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Non-pest prey do not disrupt aphid predation by a web-building spider

Published online by Cambridge University Press:  20 November 2015

K.D. Welch*
Affiliation:
USDA-ARS, North Central Agricultural Research Laboratory, Brookings, South Dakota, 57006, USA Department of Entomology, University of Kentucky, Lexington, Kentucky, 40546, USA
T.D. Whitney
Affiliation:
Department of Entomology, University of Kentucky, Lexington, Kentucky, 40546, USA
J.D. Harwood
Affiliation:
Department of Entomology, University of Kentucky, Lexington, Kentucky, 40546, USA
*
*Author for correspondence Phone: 1 (605) 688-4768 E-mail: [email protected]

Abstract

A generalist predator's ability to contribute to biological control is influenced by the decisions it makes during foraging. Predators often use flexible foraging tactics, which allows them to pursue specific types of prey at the cost of reducing the likelihood of capturing other types of prey. When a pest insect has low nutritional quality or palatability for a predator, the predator is likely to reject that prey in favour of pursuing alternative, non-pest prey. This is often thought to limit the effectiveness of generalist predators in consuming aphids, which are of low nutritional quality for many generalist predators. Here, we report behavioural assays that test the hypothesis that the generalist predator, Grammonota inornata (Araneae: Linyphiidae), preferentially forages for a non-pest prey with high nutritional quality (springtails), and rejects a pest prey with low nutritional quality (aphids). In no-choice assays, molecular gut-content analysis revealed that spiders continued to feed on the low-quality aphids at high rates, even when high-quality springtails were readily available. When provided a choice between aphids and springtails in two-way choice tests, spiders did not show the expected preference for springtails. Decision-making by spiders during foraging therefore appears to be sub-optimal, possibly because of attraction to the less frequently encountered of two preys as part of a dietary diversification strategy. These results indicate that behavioural preferences alone do not necessarily compromise the pest-suppression capacity of natural enemies: even nutritionally sub-optimal pest prey can potentially be subject to predation and suppression by natural enemies.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2015 

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References

Alderweireldt, M. (1994) Prey selection and prey capture strategies of linyphiid spiders in high-input agricultural fields. Bulletin of the British Arachnological Society 9, 300308.Google Scholar
Arnó, J., Roig, J. & Riudavets, J. (2008) Evaluation of Orius majusculus and O. laevigatus as predators of Bemisa tabaci and estimation of their prey preference. Biological Control 44, 16.Google Scholar
Bilde, T. & Toft, S. (2000) Evaluation of prey for the spider Dicymbium brevisetosum Locket (Araneae: Linyphiidae) in single-species and mixed-species diets. Ekologia-Bratislava 19, 918.Google Scholar
Bilde, T. & Toft, S. (2001) The value of three cereal aphid species as food for a generalist predator. Physiological Entomology 26, 5868.CrossRefGoogle Scholar
Bilde, T., Axelsen, J.A. & Toft, S. (2000) The value of Collembola from agricultural soils as food for a generalist predator. Journal of Applied Ecology 37, 672683.Google Scholar
Blackledge, T.A. & Wenzel, J.W. (2001) State-determinate foraging decisions and web architecture in the spider Dictyna volucripes (Araneae, Dictynidae). Ethology Ecology and Evolution 13, 105113.CrossRefGoogle Scholar
Chapman, E.G., Schmidt, J.M., Welch, K.D. & Harwood, J.D. (2013) Molecular evidence for dietary selectivity and pest suppression potential in an epigeal spider community in winter wheat. Biological Control 65, 7286.CrossRefGoogle Scholar
Chen, Y., Giles, K.L., Payton, M.E. & Greenstone, M.H. (2000) Identifying key cereal aphid predators by molecular gut analysis. Molecular Ecology 9, 18871898.CrossRefGoogle ScholarPubMed
Croissant, Y. (2013) mlogit: multinomial logit model. http://CRAN.R-project.org/package=mlogit.Google Scholar
D'Arcy, C.J. & Burnett, P.A. (eds) (1995) Barley Yellow Dwarf: 40 Years of Progress St. Paul. Minnesota, USA, The American Phytopathological Society.Google Scholar
Gavish-Regev, E., Rotkopf, R., Lubin, Y. & Coll, M. (2009) Consumption of aphids by spiders and the effect of additional prey: evidence from microcosm experiments. BioControl 54, 341350.Google Scholar
Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2001) Living where the food is: web location by linyphiid spiders in relation to prey availability in winter wheat. Journal of Applied Ecology 38, 8899.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.CrossRefGoogle ScholarPubMed
Huseynov, E.F., Cross, F.R. & Jackson, R.R. (2005) Natural diet and prey-choice behaviour of Aelurillus muganicus (Araneae: Salticidae), a myrmecophagic jumping spider from Azerbaijan. Journal of Zoology 267, 159165.Google Scholar
Huseynov, E.F., Jackson, R.R. & Cross, F.R. (2008) The meaning of predatory specialization as illustrated by Aelurillus m-nigrum, an ant-eating jumping spider (Araneae: Salticidae) from Azerbaijan. Behavioural Processes 77, 389399.Google Scholar
Kerzicnik, L.M., Chapman, E.G., Harwood, J.D., Peairs, F.B. & Cushing, P.E. (2012) Molecular characterization of Russian wheat aphid consumption by spiders in winter wheat. Journal of Arachnology 40, 7177.Google Scholar
Koss, A.M. & Snyder, W.E. (2005) Alternative prey disrupt biocontrol by a guild of generalist predators. Biological Control 32, 243251.CrossRefGoogle Scholar
Kuusk, A.K. & Agusti, N. (2008) Group-specific primers for DNA-based detection of springtails (Hexapoda: Collembola) within predator gut contents. Molecular Ecology Resources 8, 678681.Google Scholar
Madsen, M., Terkildsen, S. & Toft, S. (2004) Microcosm studies on control of aphids by generalist arthropod predators: effects of alternative prey. BioControl 49, 483504.CrossRefGoogle Scholar
Mansour, F. & Heimbach, U. (1993) Evaluation of lycosid, micryphantid and linyphiid spiders as predators of Rhopalosiphum padi (Homoptera, Aphididae) and their functional response to prey density – laboratory experiments. Entomophaga 38, 7987.CrossRefGoogle Scholar
Marcussen, B.M., Axelsen, J.A. & Toft, S. (1999) The value of two Collembola species as food for a linyphiid spider. Entomologia Experimentalis et Applicata 92, 2936.CrossRefGoogle Scholar
Mayntz, D., Raubenheimer, D., Salomon, M., Toft, S. & Simpson, S.J. (2005) Nutrient-specific foraging in invertebrate predators. Science 307, 111113.Google Scholar
Nyffeler, M. (1999) Prey selection of spiders in the field. Journal of Arachnology 27, 317324.Google Scholar
Oelbermann, K. & Scheu, S. (2009) Control of aphids on wheat by generalist predators: effects of predator density and the presence of alternative prey. Entomologia Experimentalis et Applicata 132, 225231.Google Scholar
Peterson, J.A., Romero, S.A. & Harwood, J.D. (2010) Pollen interception by linyphiid spiders in a corn agroecosystem: implications for dietary diversification and risk-assessment. Arthropod–Plant Interactions 4, 207217.Google Scholar
Pruitt, J.N., DiRienzo, N., Kralj-Fišer, S., Johnson, J.C. & Sih, A. (2011) Individual-and condition-dependent effects on habitat choice and choosiness. Behavioral Ecology and Sociobiology 65, 19871995.CrossRefGoogle Scholar
R Core Development Team (2015) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. http://www.R-project.org/.Google Scholar
Romero, S.A. & Harwood, J.D. (2010) Diel and seasonal patterns of prey available to epigeal predators: evidence for food limitation in a linyphiid spider community. Biological Control 52, 8490.Google Scholar
Schmidt, J.M., Peterson, J.A., Lundgren, J.G. & Harwood, J.D. (2013) Dietary supplementation with pollen enhances survival and Collembola boosts fitness of a web-building spider. Entomologia Experimentalis et Applicata 149, 282291.CrossRefGoogle Scholar
Symondson, W.O.C., Cesarini, S., Dodd, P.W., Harper, G.L., Bruford, M.W., Glen, D.M., Wiltshire, C.W. & Harwood, J.D. (2006) Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles. Bulletin of Entomological Research 96, 637645.Google Scholar
Toft, S. (1995) Value of the aphid Rhopalosiphum padi as food for cereal spiders. Journal of Applied Ecology 32, 552560.Google Scholar
Toft, S. (2005) The quality of aphids as food for generalist predators: implications for natural control of aphids. European Journal of Entomology 102, 371383.Google Scholar
Toft, S. & Wise, D.H. (1999) Behavioral and ecophysiological responses of a generalist predator to single- and mixed-species diets of different quality. Oecologia 119, 198207.Google Scholar
von Berg, K., Thies, C., Tscharntke, T. & Scheu, S. (2009) Cereal aphid control by generalist predators in presence of belowground alternative prey: complementary predation as affected by prey density. Pedobiologia 53, 4148.CrossRefGoogle Scholar
Welch, K.D., Haynes, K.F. & Harwood, J.D. (2013 a) Prey-specific foraging tactics in a web-building spider. Agricultural and Forest Entomology 15, 375381.Google Scholar
Welch, K.D., Haynes, K.F. & Harwood, J.D. (2013 b) Microhabitat evaluation and utilization by a foraging predator. Animal Behaviour 85, 419425.Google Scholar
Welch, K.D., Schofield, M.R., Chapman, E.G. & Harwood, J.D. (2014) Comparing rates of springtail predation by web-building spiders using Bayesian inference. Molecular Ecology 23, 38143825.Google Scholar
Wilder, S.M. & Rypstra, A.L. (2008) Diet quality affects mating behaviour and egg production in a wolf spider. Animal Behaviour 76, 439445.Google Scholar