Predation by generalist predators on the codling moth versus a closely-related emerging pest the oriental fruit moth: A molecular analysis

Agricultural and Forest Entomology

Volumn 14, Issue 3, 2012, Pages 260-269

  Boreau de Roincé, Catherine ^b,c   Lavigne, Claire ^b   Ricard, Jean Michel ^a   Franck, Pierre ^b   Bouvier, Jean Charles ^b   Garcin, Alain ^a   Symondson, William O C ^c  

^a Centre de Balandran   (France)

^b Domaine Saint Paul   (France)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Apple orchard; Biological control; Carabidae; Diagnostic PCR; Generalist predators; Spider; Tortricidae

Indexed keywords

ARANEAE; CARABIDAE; COLEOPTERA; CYDIA POMONELLA; GRAPHOLITA MOLESTA; LEPIDOPTERA; MALUS X DOMESTICA; TORTRICIDAE;

EID: 84863779174     PISSN: 14619555     EISSN: 14619563     Source Type: Journal    
DOI: 10.1111/j.1461-9563.2011.00564.x     Document Type: Article

References (66)

1. Agusti, 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.
2. Altieri, M.A. (1999) The ecological role of biodiversity in agroecosystems. Agriculture Ecosystems & Environment, 74, 19-31.
3. Barnes, M.M. (1991) Codling moth occurrence, host race formation, and damage. Tortricid Pests, their Biology, Natural Enemies and Control (ed. by L. P. S. van der Geest and H. H. Evenhuis ), pp. 313-327. Elsevier, The Netherlands.
4. Causse, R. (1976) Etude de la localisation et de la mortalité hivernale des larves de Laspeyresia pomonella L. (Lepidoptera, Tortricidae) en vergers modernes de pommiers de la basse vallée du Rhone. Annales de Zoologie et Ecologie Animale, 8, 83-101.
5. Chang, G.C. & Kareiva, P. (1999) The case for indigenous generalists in biological control. Theoretical Approaches to Biological Control (ed. by B. Hawkins and H. Cornell ), pp. 103-115. Cambridge University Press, U.K.
6. Cornic, J.F. (1978) Etude du régime alimentaire de trois espèces de carabiques et de ses variations en verger de pommiers. Annales de la Société Entomologique de France, 9, 69-87.
7. Davey, J.S. (2010) Intraguild predation among generalist predators in winter wheat. PhD thesis, Cardiff University.
8. Denholm, I., Devine, G.J. & Williamson, M.S. (2002) Evolutionary genetics-insecticide resistance on the move. Science, 297, 2222-2223.
9. Eitzinger, B. & Traugott, M. (2011) Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis. Journal of Applied Ecology, 48, 591-599.
10. Epstein, D.L., Zack, R.S., Brunner, J.F., Gut, L. & Brown, J.J. (2001) Ground beetle activity in apple orchards under reduced pesticide management regimes. Biological Control, 21, 97-104.
11. Eskelson, M.J., Chapman, E.G., Archbold, D.D., Obrycki, J.J. & Harwood, J.D. (2011) Molecular identification of predation by carabid beetles on exotic and native slugs in a strawberry agroecosystem. Biological Control, 56, 245-253.
12. Finke, D.L. & Snyder, W.E. (2010) Conserving the benefits of predator biodiversity. Biological Conservation, 143, 2260-2269.
13. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294-299.
14. Foltan, P., Sheppard, S., Konvicka, M. & Symondson, W.O.C. (2005) The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Molecular Ecology, 14, 4147-4158.
15. Franck, P., Guerin, B., Loiseau, A. & Sauphanor, B. (2005) Isolation and characterization of microsatellite loci in the codling moth Cydia pomonella L. (Lepidoptera, Tortricidae). Molecular Ecology Notes, 5, 99-102.
16. Franck, P., Reyes, M., Olivares, J. & Sauphanor, B. (2007) Genetic architecture in codling moth populations: comparison between microsatellite and insecticide resistance markers. Molecular Ecology, 16, 3554-3564.
17. Garcin, A., Demarle, O. & Soldati, F. (2004) Les carabes, indicateurs de biodiversité et auxiliaires généralistes. Ctifl-Infos, 199, 42-47.
18. Garcin, A., Darthout, L. & Lochard, G. (2008) Les carabes en verger de pommier : des auxiliaires à préserver. Ctifl-Infos, 244, 31-35.
19. Glen, D.M. (1977) Predation of codling moth eggs, Cydia pomonella, predators responsible and their alternatie prey. Journal of Applied Ecology, 14, 445-456.
20. Greenstone, M.H., Szendrei, Z., Payton, M.E., Rowley, D.L., Coudron, T.C. & Weber, D.C. (2010) Choosing natural enemies for conservation biological control: use of the prey detectability half-life to rank key predators of Colorado potato beetle. Entomologia Experimentalis et Applicata, 136, 97-107.
21. Hackermann, J., Rott, A.S. & Dorn, S. (2008) Consequences of mixed species infestation on the searching behavior and parasitism success of a larval parasitoid. Biocontrol, 53, 725-736.
22. Hagley, E.A.C. & Allen, W.R. (1988) Ground beetles (Coleoptera: Carabidae) as predators of the codling moth, Cydia pomonella (L) (Lepidoptera: tortricidae). Canadian Entomologist, 120, 917-925.
23. 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.
24. Harwood, 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.
25. Ingerson-Mahar, J. (2002) Relating diet and morphology in adult carabid beetles. The Agroecology of Carabid Beetles (ed. by J. Holland ), pp. 111-136. Intercept, U.K.
26. Ivaldi-Sender, C. (1974) A simple technique for the permanent rearing of the oriental fruit moth, Grapholita molesta (Lepidoptera Tortricidae) on an artificial medium. Techniques simples pour un elevage permanent de la tordeuse orientale, Grapholita molesta (Lepidoptera Tortricidae) sur milieu artificiel. Annales de Zoologie, Ecologie Animale, 6, 337-343.
27. Jeannel, R. (1941) Coléoptères carabiques. Faune de France, Vol. 39-40. Librairie de la Faculté des Sciences, France.
28. Jumean, Z., Jones, E. & Gries, G. (2009) Does aggregation behavior of codling moth larvae, Cydia pomonella, increase the risk of parasitism by Mastrus ridibundus? Biological Control, 49, 254-258.
29. 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.
30. King, R.A., Vaughan, I.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010) Prey choice by carabid beetles feeding on an earthworm community analysed using species- and lineage-specific PCR primers. Molecular Ecology, 19, 1721-1732.
31. Knight, A.L. & Light, D.M. (2005) Seasonal flight patterns of codling moth (Lepidoptera : Tortricidae) monitored with pear ester and codlemone-baited traps in sex pheromone-treated apple orchards. Environmental Entomology, 34, 1028-1035.
32. Koss, A.M. & Snyder, W.E. (2005) Alternative prey disrupt biocontrol by a guild of generalist predators. Biological Control, 32, 243-251.
33. Krebs, J.R., Wilson, J.D., Bradbury, R.B. & Siriwardena, G.M. (1999) The second silent spring? Nature, 400, 611-612.
34. Kuusk, A.K. & Ekbom, B. (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biological Control, 55, 20-26.
35. Landis, D.A., Wratten, S.D. & Gurr, G.M. (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, 45, 175-201.
36. Landry, B., Powell, J.A. & Sperling, F.A.H. (1999) Systematics of the Argyrotaenia franciscana (Lepidoptera : Tortricidae) species group: evidence from mitochondrial DNA. Annals of the Entomological Society of America, 92, 40-46.
37. Letourneau, D.K. & Bothwell, S.G. (2008) Comparison of organic and conventional farms: challenging ecologists to make biodiversity functional. Frontiers in Ecology and the Environment, 6, 430-438.
38. Lloyd, D.C. (1960) Significance of the type of host plant crop in successful biological control of insect pests. Nature, 187, 430-431.
39. Loreau, M., Naeem, S., Inchausti, P. et al. (2001) Ecology-biodiversity and ecosystem functioning: current knowledge and future challenges. Science, 294, 804-808.
40. Lovei, G.L. & Sunderland, K.D. (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology, 41, 231-256.
41. Mills, N. (2005) Selecting effective parasitoids for biological control introductions: codling moth as a case study. Biological Control, 34, 274-282.
42. Minarro, M., Espadaler, X., Melero, V.X. & Suarez-Alvarez, V. (2009) Organic versus conventional management in an apple orchard: effects of fertilization and tree-row management on ground-dwelling predaceous arthropods. Agricultural and Forest Entomology, 11, 133-142.
43. Mols, C.M.M., van Noordwijk, A.J. & Visser, M.E. (2005) Assessing the reduction of caterpillar numbers by great tits Parus major breeding in apple orchards. Ardea, 93, 259-269.
44. Mols, C.M.M. & Visser, M.E. (2002) Great tits can reduce caterpillar damage in apple orchards. Journal of Applied Ecology, 39, 888-899.
45. Mols, C.M.M. & Visser, M.E. (2007) Great tits (Parus major) reduce caterpillar damage in commercial apple orchards. PLoS ONE, 2, 3.
46. Monzo, C., Sabater-Munoz, B., Urbaneja, A. & Castanera, P. (2011) The ground beetle Pseudophonus rufipes revealed as predator of Ceratitis capitata in citrus orchards. Biological Control, 56, 17-21.
47. Navaneethan, T., Strauch, O., Besse, S., Bonhomme, A. & Ehlers, R.U. (2010) Influence of humidity and a surfactant-polymer-formulation on the control potential of the entomopathogenic nematode Steinernema feltiae against diapausing codling moth larvae (Cydia pomonella L.) (Lepidoptera: Tortricidae). Biocontrol, 55, 777-788.
48. Pfiffner, L., Luka, H., Schlatter, C., Juen, A. & Traugott, M. (2009) Impact of wildflower strips on biological control of cabbage lepidopterans. Agriculture Ecosystems & Environment, 129, 310-314.
49. Poltronieri, A.S., Borges Da Silva, E.D., Silva Araujo, E., Schuber, J.M. & Pastori, P.L. (2008) Biological characteristics of two strains of Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) of the oriental fruit moth eggs of different ages. Caracteristicas biologicas de duas linhagens de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) em ovos da mariposa-oriental com diferentes idades. Boletin de Sanidad Vegetal, Plagas, 34, 349-356.
50. Prasad, R.P. & Snyder, W.E. (2006) Polyphagy complicates conservation biological control that targets generalist predators. Journal of Applied Ecology, 43, 343-352.
51. Pruess-Ustuen, A., Vickers, C., Haefliger, P. & Bertollini, R. (2011) Knowns and unknowns on burden of disease due to chemicals: a systematic review. Environmental Health, 10, 9.
52. R Development Core Team (2011) R Foundation for Statistical Computing. R Development Core Team, Austria. [WWW document]. URL [accessed on 9 September 2011].
53. Reyes, M., Franck, P., Olivares, J., Margaritopoulos, J., Knight, A. & Sauphanor, B. (2009) Worldwide variability of insecticide resistance mechanisms in the codling moth, Cydia pomonella L. (Lepidoptera: Tortricidae). Bulletin of Entomological Research, 99, 359-369.
54. Riddick, E.W. & Mills, N.J. (1994) Potential of adult carabids (Coleoptera: Carabidae) as predators on 5th instar codling moth (Lepidoptera: Tortricidae) in apple orchards in California. Environmental Entomology, 23, 1338-1345.
55. Riga, E., Lacey, L.A., Guerra, N. & Headrick, H.L. (2006) Control of the oriental fruit moth, Grapholita molesta, using entomopathogenic nematodes in laboratory and fruit bin assays. Journal of nematology, 38, 168-171.
56. Roberts, M.J. (1996) Spiders of Britain and Nothern Europe. HarperCollins, U.K.
57. Rothschild, G.H.L. & Vickers, R.A. (1991) Biology, ecology and control of the oriental fruit moth. Tortricid Pests, Their Biology, Natural Enemies and Control (ed. by L. P. S. Van der Geest and H. H. Evenhuis ), pp. 389-412. Elsevier Science Publishers, The Netherlands.
58. Rozen, S. & Skaletsky, H. (2003) Primer 3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology (ed. by S. Krawetz and S. Misener ), pp. 364-386. Humana Press, Totowa, New Jersey.
59. Solomon, M.E. & Glen, D.M. (1979) Prey density and rates of predation by tits (Parus spp) on larvae of codling moth (Cydia pomonella) under bark. Journal of Applied Ecology, 16, 49-59.
60. Straub, C.S. & Snyder, W.E. (2006) Species identity dominates the relationship between predator biodiversity and herbivore suppression. Ecology, 87, 277-282.
61. Straub, C.S., Finke, D.L. & Snyder, W.E. (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biological Control, 45, 225-237.
62. Sunderland, K.D., Powell, W. & Symondson, W.C. (2005) Populations and communities. Insects as Natural Enemies: A Practical Perspective (ed. by M. A. Jervis ), pp. 299-434. Springer, Germany.
63. Symondson, W.O.C., Glen, D.M., Erickson, M.L., Liddell, J.E. & Langdon, C.J. (2000) Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera : Carabidae) within crops? Investigations using monoclonal antibodies. Molecular Ecology, 9, 1279-1292.
64. Symondson, W.O.C., Sunderland, K.D. & Greenstone, M.H. (2002) Can generalist predators be effective biocontrol agents? Annual Review of Entomology, 47, 561-594.
65. Symondson, W.O.C., Cesarini, S., Dodd, P.W. et al. (2006) Biodiversity vs. biocontrol: positive and negative effects of alternative prey on control of slugs by carabid beetles. Bulletin of Entomological Research, 96, 637-645.
66. Szendrei, Z., Greenstone, M.H., Payton, M.E. & Weber, D.C. (2009) Molecular gut-content analysis of a predator assemblage reveals the effect of habitat manipulation on biological control in the field. Basic and Applied Ecology, 11, 153-161.