On the identity of cereal aphid parasitoid wasps Aphidius uzbekistanicus, Aphidius rhopalosiphi, and Aphidius avenaphis (Hymenoptera: Braconidae: Aphidiinae) by examination of COI mitochondrial gene, geometric morphometrics, and morphology

Annals of the Entomological Society of America

Volumn 104, Issue 6, 2011, Pages 1221-1232

  Kos, K ^a   Petrovic A ^b   Stary P ^c   Kavallieratos, N G ^d   Ivanovc A ^b   Tosevski I ^e,f   Jakse J ^a   Trdan, S ^a   Tomanovic Z ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b UNIVERSITY OF BELGRADE   (Serbia)

^c INSTITUTE OF ENTOMOLOGY   (Czech Republic)

^d BENAKI PHYTOPATHOLOGICAL INSTITUTE   (Greece)

^e CABI   (Switzerland)

^f Institute for Plant Protection and Environment   (Serbia)

Author keywords

aphidiine wasps; barcoding; genetic diversity; morphological

Indexed keywords

APHID; BIOCONTROL AGENT; CEREAL; CROP PEST; DIVERGENCE; GENETIC VARIATION; MORPHOLOGY; MORPHOMETRY; PALEARCTIC REGION; PARASITOID; SYMPATRY; TAXONOMY; WASP;

EURASIA; SERBIA;

APHIDIDAE; APHIDIINAE; APHIDIUS AVENAPHIS; APHIDIUS RHOPALOSIPHI; APHIDIUS UZBEKISTANICUS; BRACONIDAE; HYMENOPTERA; VESPOIDEA;

EID: 82155170548     PISSN: 00138746     EISSN: None     Source Type: Journal    
DOI: 10.1603/AN11055     Document Type: Article

References (59)

1. Altieri, M. A., J. Trujillo, L. Campos, C. Klein-Koch, C. S Gold, and J.R. Quezada. 1989. El control biologico clasico en America Latina en su contexto historico. Manejo Int. Plagas 12: 82-107.
2. Altieri, M. A. 1992. Sustainable agricultural development in Latin America: Exploring the possibilities. Agric. Ecosyst. Environ. 39: 1-21.
3. Blackman, R. L., and V. E. Eastop. 2000. Aphids on the worldõs crops. An identification guide, 2nd ed. Wiley Ltd., Chichester, United Kingdom.
4. Bookstein, F. L. 1991. Morphometric tools for landmark data. Cambridge University Press, Cambridge, United Kingdom.
5. Bookstein, F. L. 1997. Morphometric Tools for landmark data. morphometry and biology. Cambridge University Press, Cambridge, United Kingdom.
6. Botto, E. N., C. Monetti, J. Ortego, and A. Duchetti. 1995. Natural enemies of cereal aphids and their potential impact against the Russian wheat aphid (Homoptera: Aphididae) in Argentina. Vedalia 2: 39-40.
7. Brewer, M. J., and N. C. Elliott. 2004. Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annu. Rev. Entomol. 49: 219-242.
8. Clement, M., D. Posada, and K. A. Crandall. 2000. TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9: 1657-1659.
9. Dixon, A.F.G. 1987. Cereal aphids as an applied problem. Agric. Zool. Rev. 2: 1-57.
10. Eady, R. D. 1969. A new diagnostic character in Aphidius (Hymenoptera: Braconidae) of special significance in species on pea aphid. Proc.R. Entomol. Soc. Lond. B Biol. Sci. 38: 165-173.
11. Fletcher, J. 1899. Report of the entomologist and botanist 1898, pp. 167-219. In Experimental farms reports for 1898. Queenõs Printer, Ottawa, ON, Canada.
12. Fitch, A. 1861. Sixth report on the noxious, beneficial and other insects of the State of New York. Trans. NY State Agric. Soc. 20: 839-840.
13. Folmer, O., M. Black, W. Hoeh, R. Lutz, and R. Vrijenhoek. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3: 294-297.
14. Fomitcheva, V. W., J. Schubert, F. Rabenstein, and A. Habekufl. 2005. Immunodetection of the replicative complex of barley yellow dwarf virus-PAV in vivo. Eur. J. Plant Pathol. 112: 259-266.
15. Godfray, H.C.J. 1994. Parasitoids: Behavioural and evolutionary ecology. Princeton University Press, Princeton, NJ.
16. Gruber, P. F., T. J. Poprawski, and D. Coutinot. 1994. Hymenopterous parasites and hyperparasites of Schizaphis graminum (Rondani) (Homoptera: Aphididae) on sorghum, in the Drome, France. J. Appl. Entomol. 117: 477-490.
17. Halbert, S. E., J. B. Johnson, P. L. Graves, P. M. Marsh, and D. Nelson. 1996. Aphidius uzbekistanicus (Hymenoptera: Aphidiidae) established in Idaho. Pan-Pac. Entomol. 72: 13-16.
18. Höller, C. 1990. Overwintering and hymenopterous parasitism in autumn of the cereal aphid Sitobion avenae (F.) in northern FR Germany. J. Appl. Entomol. 109: 21-28.
19. Höller, C. 1991. Evidence for the existence of a species closely related to the cereal aphid parasitoid Aphidius rhopalosiphi De Stefani-Perez based on host ranges, morphological characters, isoelectric focusing banding patterns, cross-breeding experiments, and sex pheromone specificities (Hymenoptera: Braconidae: Aphidiinae). Syst. Entomol. 16: 15-28.
20. Kavallieratos, N. G., Ž. Tomanović, P. Starý, C. G. Athanassiou, G.P. Sarlis, O. Petrović, M. Niketić, and M. Anagnou-Veroniki. 2004. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Appl. Entomol. Zool. 39: 527-563.
21. Kavallieratos, N. G., Ž. Tomanović, C. G. Athanassiou, P. Starý, V. Žikić, G.P. Sarlis, and C. Fasseas. 2005. Aphid parasitoids infesting cotton, citrus, tobacco, and cereal crops in southeastern Europe: Aphid-plant associations and keys. Can. Entomol. 137: 516-531.
22. Klingenberg, C.P. 2008. MorphoJ. Faculty of Life Sciences, University of Manchester, United Kingdom. (http://www.flywings.org.uk/MorphoJ?page.htm).
23. Latteur, G., and A. Rassel. 1980. Aphidius frumentarius n. sp. Latteur (Hymenoptera: Aphidiidae), parasite de divers pucerons de cé ré ales (Homoptera, Aphididae) en Belgique. Bull. Ann. Soc.R. Belge Entomol. 115: 311-322.
24. Macfayden, S., R. Gibson, L. Raso, D. Sint, M. Traugott, and J. Memmott. 2009. Parasitoid control of aphids in organic and conventional farming systems. Agric. Ecosyst. Environ. 133: 14-18.
25. Marsh, P. M. 1979. Aphidiidae, pp. 295-313. In K. V. Krombein, P. D. Hurd, Jr., D.R. Smith, and B. D. Burks [eds.], Catalog of Hymenoptera North of Mexico. vol. 1: Symphyta and Apocrita (Parasitica). Smithsonian Institution Press, Washington, DC.
26. Meyer, C.P., and G. Paulay. 2005. DNA barcoding: Error rates based on comprehensive sampling. PLoS Biol. 3: 2229-2238.
27. Muesebeck, C.F.W., and L. M. Walkley. 1951. Family Braconidae, pp. 90-184. In C.F.W. Muesebeck, K. V. Krombein, and H. K. Townes [eds.], Hymenoptera of America north of Mexico. Synoptic catalog. Agriculture Monograph No. 2, U.S. Government Printing Office, Washington, DC.
28. Paoletti, M. G., P. Boscolo, and D. Sommaggio. 1997. Beneficial insects in fields surrounded by hedgerows in North Eastern Italy. Entomol. Res. Org. Agric. 15: 311-323.
29. Pennacchio, F. 1989. The Italian species of the genus Aphidius Nees (Hymenoptera: Braconidae: Aphidiinae). Boll. Lab. Entomol. Agric. Filippo Silvestri 46: 75-106.
30. Pennacchio, F., and C.Höller. 1990. Identity and taxonomic status of Aphidius uzbekistanicus Luzhetzki (Hymenoptera: Braconidae), a parasitoid of Sitobion Mordvilko species (Homoptera: Aphididae). Boll. Lab. Entomol. Agric. Filippo Silvestri 47: 127-137.
31. Pike, K. S., P. Starý, T. Miller, D. Allison, L. Boydston, G. Graff, and R. Gillespie. 1997. Small-grain aphid parasitoids (Hymenoptera: Aphelinidae and Aphidiidae) of Washington: Distribution, relative abundance, seasonal occurrence, and key to known North American species. Environ. Entomol. 26: 1299-1311.
32. Pike, K. S., P. Starý, T. Miller, D. Graff, D. Allison, L. Boydston, and R. Miller. 2000. Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northwest USA. Proc. Entomol. Soc. Wash. 102: 688-740.
33. Pons, X., and P. Starý. 2003. Spring aphid-parasitoid (Homoptera: Aphididae, Hymenoptera: Braconidae) association and interactions in a Mediterranean arable crop ecosystem, including Bt maize. J. Pest Sci. 76: 133-138.
34. Powell,W. 1982. The identification of hymenopterous parasitoids attacking cereal aphids in Britain. Syst. Entomol. 7: 465-473.
35. Pungerl, N. B. 1983. Variability in characters commonly used to distinguish Aphidius species (Hymenoptera: Aphidiidae). Syst. Entomol. 8: 425-430.
36. Pungerl, N. B. 1984. Host preference of Aphidius (Hymenoptera: Aphidiidae) populations parasitising pea and cereal aphids (Hemiptera: Aphididae). Bull. Entomol. Res. 74: 153-161.
37. Pungerl, N. B. 1986. Morphometric and electrophoretic study of Aphidius species (Hymenoptera: Aphidiidae) reared from a variety of aphid hosts. Syst. Entomol. 11: 327-354.
38. Rohlf, F. J., and D. E. Slice. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39: 40-59.
39. Rohlf, F. J. 2005. TpsDig program, version 2.04. Ecology and Evolution. SUNY at Stony Brook. (http://life.bio.sunysb. edu/morph/).
40. Sharkey, M. J., and R. A. Wharton. 1997. Morphology and terminology. pp. 19-37. In R. A. Wharton, P. M. Marsh, and M. J. Sharkey [eds.], Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication 1. International Society of Hymenopterists, Washington, DC.
41. SAS Institute. 2009. The SAS System version 9.1.3. Foundation for Microsoft Windows. SAS Institute, Cary, NC.
42. Sheets, H. D. 2003. IMP suite (integrated morphometrics package). Canisius College, Buffalo, NY.
43. Starý, P. 1972. Aphidius uzbekistanicus Luzhetzki (Hymenoptera: Aphidiidae) a parasite of graminicolous pest aphids. Annot. Zool. Botan. 85: 1-7.
44. Starý, P. 1973. A review of the Aphidius species (Hymenoptera: Aphidiidae) of Europe. Annot. Zool. Botan. 84: 1-85.
45. Starý, P. 1980. Integrated control of wheat aphids. FAO Technical Cooperative Program BRA/8908/M. Mission Report. National Wheat Research Center. EMBRAPA, Passo Fundo, Brazil.
46. Starý, P. 1981. Biosystematic synopsis of parasitoids on cereal aphids in the western Palaearctic (Hymenoptera: Aphidiidae, Homoptera: Aphidoidea). Acta Entomol. Bohemoslov. 78: 382-396.
47. Starý, P., F. A. Rodriguez, M.P. Gerding, M. Norambuena, and G. Remaudiére. 1994. Distribution, frequency, host range and parasitism of two new cereal aphid pests, Sitobion fragariae (Walker) and Metopolophium festucae cerealium Stroyan (Homoptera: Aphididae), in Chile. Agric. Technol. 54: 54-59.
48. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599. (http://www.kumarlab.net/publications).
49. Templeton, A.R., K. A. Crandall, and C. F. Sing. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. 3. Cladogram estimation. Genetics 132: 619-633.
50. Tomanović, Ž., M. Brajković, and M. Korunić. 1999. Numerical discrimination of some Aphidius species (Aphidiidae: Hymenoptera) from Yugoslavia. Arch. Biol. Sci. 51: 209-218.
51. Tomanović, Ž., N. G. Kavallieratos, P. Starý, C. G. Athanassiou, V. Žikić, O. Petrović-Obradović, and G.P. Sarlis. 2003. Aphidius Nees aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Serbia and Montenegro: Tritrophic associations and key. Acta Entomol. Serbica 8: 15-39.
52. Tomanović, Ž., N. G. Kavallieratos, P. Starý, O. Petrović-Obradović, C. G. Athanassiou, and L. Stanisavljević. 2008. Cereal aphids (Hemiptera: Aphidoidea) in Serbia: Seasonal dynamics and natural enemies. Eur. J. Entomol. 105: 495-501.
53. Vickerman, G.P., and S. D. Wratten. 1979. The biology and pest status of cereal aphids (Hemiptera: Aphididae) in Europe: A review. Bull. Entomol. Res. 69: 1-32.
54. Watanabe, C. 1941. On the aphidiid parasites of the grain aphis, Macrosiphum granarium (Kirby). Insecta Matsumurana 15: 167-170.
55. Wootton, R. J. 2001. Design, function and evolution in the wings of holometabolous insects. Zool. Scr. 31: 31-40.
56. Zelditch, M. L., D. L. Swiderski, H. D. Sheets, andW.L. Fink. 2004. Geometric morphometrics for biologists: A primer. Elsevier Academic, New York.
57. Zuñiga, E., 1986a. Control biológico de los áfidos (Homoptera: Aphididae) de los cereales en Chile. 1. I. Revision historica y lineas de trabajo. Agric. Tech. 46: 475-477.
58. Zuñiga, E. 1986b. Control biológico de los áfidos (Homoptera: Aphididae) de los cereales en Chile. II Obtención, introducción y cuarantena de depredatores y parasitoides. Agric. Tech. 46: 479-487.
59. Zuñiga, E. 1987. Biological control of cereal aphids in the Southern Cone of South America, pp. 362-367. In P. A. Burnett [ed.], World perspectives on barley yellow dwarf. Proceedings of the International Workshop, 6-11 July 1987, Udine, Italy.