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

Published online by Cambridge University Press:  09 January 2015

R.A. King ,
W.O.C. Symondson  and
R.J. Thomas
R.A. King*
Affiliation:
Cardiff School of Biosciences, The Sir Martin Evans Building, Cardiff University, Museum Avenue, Cardiff CF10 3AX, UK
W.O.C. Symondson
Affiliation:
Cardiff School of Biosciences, The Sir Martin Evans Building, Cardiff University, Museum Avenue, Cardiff CF10 3AX, UK
R.J. Thomas
Affiliation:
Cardiff School of Biosciences, The Sir Martin Evans Building, Cardiff University, Museum Avenue, Cardiff CF10 3AX, UK
*
* Author for correspondence Phone: +44 (0)1392 725296 E-mail: R.A.King@Exeter.ac.uk
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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.

Keywords

Acrocephalus schoenobaenusAcrocephalus scirpaceusCettia cettidietary analysisreedbed

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Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 3 , June 2015 , pp. 261 - 272
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Copyright © Cambridge University Press 2015 

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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, 3467–3475.Google Scholar
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, 3719–3733.Google Scholar
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, 64–72.Google Scholar
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, 1715–1727.Google Scholar
Bibby, C.J. & Green, R.E. (1981) Autumn migration strategies of Reed and Sedge Warblers. Ornis Scandinavica 12, 1–12.CrossRefGoogle Scholar
Bibby, C.J. & Thomas, D.K. (1985) Breeding and diets of the Reed Warbler at a rich and a poor site. Bird Study 32, 19–31.Google Scholar
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, 9–14.Google Scholar
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, 259–266.Google Scholar
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, 3695–3705.Google Scholar
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, 922–932.Google Scholar
Chernetsov, N. & Manukyan, A. (2000) Foraging strategy of the Sedge Warbler (Acrocephalus schoenobaenus) on migration. Die Vogelwarte 40, 189–197.Google Scholar
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, 1772–1780.Google ScholarPubMed
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, 3633–3647.Google Scholar
Cramp, S., Simmons, K.E.L. & Perrins, C.M. (2004) The Birds of the Western Palearctic Interactive DVD-ROM v1.00. UK, Birdguides Ltd.Google Scholar
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, 271–279.Google Scholar
Davies, N.B. & Green, R.E. (1976) The development and ecological significance of feeding techniques in the Reed Warbler (Acrocephalus scirpaceus). Animal Behaviour 24, 213–229.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 2039–2048.Google Scholar
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, 3900–3911.Google Scholar
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, 413–421.Google Scholar
Eggenschwiler, L., Speiser, B., Bosshard, A. & Jacot, K. (2013) Improved field margins highly increase slug activity in Switzerland. Agronomy for Sustainable Development 33, 349–354.Google Scholar
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, 294–299.Google Scholar
Gratton, C., Donaldson, J. & vander Zanden, M.J. (2008) Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11, 764–774.CrossRefGoogle Scholar
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, 3799–3813.Google Scholar
Grim, T. (2006) An exceptionally high diversity of hoverflies (Syrphidae) in the food of the reed warbler (Acrocephalus scirpaceus). Biologia 61, 235–239.Google Scholar
Halpern, M., Raats, D., Lavion, R. & Mittler, S. (2006) Dependent population dynamics between chironomids (nonbiting midges) and Vibrio cholera . FEMS Microbiology Ecology 55, 98–104.Google Scholar
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, 819–827.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, 3549–3560.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of birds through DNA barcodes. PLoS Biol 2, e312.Google Scholar
Hopkin, S.P. (2007) A key to the Collembola (Springtails) of Britain and Ireland. Shrewsbury, UK, FSC Publications.Google Scholar
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, 84–88.Google Scholar
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, 239–244.CrossRefGoogle Scholar
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, 879–885.Google Scholar
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.Google Scholar
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, 421–427.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. Journal of Molecular Evolution 15, 111–120.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, 947–963.Google Scholar
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, 1721–1732.Google Scholar
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, 370–373.Google Scholar
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, 3657–3671.Google Scholar
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, 516–524.Google Scholar
Medeiros, R.J. (2011) The migration strategy, diet and foraging ecology of a small seabird in a changing environment. PhD Thesis, Cardiff University.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 620–628.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 1931–1950.Google Scholar
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, 331–340.Google Scholar
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, 45–49.Google Scholar
Robinson, R.A., Julliard, R. & Saracco, J.F. (2009) Constant effort: studying avian population processes using standardised ringing. Ringing and Migration 24, 199–204.Google Scholar
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, 325–345.Google Scholar
Rosenberg, K.V. & Cooper, R.J. (1990) Approaches to avian diet analysis. pp. 80–90 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.Google Scholar
Rotheray, G.E. (1983) Feeding behaviour of Syrphis ribesii and Melanostoma scalare on Aphis fabae . Entomologia Experimentalis et Applicata 34, 148–154.Google Scholar
Scribner, K.T. & Bowman, T.D. (1998) Microsatellites identify depredated waterfowl remains from glaucous gull stomachs. Molecular Ecology 7, 1401–1405.Google Scholar
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, 4461–4468.Google Scholar
Stubbs, A.E. & Falk, S.J. (2002) British Hoverflies. 2nd edn. Reading, UK, British Entomological and Natural History Society.Google Scholar
Sutherland, R.M. (2000) Molecular analysis of avian diets. PhD Thesis, University of Oxford, UK.Google Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.Google Scholar
Tamura, K., Dudle, J., Nei, M. & Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Thomas, C.F.G., Holland, J.M. & Brown, N.J. (2002) The spatial distribution of carabid beetles in agricultural landscapes. pp. 305–344 in Holland, J.M. (Ed.) The Agroecology of Carabid Beetles. Andover, UK, Intercept.Google Scholar
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, 265–343.CrossRefGoogle Scholar
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, 239–247.Google Scholar
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, 2117–2128.Google Scholar
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