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

Bulletin of Entomological Research

Volumn 102, Issue 5, 2012, Pages 566-572

  Romeu Dalmau, C ^a   Pinol J ^a   Agusti N ^b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b IRTA   (Spain)

Author keywords

Aphis spiraecola; COI; Dermaptera; Forficula auricularia; gut content analysis; PCR

Indexed keywords

APHID; DISEASE TRANSMISSION; FRUIT; INTEGRATED PEST MANAGEMENT; MOLECULAR ANALYSIS; ORCHARD; PEST DAMAGE; POLYMERASE CHAIN REACTION; VIRAL DISEASE;

APHIDIDAE; APHIDOIDEA; APHIS; APHIS SPIRAECOLA; AURICULARIA; CITRUS; DERMAPTERA; FORFICULA AURICULARIA; FORFICULIDAE; HEMIPTERA;

BIOLOGICAL MARKER; CYTOCHROME C OXIDASE; INSECT PROTEIN;

ANIMAL; APHID; BIOLOGICAL PEST CONTROL; CITRUS; FEMALE; FOOD CHAIN; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT; MALE; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; APHIDS; BIOLOGICAL MARKERS; CITRUS; ELECTRON TRANSPORT COMPLEX IV; FEMALE; FOOD CHAIN; INSECT PROTEINS; INSECTS; MALE; PEST CONTROL, BIOLOGICAL; POLYMERASE CHAIN REACTION;

EID: 84872043991     PISSN: 00074853     EISSN: 14752670     Source Type: Journal    
DOI: 10.1017/S0007485312000132     Document Type: Article

References (47)

1. 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.
2. 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.
3. Albouy, V. & Caussanel, C. (1990) Dermaptères ou Perce-Oreilles. Faune de France, 75. Paris, France, Fédération Française des Sociétés de Sciences Naturelles.
4. Barbagallo, S., Cocuzza, G., Cravedi, P. & Komazaki, S. (2007) 30-IPM sase Studies: tropical and subtropical fruit trees. p. 663 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Cambridge, UK, CAB International.
5. Belliure, B., Pérez, P., Marcos, M.A., Michelena, J.M. & Hermoso de Mendoza, A. (2008) Capítulo 14. Control biológico de pulgones. pp.209-238 in Jacas, J.A. & Urbaneja, A. (Eds) Control Biológico de Plagas Agrícolas. Valencia, España, Phytoma-España.
6. 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.
7. De León, J.H., Fournier, V., Hagler, J.R. & Daane, K.M. (2006) Development of molecular diagnostic markers for sharp-shooters Homalodisca coagulata and Homalodisca literata for use in predator gut content examinations. Entomologia Experimentalis et Applicata 119, 109-119.
8. Díaz, B.M., Legarrea, S., Marcos-García, M.A. & Fereres, A. (2010) The spatio-temporal relationships among aphids, the entomophthoran fungus, Pandora neoaphidis, and aphido-phagous hoverflies in outdoor lettuce. Biological Control 53, 304-311.
9. 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.
10. Dixon, A.F.G. (1998) Aphid Ecology: An optimization Approach. 2nd edn, London, UK, Chapman & Hall.
11. 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.
12. Ebeling, W. (1959) Subtropical Fruit Pests. Los Angeles, CA, USA, University of California Press.
13. 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.
14. Hardwood, J.D. & Obrycki, J. (2005) Quantifying aphid predation rates of generalist predators in the field. European Journal of Entomology 102,335-350.
15. 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 pre-dation by Orius insidiosus: a molecular approach. Molecular Ecology 16,4390M400.
16. 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.
17. 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.
18. 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.
19. Innis, M.A. & Gelfand, D.H. (1990) Optimization of PCRs. pp. 3-12 in Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds) PCR Protocols. San Diego, CA, USA, Academic Press.
20. Irwin, M.E., Kampmeier, G.E. & Weisser, W.W. (2007) 7-Aphid movement: process and consequences. p. 172 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Cambridge, UK, CAB International.
21. Juen, A. & Traugott, M. (2007) Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Molecular Ecology 16,1545-1557.
22. 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.
23. 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.
24. 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.
25. Kuusk, A.-K. & Ekbom, B. (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological con-trol. Biological Control 55, 20-26.
26. Kuusk, A.-K., Cassel-Lundhagen, A., Kvarnheden, A. & Ekbom, B. (2008) Tracking aphid predation by lycosid spi-ders in spring-sown cereals using PCR-based gut-content analysis. Basic and Applied Ecology 9, 718-725.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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).
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. Reinink, K. & Dieleman, F.L. (1993) Survey of aphid species on lettuce. Bulletin ofIOBC/WPRS 16, 56-68.
39. Romeu-Dalmau, C., Espadaler, X. & Piñol, J. Abundance, inter-annual 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).
40. Saiki, R.K. (1990) Amplification of genomic DNA. pp. 13-20 in Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds) PCR Protocols. San Diego, CA, USA, Academic Press.
41. 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.
42. 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 cen-tral Europe-3. Predators. Biocontrol Science and Technology 10, 91-128.
43. 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.
44. Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627-641.
45. Urbaneja, A., Jacas, J.A. & Garcia-Marí, F. (2008) Capítulo 21. Control biológico en cítricos. pp. 335-348 in Jacas, J.A. & Urbaneja, A. (Eds) Control Biológico de Plagas Agrícolas. Valencia, España, Phytoma-España.
46. 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.
47. 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.