A multi-approach study to delineate interactions between carabid beetles and soybean aphids

Environmental Entomology

Volumn 42, Issue 1, 2013, Pages 89-96

  Firlej, Annabelle ^a   Doyon, Josée ^a   Harwood, James D ^b   Brodeur, Jacques ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Aphis glycines; field cage study; molecular gut content analysis; Pterostichus melanarius; soybean

Indexed keywords

PRIMER DNA;

APHID; BEETLE; CROP DAMAGE; CROP PEST; GROWING SEASON; MOLECULAR ANALYSIS; NATURAL ENEMY; PREDATION; PREDATOR; SOYBEAN;

ANIMAL; APHID; ARTICLE; BEETLE; BIOLOGICAL PEST CONTROL; CHEMISTRY; FEMALE; HERBIVORY; MALE; PREDATION; SOYBEAN; STANDARD; STOMACH JUICE;

ANIMALS; APHIDS; BEETLES; DNA PRIMERS; FEMALE; GASTROINTESTINAL CONTENTS; HERBIVORY; MALE; PEST CONTROL, BIOLOGICAL; PREDATORY BEHAVIOR; SOYBEANS;

NORTH AMERICA;

EID: 84873554723     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN11303     Document Type: Article

References (57)

1. Behura, S. K. 2006. Molecular marker systems in insects: current trends and future avenues. Mol. Ecol. 15: 3087-3113. (Pubitemid 44379720)
2. Bender, W., P. Spierer, D. S. Hogness, and P. Chambon. 1983. Chromosomal walking and jumping to isolate DNA from the Ace and Rosy loci and the bithorax complex in Drosophila melanogaster. J. Mol. Biol. 168: 17-33.
3. Bilde, T., and S. Toft. 1994. Prey preference and egg production of the carabid beetle Agonum dorsale. Entomol. Exp. Appl. 73: 151-156.
4. Bilde, T., and S. Toft. 1997. Consumption by carabid beetles of three cereal aphids species relative to other prey types. Entomophaga 42: 21-32. (Pubitemid 127760808)
5. Bommarco, R., S. O. Firle, and B. Ekbom. 2007. Outbreak suppression by predators depends on spatial distribution of prey. Ecol. Modell. 201: 163-170. (Pubitemid 46108249)
6. Breault, J., B. Duval, G. Labrie, F. Meloche, C. Parent, and A. Rondeau. 2011. Stratégie d'intervention recommandée au Québec contre le puceron du soya en 2011. Bulletin d'information 10: 1-5.
7. Chiverton, P. A. 1987. Predation of Rhopalosiphum padi (Homoptera: Aphididae) by polyphagous predatory arthropods during the aphids' pre-peak period in spring barley. Ann. Appl. Biol. 111: 257-269.
8. Edwards, C. A., K. D. Sunderland, and K. S. George. 1979. Studies on polyphagous predators of cereal aphids. J. Appl. Ecol. 16: 811-823.
9. Eitzinger, B., and M. Traugott. 2011. Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis. J. Appl. Ecol. 48: 591-599.
10. Eskelson, M. J., E. G. Chapman, D. D. Archbold, J. J. Obrycki, and J. D. Harwood. 2011. Molecular identification of predation by carabid beetles on exotic and native slugs in a strawberry agroecosystem. Biol. Control 56: 245-253.
11. Firlej, A., A.-É. Gagnon, S. Laurin-Lemay, and J. Brodeur. 2012. Diversity and seasonal abundance of carabid beetles in the soybean crop in Québec, Canada. Can. Ento-mol. 144: 542-554.
12. Fleming, R. A. 1980. The potential control of cereal rust by natural enemies. Theor. Popul. Biol. 18: 374-395.
13. Griffiths, G.J.K., C. J. Alexander, J. M. Holland, P. J. Kennedy, J. N. Perry, and W.O.C. Symondson. 2008. Monoclonal antibodies reveal changes in predator efficiency with prey spatial pattern. Mol. Ecol. 17: 1828-1839. (Pubitemid 351441707)
14. Hajek, A. E., J. J. Hannam, C. Nielsen, A. J. Bell, and J. K. Liebherr. 2007. Distribution and abundance of carabi-dae (Coleoptera) associated with soybean aphid (Hemiptera: Aphididae) populations in central New York. Ann. Entomol. Soc. Am. 100: 876-886. (Pubitemid 350226051)
15. Harper, G. L., R. A. King, C. S. Dodd, J. D. Harwood, D. M. Glen, M. W. Bruford, and W.O.C. Symondson. 2005. Rapid screening of invertebrate predators for multiple prey DNA targets. Mol. Ecol. 14: 819-827. (Pubitemid 40346473)
16. Harwood, J. D., and M. H. Greenstone. 2008. Molecular diagnosis of natural enemy-host interactions, pp. 41-57. In N. Liu (ed.), Recent advances in insect physiology, toxicology and molecular biology. Research Signpost, Kerala, India.
17. Harwood, J. D., N. Desneux, H.Y.S. Yoo, D. L. Rowley, M. H. Greenstone, J. J. Obrycki, and R. J. O'Neil. 2007. Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol. Ecol. 16: 4390-4400. (Pubitemid 47511218)
18. Harwood, J. D., S. W. Phillips, J. Lello, K. D. Sunderland, D. M. Glen, M. W. Bruford, G. L. Harper, and W.O.C. Symondson. 2009a. Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops. Biol. Control 51: 499-506.
19. Harwood, J. D., H.J.S. Yoo, M. H. Greenstone, D. L. Rowley, and R. J. O'Neil. 2009b. Differential impact of adults and nymphs of a generalist predator on an exotic invasive pest demonstrated by molecular gut-content analysis. Biol. Invasions 11: 895-903.
20. Holland, J. M., S. R. Thomas, and A. Hewitt. 1996. Some effects of polyphagous predators on an outbreak of cereal aphid (Sitobion avenae F.) and orange wheat blossom midge (Sitodoplosis mosellana Gehin). Agric. Ecosyst. Environ. 59: 181-190.
21. Holland, J. M., and S. R. Thomas. 1997. Assessing the role of beneficial invertebrates in conventional and integrated farming systems during an outbreak of Sitobion avenae. Biol. Agric. Hortic. 15: 73-82. (Pubitemid 28390838)
22. Ishijima, C., A. Taguchi, M. Takagi, T. Motobayashi, M. Nakai, and Y. Kunimi. 2006. Observational evidence that the diet of wolf spiders (Araneae: Lycosidae) in paddies temporarily depends on dipterous insects. Appl. Entomol. Ecol. 41: 195-200. (Pubitemid 43854504)
23. Juen, A., and M. Traugott. 2007. Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Mol. Ecol. 16: 1545-1557. (Pubitemid 46474769)
24. Kielty, J. P., L. J. Allen-Williams, and N. Underwood. 1999. Prey preferences of six species of Carabidae (Co-leoptera) and one Lycosidae (Araneae) commonly found in UK arable crop fields. J. Appl. Entomol. 123: 193-200. (Pubitemid 29250453)
25. King, R. A., D. S. Read, M. Traugott, and W.O.C. Symondson. 2008. Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol. Ecol. 17: 947-963. (Pubitemid 351197358)
26. King, R. A., I. P. Vaughan, J. R. Bell, D. A. Bohan, and W.O.C. Symondson. 2010. Prey choice by carabid beetles feeding on an earthworm community analysed using speciesand lineage-specific PCR primers. Mol. Ecol. 19: 1721-1732.
27. Kromp, B. 1999. Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agric. Ecosys. Environ. 74: 187-228. (Pubitemid 29384420)
28. Landis, D. A., and W. van der Werf. 1997. Early-season predation impacts the establishment of aphids and spread of beet yellows virus in sugar beet. Entomophaga 42: 499-516. (Pubitemid 127760860)
29. Lang, A., J. Filser, and J. R. Henschel. 1999. Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop. Agric. Ecosys. Environ. 72: 189-199. (Pubitemid 29087658)
30. Lang, A., and S. Gsödl. 2001. Prey vulnerability and active predator choice as determinants of prey selection: a cara-bid beetle and its aphid prey. J. Appl. Entomol. 125: 53-61. (Pubitemid 32265358)
31. Lang, A. 2003. Intraguild interference and biological control effects of generalist predators in a winter wheat field. Oecologia 134: 144-153. (Pubitemid 36174808)
32. Larochelle, A. 1990. The food of the carabid beetles (Co-leoptera: Carabidae, including Cicindelinae). Fabreries, Supplément 5: 1-132.
33. Lindroth, C. H. 1992. Ground beetles (Carabidae) of Fen-noscandia. A zoogeographic study Part III, Smithsonian Institution Libraries and National Science Foundation, Washington, DC.
34. Lundgren, J. G. 2009. Relationships of natural enemies and non-prey foods. Springer, Dordrecht, The Netherlands.
35. Lundgren, J. G., M. E. Ellsbury, and D. A. Prischmann. 2009. Analysis of the predator community of a subterranean herbivorous insect based on polymerase chain reaction. Ecol. Appl. 19: 2157-2166.
36. Lys, J.-A., and W. Nentwig. 1991. Surface activity of carabid beetles inhabiting cereal fields. Pedobiologia 35: 129-138.
37. Madsen, M., S. Terkildsen, and S. Toft. 2004. Microcosm studies on control of aphids by generalist arthropod predators: effects of alternative preys. Biocontrol 49: 483-504. (Pubitemid 39067243)
38. Mundy, C. A., L. J. Allen-Williams, N. Underwood, and S. Warrington. 2000. Prey selection and foraging behaviour by Pterostichus cupreus L. (Col., Carabidae) under laboratory conditions. J. Appl. Entomol. 124: 349-358. (Pubitemid 32122195)
39. Ö stman, Ö., B. Ekbom, and J. Bengtsson. 2003 Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecol. Econ. 45: 149-158. (Pubitemid 36551357)
40. Ragsdale, D. W., D. A. Landis, J. Brodeur, G. E. Heimpel, and N. Desneux. 2011. Ecology and management of the soybean aphid in North America. Annu. Rev. Entomol. 56: 375-399.
41. Rhainds, M., J. Brodeur, D. Borcard, and P. Legendre. 2008. Toward management guidelines for soybean aphid, Aphis glycines, in Quebec. II. Spatial distribution of aphid populations in commercial soybean fields. Can. Entomol. 140: 219-234. (Pubitemid 351613500)
42. Rutledge, C. E., R. J. O'Neil, T. B. Fox, and D. A. Landis. 2004. Soybean aphid predators and their use in integrated pest management. Ann. Entomol. Soc. Am. 97: 240-248. (Pubitemid 38546781)
43. Rutledge, C. E., and R. J. O'Neil. 2005. Orius insidiosus (Say) as a predator of the soybean aphid, Aphis glycines Matsumura. Biol. Control 33: 56-64. (Pubitemid 40359153)
44. Settle, W. H., H. Ariawan, E. T. Astuti, W. Cahyana, A. L. Hakim, D. Hindayana, A. S. Lestari, and P. Sartanto. 1996. Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77: 1975-1988.
45. Sheppard, S. K., and J. D. Harwood. 2005. Advances in molecular ecology: tracking trophic links through predator-prey food webs. Funct. Ecol. 19: 751-762. (Pubitemid 44933499)
46. Snyder, W. E., S. B. Joseph, R. F. Preziosi, and A. J. Moore. 2000. Nutritional benefits of cannibalism for the lady beetle Harmonia axyridis (Coleoptera: Coccinellidae) when prey quality is poor. Environ. Entomol. 29: 1173-1179. (Pubitemid 32100196)
47. Sunderland, K. D., and G. P. Vickerman. 1980. Aphid feeding by some polyphagous predators in relation to aphid density in cereal fields. J. Appl. Ecol. 17: 389-396.
48. Sunderland, K. D., N. E. Crook, D. L. Stacey, and B. J. Fuller. 1987. A study of feeding by polyphagous predators on cereal aphids using elisa and gut dissection. J. Appl. Ecol. 24: 907-933.
49. Symondson, W.O.C. 2002. Molecular identification of prey in predator diets. Mol. Ecol. 11: 627-641. (Pubitemid 34443719)
50. Symondson, W.O.C., K. D. Sunderland, and M. H. Greenstone. 2002. Can generalist predators be effective bio-control agents? Annu. Rev. Entomol. 47: 561-594. (Pubitemid 34108591)
51. Szendrei, Z., M. H. Greenstone, M. E. Payton, and D. C. Weber. 2010. Molecular gut-content analysis of a predator assemblage reveals the effect of habitat manipulation on biological control in the field. Basic Appl. Ecol. 11: 153-161.
52. Thomas, C.F.G., L. Parkinson, and E.J.P. Marshal. 1998. Isolating the components of activity-density for the carabid beetle Pterostichus melanarius in farmland. Oecologia 116: 103-112. (Pubitemid 28398093)
53. Toft, S. 2005. The quality of aphids as food for generalist predators: implications for natural control of aphids. Eur. J. Entomol. 102: 371-383. (Pubitemid 41213925)
54. Venette, R. C., and D. W. Ragsdale. 2004. Assessing the invasion by the soybean aphid (Homoptera: Aphididae): where will it end? Ann. Entomol. Soc. Am. 97: 219-226. (Pubitemid 38546777)
55. Wallin, H., and B. S. Ekbom. 1988. Movements of carabid beetles (Coleoptera: Carabidae) inhabiting cereal fields: a field tracing study. Oecologia 77: 39-43. (Pubitemid 20422140)
56. Wallin, H., P. A. Chiverton, B. Ekbom, and A. Borg. 1992. Diet, fecundity and egg size in some polyphagous predatory carabid beetles. Entomol. Exp. Appl. 65: 129-140.
57. Winder, L., C. J. Alexander, J. M. Holland, W.O.C. Symond-son, J. N. Perry, and C. Woolley. 2005. Predatory activity and spatial pattern: the response of generalist carabids to their aphid prey. J. Anim. Ecol. 74: 443-454. (Pubitemid 40764392)