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Molecular analysis of faecal samples from birds to identify potential crop pests and useful biocontrol agents in natural areas

  • R.A. King (a1), W.O.C. Symondson (a1) and R.J. Thomas (a1)

Abstract

Wild habitats adjoining farmland are potentially valuable sources of natural enemies, but also of pests. Here we tested the utility of birds as ‘sampling devices’, to identify the diversity of prey available to predators and particularly to screen for pests and natural enemies using natural ecosystems as refugia. Here we used PCR to amplify prey DNA from three sympatric songbirds foraging on small invertebrates in Phragmites reedbed ecosystems, namely the Reed Warbler (Acrocephalus scirpaceus), Sedge Warbler (Acrocephalus schoenobaenus) and Cetti's Warbler (Cettia cetti). A recently described general invertebrate primer pair was used for the first time to analyse diets. Amplicons were cloned and sequenced, then identified by reference to the Barcoding of Life Database and to our own sequences obtained from fresh invertebrates. Forty-five distinct prey DNA sequences were obtained from 11 faecal samples, of which 39 could be identified to species or genus. Targeting three warbler species ensured that species-specific differences in prey choice broadened the range of prey taken. Amongst the prey found in reedbeds were major pests (including the tomato moth Lacanobia oleracea) as well as many potentially valuable natural enemies including aphidophagous hoverflies and braconid wasps. Given the mobility of birds, this approach provides a practical way of sampling a whole habitat at once, providing growers with information on possible invasion by locally resident pests and the colonization potential of natural enemies from local natural habitats.

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* Author for correspondence Phone: +44 (0)1392 725296 E-mail: R.A.King@Exeter.ac.uk

References

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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.
Alonso, H., Granadeiro, J.P., Waap, S., Xavier, J., Symondson, W.O.C., Ramos, J.A. & Catry, P. (2014) An holistic ecological analysis of the diet of Cory's shearwaters using prey morphological characters and DNA barcoding. Molecular Ecology 23, 37193733.
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.
Bianchi, F.J.J.A., Booij, C.J.H. & Tscharntke, T. (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proceedings of the Royal Society B 273, 17151727.
Bibby, C.J. & Green, R.E. (1981) Autumn migration strategies of Reed and Sedge Warblers. Ornis Scandinavica 12, 112.
Bibby, C.J. & Thomas, D.K. (1985) Breeding and diets of the Reed Warbler at a rich and a poor site. Bird Study 32, 1931.
Blondel, J., Dervieux, A., Maistre, M. & Perret, P. (1991) Feeding ecology and life history variation of the Blue Tit in Mediterranean deciduous and sclerophyllous habitats. Oecologia 88, 914.
Brown, D.S., Jarman, S.N. & Symondson, W.O.C. (2012) Pyrosequencing of prey DNA in reptile faeces: analysis of earthworm consumption by slow worms. Molecular Ecology Resources 12, 259266.
Brown, D.S., Burger, R., Cole, N., Vencatasamy, D., Clare, E.L., Montazam, A. & Symondson, W.O.C. (2014) Dietary competition between the alien Asian Musk Shrew (Suncus murinus) and a reintroduced population of Telfair's Skink (Leiolopisma telfairii). Molecular Ecology 23, 36953705.
Chaplin-Kramer, R., O'Rourke, M.E., Blitzer, E.J. & Kremen, C. (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecology Letters 14, 922932.
Chernetsov, N. & Manukyan, A. (2000) Foraging strategy of the Sedge Warbler (Acrocephalus schoenobaenus) on migration. Die Vogelwarte 40, 189197.
Clare, E.L., Barber, B.R., Sweeney, B.W., Hebert, P.D.N. & Fenton, M.B. (2011) Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus). Molecular Ecology 20, 17721780.
Clare, E.L., Symondson, W.O.C. & Fenton, M.B. (2014) An inordinate fondness for beetles? Variation in seasonal dietary preferences of night roosting big brown bats (Eptesicus fuscus). Molecular Ecology 23, 36333647.
Cramp, S., Simmons, K.E.L. & Perrins, C.M. (2004) The Birds of the Western Palearctic Interactive DVD-ROM v1.00. UK, Birdguides Ltd.
Davey, J.S., Vaughan, I.P., King, R.A., Bell, J.R., Bohan, D.A., Bruford, M.W., Holland, J.M. & Symondson, W.O.C. (2013) Intraguild predation in winter wheat: prey choice by a common epigeal carabid consuming spiders. Journal of Applied Ecology 50, 271279.
Davies, N.B. & Green, R.E. (1976) The development and ecological significance of feeding techniques in the Reed Warbler (Acrocephalus scirpaceus). Animal Behaviour 24, 213229.
Deagle, B.E., Gales, N.J., Evans, K., Jarman, S.N., Robinson, S., Trebilco, R. & Hindell, M.A. (2007) Studying seabird diet through genetic analysis of faeces: a case study on macaroni penguins (Eudyptes chrysolophus). PLoS ONE 2, e831.
Deagle, B.E., Chiaradia, A., McInnes, J. & Jarman, S.N. (2010) Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out? Conservation Genetics 11, 20392048.
Derocles, S.A.P., Le Ralec, A., Besson, M.M., Maret, M., Walton, A., Evans, D.M. & Plantegenest, M. (2014) Molecular analysis reveals high compartmentalization in aphid-primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats. Molecular Ecology 23, 39003911.
Dziock, F. (2005) Evolution of prey specialization in aphidophagous syrphids of the genera Melanostoma and Platycheirus (Diptera : Syrphidae) – 1. Body size, development and prey traits. European Journal of Entomology 102, 413421.
Eggenschwiler, L., Speiser, B., Bosshard, A. & Jacot, K. (2013) Improved field margins highly increase slug activity in Switzerland. Agronomy for Sustainable Development 33, 349354.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for the amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.
Gratton, C., Donaldson, J. & vander Zanden, M.J. (2008) Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11, 764774.
Greenstone, M.H., Payton, M.E., Weber, D.C. & Simmons, A.M. (2014) The detectability half-life in arthropod predator–prey research: what it is, why we need it, how to measure it, and how to use it. Molecular Ecology 23, 37993813.
Grim, T. (2006) An exceptionally high diversity of hoverflies (Syrphidae) in the food of the reed warbler (Acrocephalus scirpaceus). Biologia 61, 235239.
Halpern, M., Raats, D., Lavion, R. & Mittler, S. (2006) Dependent population dynamics between chironomids (nonbiting midges) and Vibrio cholera . FEMS Microbiology Ecology 55, 98104.
Harper, G.L., King, R.A., Dodd, C.S., Harwood, J.D., Glen, D., Bruford, M.W. & Symondson, W.O.C. (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology 14, 819827.
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.
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of birds through DNA barcodes. PLoS Biol 2, e312.
Hopkin, S.P. (2007) A key to the Collembola (Springtails) of Britain and Ireland. Shrewsbury, UK, FSC Publications.
Horvath, M.B., Martinez-Cruz, B., Negro, J.J., Kalmar, L. & Godoy, J.A. (2005) An overlooked DNA source for non-invasive genetic analysis in birds. Journal of Avian Biology 36, 8488.
Jarrett, P. & Burges, H.D. (2011) Control of the Tomato Moth Lacanobia oleracea by Bacillus thuringiensis on glasshouse tomatoes and the influence of larval behaviour. Entomologia Experimentalis et Applicata 31, 239244.
Jedlicka, J.A., Sharma, A.M. & Almeida, R.P.P. (2013) Molecular tools reveal diets of insectivorous birds from predator fecal matter. Conservation Genetic Resources 5, 879885.
Kerr, K.C.R., Lijtmaer, D.A., Barreira, A.S., Hebert, P.D.N. & Tubaro, P.L. (2009) Probing evolutionary patterns in Neotropical birds through DNA barcodes. PLoS ONE 4, e4379.
Kim, M.K., Kim, B.J., Lee, H., Won, Y.J. & Lee, S.D. (2009) Application of molecular methods to identify food resources of Short-Eared Owl (Asio flammeus) in wetland community. Genes and Genomics 31, 421427.
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. Journal of Molecular Evolution 15, 111120.
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.
King, R.A., Vaughan, I.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010 a) Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers. Molecular Ecology 19, 17211732.
King, R.A., Moreno-Ripoll, R., Agustí, N., Shayler, S.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010 b) Multiplex reactions for the molecular detection of predation on pest and non-pest invertebrates in agroecosystems. Molecular Ecology Resources 11, 370373.
Krüger, F., Clare, E.L., Greif, S., Siemers, B.M., Symondson, W.O.C. & Sommer, R.S. (2014) An integrative approach to detect subtle trophic niche differentiation in the sympatric trawling bat species Myotis dasycneme and Myotis daubentonii . Molecular Ecology 23, 36573671.
Macfadeyn, S., Gibson, R., Symondson, W.O.C. & Memmott, J. (2011) Landscape structure influences modularity patterns in farm food webs: consequences for pest control. Ecological Applications 21, 516524.
Medeiros, R.J. (2011) The migration strategy, diet and foraging ecology of a small seabird in a changing environment. PhD Thesis, Cardiff University.
Medeiros, R.J., King, R.A., Symondson, W.O.C., Cadiou, B., Zonfrillo, B., Bolton, M., Morton, R., Howell, S., Clinton, A., Felgueiras, M. & Thomas, R.J. (2012) Molecular evidence for gender differences in the migratory behaviour of a small seabird. PLoS ONE 7, e46330.
Nyman, T., Vikberg, V., Smith, D.R. & Boevé, J.L. (2010) How common is ecological speciation in plant-feeding insects? A ‘Higher’ Nematinae perspective. BMC Evolutionary Biology 10, 266.
Oehm, J., Juen, A., Nagiller, K., Neuhauser, S. & Traugott, M. (2011) Molecular scatology: how to improve prey DNA detection success in avian faeces? Molecular Ecology Reourcess 11, 620628.
Park, D.S., Foottit, R., Maw, E. & Hebert, P.D.N. (2011) Barcoding bugs: DNA-based identification of the true bugs (Insecta: Hemiptera: Heteroptera). PLoS ONE 6, e18749.
Pompanon, F., Deagle, B.E., Symondson, W.O.C., Brown, D.S., Jarman, S.D. & Taberlet, P. (2012) Who is eating what: diet assessment using next generation sequencing. Molecular Ecology 21, 19311950.
Poulakakis, N., Lymberakis, P., Paragamian, K. & Mylonas, M. (2005) Isolation and amplification of shrew DNA from barn owl pellets. Biological Journal of the Linnean Society 85, 331340.
Rakauskas, R.P. (1984) Hemiptera Heteroptera Nabidae Anthocoridae Miridae feeding on aphids from fruit and berry crops in Lithuanian-SSR USSR. Lietuvos TSR Mokslu Akademijos Darbai Serija C Biologijos Mokslai 2, 4549.
Robinson, R.A., Julliard, R. & Saracco, J.F. (2009) Constant effort: studying avian population processes using standardised ringing. Ringing and Migration 24, 199204.
Roe, A.D. & Sperling, F.A.H. (2007) Patterns of evolution of mitochondrial cytochrome c oxidase I and II and implications for DNA barcoding. Molecular Phylogenetics and Evolution 44, 325345.
Rosenberg, K.V. & Cooper, R.J. (1990) Approaches to avian diet analysis. pp. 8090 in Morrison, M.L., Ralph, C.J., Verner, J. & Jehl, J.R. (Eds) Avian Foraging: Theory, Methodology, and Applications. Los Angeles, USA, Cooper Ornithological Society.
Rotheray, G.E. (1983) Feeding behaviour of Syrphis ribesii and Melanostoma scalare on Aphis fabae . Entomologia Experimentalis et Applicata 34, 148154.
Scribner, K.T. & Bowman, T.D. (1998) Microsatellites identify depredated waterfowl remains from glaucous gull stomachs. Molecular Ecology 7, 14011405.
Sheppard, S.K., Bell, J.R., Sunderland, K.D., Fenlon, J., Skirvin, D.J. & Symondson, W.O.C. (2005) Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Molecular Ecology 14, 44614468.
Stubbs, A.E. & Falk, S.J. (2002) British Hoverflies. 2nd edn. Reading, UK, British Entomological and Natural History Society.
Sutherland, R.M. (2000) Molecular analysis of avian diets. PhD Thesis, University of Oxford, UK.
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627641.
Tamura, K., Dudle, J., Nei, M. & Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.
Thomas, C.F.G., Holland, J.M. & Brown, N.J. (2002) The spatial distribution of carabid beetles in agricultural landscapes. pp. 305344 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.
Tinbergen, L. (1960) The natural control of insects in pine woods I. Factors influencing the intensity of predation by songbirds. Archives Néerlandaises de Zoologie 13, 265343.
Traugott, M., Bell, J.R., Raso, L., Sint, D. & Symondson, W.O.C. (2012) Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. Bulletin of Entomolgical Research 102, 239247.
Vaughan, I.P., Newberry, C., Hall, D.J., Liggett, J.S. & Ormerod, S.J. (2008) Evaluating large-scale effects of Bacillus thuringiensis var. israelensis on non-biting midges (Chironomidae) in a eutrophic urban lake. Freshwater Biology 53, 21172128.

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Molecular analysis of faecal samples from birds to identify potential crop pests and useful biocontrol agents in natural areas

  • R.A. King (a1), W.O.C. Symondson (a1) and R.J. Thomas (a1)

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