Factors contributing to the poor performance of a soybean aphid parasitoid binodoxys communis (Hymenoptera: Braconidae) on an herbivore resistant soybean cultivar

Environmental Entomology

Volumn 41, Issue 6, 2012, Pages 1417-1425

  Ballman, E S ^a   Ghising, K ^a   Prischmann Voldseth, D A ^a   Harmon, J P ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Aphis glycines; Binodoxys communis; biological control; host plant resistance; soybean

Indexed keywords

APHID; BIOCONTROL AGENT; BIOLOGICAL CONTROL; CULTIVAR; EMERGENCE; HERBIVORE; HOST PLANT; INTEGRATED PEST MANAGEMENT; INVASIVE SPECIES; NATURAL ENEMY; PARASITOID; PEST SPECIES; RESISTANCE MANAGEMENT; SOYBEAN; WASP;

ANIMAL; APHID; ARTICLE; BIOLOGICAL CONTROL AGENT; BIOLOGICAL PEST CONTROL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HERBIVORY; PHYSIOLOGY; SOYBEAN; WASP;

ANIMALS; APHIDS; BIOLOGICAL CONTROL AGENTS; HERBIVORY; PEST CONTROL, BIOLOGICAL; SOYBEANS; WASPS;

UNITED STATES;

APHIDIDAE; APHIS GLYCINES; BINODOXYS; BRACONIDAE; GLYCINE MAX; HYMENOPTERA;

EID: 84871593670     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN12188     Document Type: Article

References (67)

1. Ananthakrishnan, T. N. 1990. Chemical ecology in biological-control. Curr. Sci. 59: 1319-1322.
2. Bergman, J. M., and W. M. Tingey. 1979. Aspects of interaction between plant genotypes and biological control. Bull. ESA 25: 275-279.
3. Bernal, J. S., R. F. Luck, and J. G. Morse. 1999. Host Influences on sex ratio, longevity, and egg load of two Metaphycus species parasitic on soft scales: implications for insectary rearing. Entomol. Exp. Appl. 92: 191-204.
4. Campbell, A., B. D. Frazer, N. Gilbert, A. P. Gutierrez, and M. Mackauer. 1974. Temperature requirements of some aphids and their parasites. J. Appl. Ecol. 11: 431-438.
5. Chacón, J. M., M. K. Asplen, and G. E. Heimpel. 2012. Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field. Biol. Control 60: 16-25.
6. Chiozza, M. V., M. E. O'Neal, and G. C. MacIntosh. 2010. Constitutive and induced differential accumulation of amino acid in leaves of susceptible and resistant soybean plants in response to the soybean aphid (Hemiptera: Aphididae). Environ. Entomol. 39: 856-864.
7. Costamagna, A. C., and D. A. Landis. 2006. Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol. Appl. 16: 1619-1628.
8. Costamagna, A. C., and D. A. Landis. 2011. Lack of strong refuges allows top-down control of soybean aphid by generalist natural enemies. Biol. Control 57: 184-192.
9. Dicke, M. 1999. Direct and indirect effects of plants on performance of beneficial organisms, pp. 105-153. In J. R. Ruberson (ed.), Handbook of Pest Management. Marcel Dekker, New York, NY.
10. Dicke, M., and L.E.M. Vet. 1999. Plant-carnivore interactions: evolution and ecological consequences for plant, herbivore and carnivore, pp. 483-520. In H. Olff, V. K. Brown, and R. H. Drent (eds.), Herbivores: Between Plants and Predators. Blackwell, Oxford, United Kingdom.
11. Donaldson, J. R., S. W. Myers, and C. Gratton. 2007. Density-dependent responses of soybean aphid (Aphis glycines Matsumura) populations to generalist predators in mid to late season soybean fields. Biol. Control 43: 111-118.
12. Fehr, W. R., and C. E. Caviness. 1977. Stages of soybean development. Agriculture and Home Economics Experiment Station Iowa State University of Science and Technology, Ames, IA.
13. Eigenbrode, S. D. 2004. The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthropod Struct. Dev. 33: 91-102.
14. Fox, T. B., D. A. Landis, F. F. Cardoso, and C. D. Difonzo. 2004. Predators suppress Aphis glycines Matsumura population growth in soybean. Environ. Entomol. 33: 608-618.
15. Gardiner, M. M., D. A. Landis, C. Gratton, C. D. DiFonzo, M. O'Neal, J. M. Chacón, M. T. Wayo, N. P. Schmidt, E. E. Mueller, and G. E. Heimpel. 2009. Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol. Appl. 19: 143-154.
16. Gassmann, A. J., S. P. Stock, M. S. Sisterson, Y. Carriere, and B. E. Tabashnik. 2008. Synergism between entomopathogenic nematodes and Bacillus thuringiensis crops: integrating biological control and resistance management. J. Appl. Ecol. 45: 957-966.
17. Ghising, K. 2011. Impact of Rag1 aphid resistant soybeans on Binodoxyscommunis(Gahan)(Hymenoptera: Braconidae), a parasitoid of soybean aphid Aphis glycines (Matsumura) (Hemiptera: Aphididae). M.S. thesis, North Dakota State University, Fargo, ND.
18. Ghising, K., J. P. Harmon, P. B. Beauzay, D. A. Prischmann-Voldseth, T. C. Helms, P. J. Ode, and J. J. Knodel. 2012. Impact of Rag1 aphid resistant soybeans on Binodoxys communis (Hymenoptera: Braconidae), a parasitoid of soybean aphid (Hemiptera: Aphididae) Environ. Entomol. 41: 282-288.
19. Godfray, H.C.J. 1993. Parasitoids: behavior and evolutionary ecology. Princeton University Press, Princeton, NJ.
20. Gould, F., G. G. Kennedy, and M. T. Johnson. 1991. Effects of natural enemies of the rate of herbivore adaptation to resistant host plants. Entomol. Exp. Appl. 58: 1-14.
21. Groot, A. T., and M. Dicke. 2002. Insect-resistant transgenic plants in a multi-trophic context. Plant J. 31: 387-406.
22. Harvey, J. A. 2005. Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomol. Exp. Appl. 117: 1-13.
23. Heimpel, G. E., L. E. Frelich, D. A. Landis, K. R. Hopper, K. A. Hoelmer, Z. Sezen, M. K. Asplen, and K. M. Wu. 2010. European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol. Invasions 12: 2913-2931.
24. Hesler, L. S., and K. E. Dashiell. 2008. Identification and characterization of new sources of resistance to Aphis glycines Matsumura (Hemiptera: Aphididae) in soybean lines. Appl. Entomol. Zool. 43: 197-206.
25. Hill, C. B., Y. Li, and G. L. Hartman. 2004. Resistance to the soybean aphid in soybean germplasm. Crop Sci. 44: 98-106.
26. Hill, C. B., Y. Li, and G. L. Hartman. 2006. A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Sci. 46: 1601-1605.
27. Hill, C. B., L. Crull, T. K. Herman, D. J. Voegtlin, and G. L. Hartman. 2010. A new soybean aphid (Hemiptera: Aphididae) biotype identified. J. Econ. Entomol. 103: 509-515.
28. Hill, C. B., A. Chirumamilla, and G. L. Hartman. 2012. Resistance and virulence in the soybean-Aphis glycines interaction. Euphytica. (doi: 10.1007/s10681-012-0695-z).
29. Hodgson, E. W., R. C. Venette, M. Abrahamson, and D. W. Ragsdale. 2005. Alate production of soybean aphid (Homoptera: Aphididae) in Minnesota. Environ. Entomol. 34: 1456-1463.
30. Ives, A. R., S. S. Schooler, V. J. Jagar, S. E. Knuteson, M. Grbic, and W. H. Settle. 1999. Variability and parasitoid foraging efficiency: a case study of pea aphids and Aphidius ervi. Am. Nat. 154: 652-673.
31. JMP. 2010. JMP version 9.0. SAS Institute, Cary, NC.
32. Jun, T. H., M.A.R. Mian, and A. P. Michel. 2012. Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor. Appl. Genet. 124: 13-22.
33. Kim, K. S., C. B. Hill, G. L. Hartman, M.A.R. Mian, and B. W. Diers. 2008. Discovery of soybean aphid biotypes. Crop Sci. 48: 923-928.
34. Kratina, P., M. Vos, A. Bateman, and B. R. Anholt. 2009. Functional responses modified by predator density. Oecologia 159: 425-433.
35. Lampson, L. J., J. G. Morse, and R. F. Luck. 1996. Host selection, sex allocation, and host feeding by Metaphycus helvolus (Hymenoptera: Encyrtidae) on Saissetia oleae (Homoptera: Coccidae) and its effect on parasitoid size, sex, and quality. Environ. Entomol. 25: 283-294.
36. Li, Y., C. B. Hill, and G. L. Hartman. 2004. Effect of three resistant soybean genotypes on the fecundity, mortality, and maturation of soybean aphid (Homoptera: Aphididae). J. Econ. Entomol. 97: 1106-1111.
37. Li, Y., J. Zou, M. Li, D. D. Bilgin, L. O. Vodkin, G. L. Hartman, and S. T. Clough. 2008. Soybean defense responses to the soybean aphid. New Phytol. 179: 185-195.
38. Liu, J., K. M. Wu, K. R. Hopper, and K. J. Zhao. 2004. Population dynamics of Aphis glycines (Homoptera: Aphididae) and its natural enemies in soybean in northern China. Ann. Entomol. Soc. Am. 97: 235-239.
39. Lovinger, A., D. Liewehr, and W. O. Lamp. 2000. Glandular trichomes on alfalfa impede searching behavior of the potato leafhopper parasitoid. Biol. Control 18: 187-192.
40. Lundgren, J. G., L. S. Hesler, K. Tilmon, K. Dashiell, and R. Scott. 2009. Direct effects of soybean varietal selection and Aphis glycines-resistant soybeans on natural enemies. Arthropod-Plant Interact. 3: 9-16.
41. Mensah, C., C. DiFonzo, R. L. Nelson, and D. C. Wang. 2005. Resistance to soybean aphid in early maturing soybean germplasm. Crop Sci. 45: 2228-2233.
42. Miao, J., K. M. Wu, K. R. Hopper, and G. X. Li. 2007. Population dynamics of Aphis glycines (Homoptera: Aphididae) and impact of natural enemies in Northern China. Environ. Entomol. 36: 840-848.
43. Mian, M.A.R., R. B. Hammond, and S.K.S. Martin. 2008a. New plant introductions with resistance to the soybean aphid. Crop Sci. 48: 1055-1061.
44. Mian, M.A.R., S. T. Kang, S. E. Beil, and R. B. Hammond. 2008b. Genetic linkage mapping of the soybean aphid resistance gene in PI 243540. Theor. Appl. Genet. 117: 955-962.
45. Michel, A. P., M. Omprakash, and M. A. Rouf Mian. 2011. Evolution of soybean aphid biotypes: understanding and managing virulence to host-plant resistance, soybean-molecular aspects of breeding. In A. Sudaric (ed.), (ISBN: 978-953-307-240-1). InTech. (http://www.intechopen. com/books/soybean-molecular- aspects-of-breeding/evolution-of-soybean-aphid-biotypes-understanding- andmanaging-virulence-to-host-plant-resistance).
46. Mishra, S., and R. Singh. 1991. Effect of host density on the demographic-statistics of an aphid parasitoid Lysiphlebusdelhiensis (Subba Rao and Sharma) (Hympenoptera, Aphidiidae). Biol. Agric. Hortic. 7: 281-302.
47. Noma, T., C. Gratton, M. Colunca-Garcia, M. J. Brewer, E. E. Mueller, K.A.G. Wyckhuys, G. E. Heimpel, and M. E. O'Neal. 2010. Relationship of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, landscape structure, and natural enemies. Environ. Entomol. 39: 31-41.
48. Ode, P. J. 2006. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51: 163-185.
49. Price, P. W., C. E. Bouton, P. Gross, B. A. McPheron, J. N. Thompson, and A. E. Weis. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11: 41-65.
50. Quisenberry, S. S., and D. J. Schotzko. 1994. Integration of plant-resistance with pest-management methods in crop production systems. J. Agric. Entomol. 11: 279-290.
51. Ragsdale, D. W., B. P. McCornack, R. C. Venette, B. D. Potter, I. V. Macrae, E. W. Hodgson, M. E. O'Neal, K. D. Johnson, R. J. O'Neil, C. D. Difonzo, et al. 2007. Economic threshold for soybean aphid (Hemiptera: Aphididae). J. Econ. Entomol. 100: 1258-1267.
52. 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.
53. Rhainds, M., H.J.S. Yoo, P. Kindlmann, D. Voegtlin, D. Castillo, C. Rutledge, C. Sadof, S. Yaninek, and R. J. O'Neil. 2010. Two-year oscillation cycle in abundance of soybean aphid in Indiana. Agric. For. Entomol. 12: 251-257.
54. 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.
55. Schooler, S. S., A. R. Ives, and J. Harmon. 1996. Hyperparasitoid aggregation to variation in Aphidius ervi host densities at three spatial scales. Ecol. Entomol. 21: 249-258.
56. Schuler, T. H., G. M. Poppy, B. R. Kerry, and I. Denholm. 1999. Potential side effects of insect-resistant transgenic plants on arthropod natural enemies. Trends Biotechnol. 17: 210-216.
57. Song, F., and S. M. Swinton. 2009. Returns to integrated pest management research and outreach for soybean aphid. J. Econ. Entomol. 102: 2116-2125.
58. Thurn, A. C. 2010. Effects of soybean aphid resistance on the lady beetle Harmonia axyridis mediated by the soy-bean aphid Aphis glycines. M.S. thesis, North Dakota State University Fargo, ND. van Emden, H. F. 1995. Host plant-Aphidophaga interactions. Agric. Ecosys. Environ. 52: 3-11.
59. Vinson, S. B. 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21: 109-133.
60. White, J. A., and D. A. Andow. 2005. Host-parasitoid interactions in a transgenic landscape: spatial proximity effects of host density. Environ. Entomol. 34: 1493-1500.
61. Wiarda, S. L., W. R. Fehr, and M. E. O'Neal. 2012. Soybean aphid (Hemiptera: Aphididae) development on soybean with Rag1 alone, Rag2 alone, and both genes combined. J. Econ. Entomol. 105: 252-258.
62. Wu, Z. S., D. Schenk-Hamlin, W. Y. Zhan, D. W. Ragsdale, and G. E. Heimpel. 2004. The soybean aphid in China: a historical review. Ann. Entomol. Soc. Am. 97: 209-218.
63. Wyckhuys, K.A.G., K. R. Hopper, K. M. Wu, C. Straub, C. Gratton, and G. E. Heimpel. 2007. Predicting potential ecological impact of soybean aphid biological control introductions. Biocontrol News Information 28N: 30-34.
64. Wyckhuys, K.A.G., J. E. Strange-George, C. A. Kulhanek, F. L. Wackers, and G. E. Heimpel. 2008a. Sugar feeding by the aphid parasitoid Binodoxys communis: how does honeydew compare with other sugar sources? J. Insect Physiol. 54: 481-491.
65. Wyckhuys, K.A.G., L. Stone, N. Desneux, K. A. Hoelmer, K. R. Hopper, and G. E. Heimpel. 2008b. Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance. Bull. Entomol. Res. 98: 361-370.
66. Zhang, G. R., C. H. Gu, and D. C. Wang. 2009. Molecular mapping of soybean aphid resistance genes in PI 567541B. Theor. Appl. Genet. 118: 473-482.
67. Zhang, G. R., C. H. Gu, and D. C. Wang. 2010. Anovel locus for soybean aphid resistance. Theor. Appl. Genet. 120: 1183-1191.