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Detecting aphid predation by earwigs in organic citrus orchards using molecular markers

Published online by Cambridge University Press:  14 March 2012

C. Romeu-Dalmau ,
J. Piñol  and
N. Agustí
C. Romeu-Dalmau*
Affiliation:
Department of Animal Biology, Plant Biology and Ecology, and Centre for Ecological Research and Forestry Applications (CREAF). Universitat Autònoma de Barcelona, Facultat de Biociències, 08193, Bellaterra, Barcelona, Spain
J. Piñol
Affiliation:
Department of Animal Biology, Plant Biology and Ecology, and Centre for Ecological Research and Forestry Applications (CREAF). Universitat Autònoma de Barcelona, Facultat de Biociències, 08193, Bellaterra, Barcelona, Spain
N. Agustí
Affiliation:
IRTA, Entomology, Carretera de Cabrils, Km 2, E-08348 Cabrils, Barcelona, Spain
*
*Author for correspondence Fax: 0034 93 5814151 E-mail: [email protected]
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Abstract

Aphids (Hemiptera: Aphidoidea) can damage citrus trees via direct damage to leaves and flowers or via the indirect transmission of viruses. Predators such as the European earwig, Forficula auricularia Linnaeus (Dermaptera: Forficulidae), may assist in keeping aphid populations under control in citrus orchards. Group-specific primers were developed to detect aphid DNA in earwigs, in order to determine earwig predation rates in aphids in Mediterranean organic citrus trees. These primers were designed in accordance with the alignment of comparable sequences of aphids and earwigs, and they amplified a 224 bp fragment of the mitochondrial cytochrome c oxidase subunit I (COI) region. Following the consumption of three to five Aphis spiraecola Patch, aphid DNA was still detectable in 50% of earwigs one day after the ingestion. When predation was evaluated in the field, aphid DNA was detected in earwigs in May, June and July but not in April and August. The most interesting result is that of May, when aphid abundance was very low but 30% of the earwigs tested positive for aphid DNA. This finding suggests that earwigs are important aphid predators in citrus orchards, as they probably alter aphid dynamics as a result of early seasonal pressure on this pest.

Keywords

DermapteraForficula auriculariaAphis spiraecolaPCRgut-content analysisCOI
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 5 , October 2012 , pp. 566 - 572
Copyright
Copyright © Cambridge University Press 2012

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References

Agustí, N., Shayler, S.P., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003a) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 3467–3495.CrossRefGoogle ScholarPubMed
Agustí, N., Unruh, T.R. & Welter, S.C. (2003b) Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers. Bulletin of Entomological Research 93, 179–185.CrossRefGoogle ScholarPubMed
Albouy, V. & Caussanel, C. (1990) Dermaptères ou Perce-Oreilles. Faune de France, 75. Paris, France, Fédération Française des Sociétés de Sciences Naturelles.Google Scholar
Barbagallo, S., Cocuzza, G., Cravedi, P. & Komazaki, S. (2007) 30-IPM sase Studies: tropical and subtropical fruit trees. p. 663in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Cambridge, UK, CAB International.CrossRefGoogle Scholar
Belliure, B., Pérez, P., Marcos, M.A., Michelena, J.M. & Hermoso de Mendoza, A. (2008) Capítulo 14. Control biológico de pulgones. pp.209–238in Jacas, J.A. & Urbaneja, A. (Eds) Control Biológico de Plagas Agrícolas. Valencia, España, Phytoma-España.Google 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, 1887–1898.CrossRefGoogle ScholarPubMed
De León, J.H., Fournier, V., Hagler, J.R. & Daane, K.M. (2006) Development of molecular diagnostic markers for sharpshooters Homalodisca coagulata and Homalodisca literata for use in predator gut content examinations. Entomologia Experimentalis et Applicata 119, 109–119.CrossRefGoogle Scholar
Díaz, B.M., Legarrea, S., Marcos-García, M.A. & Fereres, A. (2010) The spatio-temporal relationships among aphids, the entomophthoran fungus, Pandora neoaphidis, and aphidophagous hoverflies in outdoor lettuce. Biological Control 53, 304–311.CrossRefGoogle Scholar
Dib, H., Simon, S., Sauphanor, B. & Capowiez, Y. (2010) The role of natural enemies on the population dynamics of the rosy apple aphid, Dysaphis plantaginea Passerini (Hemiptera: Aphididae) in organic apple orchards in south-eastern France. Biological Control 55, 97–109.CrossRefGoogle Scholar
Dixon, A.F.G. (1998) Aphid Ecology: An optimization Approach. 2nd edn, London, UK, Chapman & Hall.Google Scholar
Dixon, A.F.G., Kindlmann, P., Leps, J. & Holman, J. (1987) Why there are so few species of aphids especially in the tropics? The American Naturalist 129, 580–592.CrossRefGoogle Scholar
Ebeling, W. (1959) Subtropical Fruit Pests. Los Angeles, CA, USA, University of California Press.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, 201–209.CrossRefGoogle ScholarPubMed
Hardwood, J.D. & Obrycki, J. (2005) Quantifying aphid predation rates of generalist predators in the field. European Journal of Entomology 102, 335–350.CrossRefGoogle Scholar
Hardwood, 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, 4390–4400.CrossRefGoogle Scholar
Harper, G.L., King, R.A., Dodd, C.S., Hardwood, 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
Hoogendoorn, M. & Heimpel, G.E. (2001) PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Molecular Ecology 10, 2059–2067.CrossRefGoogle ScholarPubMed
Hosseini, R., Schmidt, O. & Keller, M.A. (2008) Factors affecting detectability of prey DNA in the gut contents of invertebrate predators: a polymerase chain reaction-based method. Entomologia Experimentalis et Applicata 126, 194–202.CrossRefGoogle Scholar
Innis, M.A. & Gelfand, D.H. (1990) Optimization of PCRs. pp. 3–12in Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds) PCR Protocols. San Diego, CA, USA, Academic Press.Google Scholar
Irwin, M.E., Kampmeier, G.E. & Weisser, W.W. (2007) 7-Aphid movement: process and consequences. p. 172in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Cambridge, UK, CAB International.CrossRefGoogle Scholar
Juen, A. & Traugott, M. (2007) Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Molecular Ecology 16, 1545–1557.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
King, R.A., Moreno-Ripoll, R., Agustí, N., Shayler, S.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2011) Multiplex reactions for the molecular detection of predation on pest and nonpest invertebrates in agroecosystems. Molecular Ecology Resources 11, 370–373.CrossRefGoogle ScholarPubMed
Kuusk, A.-K. & Agustí, N. (2008) Group-specific primers for DNA-based detection of springtails (Hexapoda: Collembola) within predator gut contents. Molecular Ecology Resources 8, 678–681.CrossRefGoogle ScholarPubMed
Kuusk, A.-K. & Ekbom, B. (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biological Control 55, 20–26.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, 718–725.CrossRefGoogle Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Ma, J., Li, D., Keller, M., Schmidt, O. & Feng, X. (2005) A DNA marker to identify predation of Plutella xylostella (Lep., Plutellidae) by Nabis kinbergii (Hem., Nabidae) and Lycosa sp. (Araneae, Lycosidae). Journal of Applied Entomology 129, 330–335.CrossRefGoogle Scholar
Monzó, C., Sabater Muñoz, B., Urbaneja, A. & Castañera, P. (2010) Tracking medfly predation by the wolf spider, Pardosa cribata Simon, in citrus orchards using PCR-based gut-content analysis. Bulletin of Entomological Research 100, 145–152.CrossRefGoogle ScholarPubMed
Moreno, P., Ambros, S., Albiach-Martí, M.R., Guerri, J. & Pena, L. (2008) Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology 9, 251–268.CrossRefGoogle ScholarPubMed
Moreno-Ripoll, R., Gabarra, R., Symondson, W.O.C., King, R.A. & Agustí, N.Trophic relationships between predators, whiteflies and their parasitoids in tomato greenhouses: a molecular approach. Bulletin of Entomological Research, in press (doi: 10.1017/S0007485311000836).Google Scholar
Mueller, T.F., Blommers, L.H.M. & Mols, P.J.M. (1988) Earwig (Forficula auricularia) predation on the woolly apple aphid, Eriosoma lanigerum. Entomologia Experimentalis et Applicata 47, 145–152.CrossRefGoogle Scholar
Nicholas, A.H., Spooner-Hart, R.N. & Vickers, R.A. (2005) Abundance and natural control of the woolly aphid Eriosoma lanigerum in an Australian apple orchard IPM program. BioControl 50, 271–291.CrossRefGoogle Scholar
Pineda, A., Morales, M.A., Marcos-García, L. & Fereres, A. (2007) Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues. Biological Control 42, 274–280.CrossRefGoogle Scholar
Piñol, J., Espadaler, X., Cañellas, N. & Pérez, N. (2009a) Effects of the concurrent exclusion of ants and earwigs on aphid abundance in an organic citrus grove. BioControl 54, 515–527.CrossRefGoogle Scholar
Piñol, J., Espadaler, X., Pérez, N. & Beven, K. (2009b) Testing a new model of aphid abundance with sedentary and non-sedentary predators. Ecological Modelling 220, 2469–2480.CrossRefGoogle Scholar
Read, D.S., Sheppard, S.K., Bruford, M.W., Glen, D.M. & Symondson, W.O.C. (2006) Molecular detection of predation by soil micro-arthropods on nematodes. Molecular Ecology 15, 1963–1972.CrossRefGoogle ScholarPubMed
Reinink, K. & Dieleman, F.L. (1993) Survey of aphid species on lettuce. Bulletin of IOBC/WPRS 16, 56–68.Google Scholar
Romeu-Dalmau, C., Espadaler, X. & Piñol, J.Abundance, interannual variation and potential pest predator role of two co-occurring earwig species in citrus canopies. Journal of Applied Entomology, in press (doi: 10.1111/j.1439-0418.2011.01671.x).Google Scholar
Saiki, R.K. (1990) Amplification of genomic DNA. pp. 13–20in Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds) PCR Protocols. San Diego, CA, USA, Academic Press.Google Scholar
Sheppard, S.K., Bell, J., 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, 4461–4468.CrossRefGoogle ScholarPubMed
Solomon, M.G., Cross, J.V., Fitzgerald, J.D., Campbell, C.A.M., Jolly, R.L., Olszak, R.W., Niemczyk, E. & Vogt, H. (2000) Biocontrol of pests of apples and pears in northern and central Europe - 3. Predators. Biocontrol Science and Technology 10, 91–128.CrossRefGoogle Scholar
Suckling, D.M., Burnip, G.M., Hackett, J.K. & Daly, J.M. (2006) Frass sampling and baiting indicate European earwig (Forficula auricularia) foraging in orchards. Journal of Applied Entomology 130, 263–267.CrossRefGoogle Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.CrossRefGoogle ScholarPubMed
Urbaneja, A., Jacas, J.A. & Garcia-Marí, F. (2008) Capítulo 21. Control biológico en cítricos. pp. 335–348in Jacas, J.A. & Urbaneja, A. (Eds) Control Biológico de Plagas Agrícolas. Valencia, España, Phytoma-España.Google Scholar
von Berg, K., Traugott, M., Symondson, W.O.C. & Scheu, S. (2008) The effects of temperature on detection of prey DNA in two species of carabid beetle. Bulletin of Entomological Research 98, 263–269.CrossRefGoogle ScholarPubMed
Zhang, G.-F., Lü, Z.-C. & Wan, F.-H. (2007) Detection of Bemisia tabaci remains in predator guts using a sequence-characterized amplified region marker. Entomologia Experimentalis et Applicata 123, 81–90.CrossRefGoogle Scholar