Schmidt, M.H., Thewes, U., Thies, C. & Tscharntke, T. (2004) Aphid suppression by natural enemies in mulched Cereals. Entomologia Experimentalis et Applicata 113, 8793.CrossRefGoogle Scholar
Sheppard, S.K., Bell, J.R., Sunderland, K.D., Fenlon, J., Skervin, D. & Symondson, W.O.C. (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Molecular Ecology 14, 44614468.Google Scholar
Sint, D., Raso, L., Kaufmann, R. & Traugott, M. (2011) Optimizing methods for PCR-based analysis of predation. Molecular Ecology Resources 11, 795801.Google Scholar
Snyder, G.B., Finke, D.L. & Snyder, W.E. (2008) Predator biodiversity strengthens aphid suppression across single- and multiple-species prey communities. Biological Control 44, 5260.CrossRefGoogle Scholar
Snyder, W.E. & Ives, A.R. (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82, 705716.Google Scholar
Sunderland, K.D., Axelsen, J.A., Dromph, K., Freier, B., Hemptinne, J.-L., Holst, N.H., Mols, P.J.M., Petersen, M.K., Powell, W., Ruggle, P., Triltsch, H. & Winder, L. (1997) Pest control by a community of natural enemies. Acta Jutlandica 72, 271326.Google Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627641.Google Scholar
Szendrei, Z., Greenstone, M.H., Payton, M.E. & Weber, D.C. (2010) Molecular gut-content analysis of a predator assemblage reveals the effect of habitat manipulation on biological control in the field. Basic and Applied Ecology 11, 153161.CrossRefGoogle Scholar
Traugott, M. & Symondson, W.O.C. (2008) Molecular analysis of predation on parasitized hosts. Bulletin of Entomological Research 98, 223231.Google Scholar
Traugott, M., Bell, J.R., Broad, G.R., Powell, W., van Veen, F.J.F., Vollhardt, I.M.G. & Symondson, W.O.C. (2008) Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Molecular Ecology 17, 39283938.Google Scholar
van Emden, H.F. & Harrington, R. (2007) Aphids as Crop Pests. Wallingford, UK, CABI.CrossRefGoogle Scholar
van Veen, F.J.F., Morris, R.J. & Godfray, H.C.J. (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annual Review of Entomology 51, 187208.Google Scholar
van Veen, F.J.F., Müller, C.B., Pell, J.K. & Godfray, H.C.J. (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. Journal of Animal Ecology 77, 191200.Google Scholar
Vance-Chalcraft, H.D., Rosenheim, J.A., Vonesh, J.R., Osenberg, C.W. & Sih, A. (2007) The influence of intraguild predation on prey suppression and prey release: a meta-analysis. Ecology 88, 26892696.CrossRefGoogle ScholarPubMed
Völkl, W. & Kraus, W. (1996) Foraging behaviour and resource utilization of the aphid parasitoid Pauesia unilachni: adaptation to host distribution and mortality risks. Entomologia Experimentalis et Applicata 79, 101109.Google Scholar
von Berg, K., Thies, C., Tscharntke, T. & Scheu, S. (2009) Cereal aphid control by generalist predators in presence of below-ground alternative prey: Complementary predation as affected by prey density. Pedobiologia 53, 4148.Google Scholar
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