Influence of cornicle droplet secretions of the cabbage aphid, Brevicoryne brassicae, on parasitism behavior of naïve and experienced Diaeretiella rapae

Insect Science

Volumn 21, Issue 1, 2014, Pages 56-64

  Moayeri, Hamid R S ^a,b   Rasekh, Arash ^c   Enkegaard, Annie ^d  

^a Department of Water Engineering   (Iran)

^b UNIVERSITY OF ZANJAN   (Iran)

^c SHAHID CHAMRAN UNIVERSITY OF AHVAZ   (Iran)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

alarm pheromone; Kairomone; Learning; Oviposition preference; Physiological cost; Y tube olfactometer

Indexed keywords

APHIDIDAE; BRASSICA OLERACEA VAR. CAPITATA; BREVICORYNE BRASSICAE; DIAERETIELLA RAPAE; HEXAPODA;

KAIROMONE; PHEROMONE;

ANIMAL; APHID; ARTICLE; CHEMISTRY; DRUG EFFECT; EGG LAYING; FEMALE; HOST PARASITE INTERACTION; LEARNING; MALE; METABOLISM; OVIPOSITION PREFERENCE; PHYSIOLOGICAL COST; PHYSIOLOGY; WASP; Y-TUBE OLFACTOMETER;

ALARM PHEROMONE; KAIROMONE; LEARNING; OVIPOSITION PREFERENCE; PHYSIOLOGICAL COST; Y-TUBE OLFACTOMETER;

ANIMALS; APHIDS; FEMALE; HOST-PARASITE INTERACTIONS; MALE; OVIPOSITION; PHEROMONES; WASPS;

EID: 84892367015     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/1744-7917.12022     Document Type: Article

References (51)

1. Acar, E.B., Medina, J.C., Lee, M.L. and Booth, G.M. (2001) Olfactory behavior of convergent lady beetles (Coleoptera: Coccinellidae) to alarm pheromone of green peach aphid (Hemiptera: Aphididae). Canadian Journal of Entomology, 133, 389-397.
2. Agarwal, M.L. (2009) Perspectives in Insect Behaviour. International Book Distributing Co. Lucknow, U.P., India, 596 pp.
3. Almohamad, R., Verheggen, F.J., Francis, F., Lognay, G. and Haubruge, E. (2008) Emission of alarm pheromone by non-preyed aphid colonies. Journal of Applied Entomology, 132, 601-604.
4. Ameixa, O. and Kindlmann, P. (2012) Effect of synthetic and plant-extracted aphid pheromones on the behaviour of Aphidius colemani. Journal of Applied Entomology, 136, 292-301.
5. Bahana, J. and Karhioc, G.K. (1986) The role of Diaeretiella rapae in population control of cabbage aphid. Journal of Insect Science, 7, 605-607.
6. Battaglia, D., Pennacchio, F., Marincola, G. and Tranfaglia, A. (1993) Cornicle secretion of Acyrthosiphon pisum (Homoptera: Aphididae) as a contact kairomone for the parasitoid Aphidius ervi (Hymenoptera: Braconidae). European Journal of Entomology, 90, 423-428.
7. Behdad, E. (2002) Introductory Entomology and Important Plant Pests in Iran. Yadbood Publishing, Isfahan, Iran, 824 pp.
8. Blande, J.D., Pickett, J.A. and Poppy, G.M. (2004) Attack rate and success of the parasitoid Diaeretiella rapae on specialist and generalist feeding aphids. Journal of Chemical Ecology, 30, 1781-1795.
9. Blande, J.D., Pickett, J.A. and Poppy, G.M. (2007) A comparison of semiochemically mediated interactions involving specialist and generalist Brassica-feeding aphids and the braconid parasitoid Diaeretiella rapae. Journal of Chemical Ecology, 33, 767-779.
10. Boo, K.S., Chung, I.B., Han, K.S., Pickett, J.A. and Wadhams, L.J. (1998) Response of the lacewing Chrysopa cognate to pheromones of its aphid prey. Journal of Chemical Ecology, 24, 631-643.
11. Bouchard, Y. and Cloutier, C. (1985) Role of olfaction in host finding by aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae). Journal of Chemical Ecology, 11, 801-808.
12. Butler, C.D. and O'Neil, R.J. (2006) Defensive response of soybean aphid (Hemiptera: Aphididae) to predation by insidious flower bug (Hemiptera: Anthocoridae). Annals of the Entomological Society of America, 99, 317-320.
13. De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. and Tumlinson, J.H. (1998) Herbivore-infested plants selectively attract parasitoids. Nature, 393, 570-573.
14. Flint, M.L. (1985) Cabbage Aphid, Brevicoryne brassicae. Integrated Pest Management for Cole Crops and Lettuce. University of California Publication 3307, pp. 36-39.
15. Francis, F., Lognay, G., Gaspar, C. and Haubruge, E. (2004) Olfactory responses to aphid and host plant volatile releases: (E)-β-farnesene an effective kairomone for the predator Adalia bipunctata. Journal of Chemical Ecology, 30, 741-755.
16. Gabrys, B.J., Gadomski, H.J., Klukowski, Z., Pickett, J.A., Sobota, G.T., Wadhams, L.J. and Woodcock, C.M. (1997) Sex pheromone of cabbage aphid Brevicoryne brassicae: identification and field trapping of male aphids and parasitoids. Journal of Chemical Ecology, 23, 1881-1890.
17. Girling, R.D., Hassall, M., Turner J.G. and Poppy, G.M. (2006) Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae. Entomologia Experimentalis et Applicata, 120, 1-9.
18. Girling, R.D., Stewart-Jones, A., Dherbecourt, J., Staley, J.T., Wright, D.J. and Poppy G.M. (2011) Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles. Proceedings of the Royal Society, 278, 2646-2653.
19. Godfray, H.C.J. (1994) Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press. Princeton, New Jersey, 473 pp.
20. Hatano, E., Kunert, G., Michaud, J.P. and Weisser, W.W. (2008) Chemical cues mediating aphid location by natural enemies. European Journal of Entomology, 105, 797-806.
21. Husebye, H., Arzt, S., Burmeister, W.P., Härtel, F.V., Brandt, A., Rossiter, J.T. and Bones, A.M. (2005) Crystal structure at 1.1 Angstroms resolution of an insect myrosinase from Brevicoryne brassicae shows its close relationship to beta-glucosidases. Insect Biochemistry and Molecular Biology, 35, 1311-1320.
22. Kunert, G., Otto, S., Rose, U.S.R., Gershenzon, J. and Weisser, W.W. (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters, 8, 596-603.
23. Lester, P.J. and Holtzer, T.O. (2002) Patch and prey utilization behaviors by Aphelinus albipodus and Diaeretiella rapae (Hymenoptera: Aphelinidae and Aphidiidae) on Russian wheat aphid (Homoptera: Aphididae). Biological Control, 24, 183-191.
24. Micha, S.G. and Wyss, U. (1996) Aphid alarm pheromone (E)-β-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology, 7, 132-139.
25. Michaud, J.P. and Mackauer, M. (1994) The use of visual cues in host evaluation by Aphidiid wasps. Ι. Comparison between 3 Aphidius parasitoids of the pea aphid. Entomologia Experimentalis et Applicata, 70, 273-283.
26. Moayeri, H.R.S., Ashouri, A., Brødsgaard, H.F. and Enkegaard, A. (2006) Odour-mediated responses of the predatory mirid bug, Macrolophus caliginosus Wagner (Heteroptera: Miridae) and its prey, the two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae). Experimental and Applied Acarology, 40, 27-36.
27. Moayeri, H.R.S., Ashouri, A., Goldansaz, S.H., Mohaghegh, J., Poll, L. and Enkegaard, A. (2008) Olfactory response of the predatory mirid bug, Macrolophus caliginosus (Het.: Miridae) to clean and infested green bean with two-spotted spider mite and identification of their volatile compounds by using GC-MS technique. Journal of Entomological Society of Iran, 27, 79-92.
28. Moayeri, H.R.S., Ashouri, A. and Mohandesi, A. (2012) Fitness costs of cotton aphid's (Aphis gossypii) cornicle secretion, as a defense mechanism. Journal of Entomological Society of Iran, 31, 51-61.
29. Mondor, E. and Roitberg, B. (2000) Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior? Journal of Insect Behaviour, 13, 321-329.
30. Mondor, E. and Roitberg, B. (2003) Aphid alarm signalling: direct effects on the emitter's development and reproduction. Canadian Journal of Zoology, 81, 756-762.
31. Montgomery, M.E. and Nault, L.R. (1977) Comparative response of aphids to the alarm pheromone, (E)-beta-farnesene. Entomologia Experimentalis et Applicata, 22, 236-242.
32. Mumm, R. and Hilker, M. (2005) The significance of background odour for an egg parasitoid to detect plants with host eggs. Chemical Senses, 30, 337-343.
33. Nishino, C., Bowers, W.S., Montgomery, M.E., Nault, L.R. and Nielson, M.W. (1976) Alarm pheromone of the spotted alfalfa aphid Therioaphis maculata Buckton (Homoptera: Aphididae). Journal of Chemical Ecology, 3, 349-357.
34. Nault, L.R. and Phelan, P.L. (1984) Alarm pheromones and sociality in pre-social insects. Chemical Ecology of Insects (eds. W.J. Bell & R.T. Carde), pp. 237-256. Chapman and Hall, London, UK.
35. Nault, L.R. and Montgomery, M.E. (1977) Aphid pheromones. Aphids as Virus Vectors (eds. K.F. Harris & K. Maramorosch), pp. 527-545. Academic Press, New York.
36. Pickett, J.A. and Griffith, D.C. (1980) Composition of aphid alarm pheromones. Journal of Chemical Ecology, 6, 349-360.
37. Powell, W., Pennacchio, F., Poppy, G.M. and Tremblay, E. (1998) Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae). Biological Control, 11, 104-112.
38. Rasekh, A., Michaud, J.P., Kharazi-Pakdel, A. and Allahyari, H. (2010) Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae). Journal of Insect Science, 10, 14.
39. Reed, H.C., Tan, S.H., Haapanen, K., Killmon, M., Reed, D.K. and Eklliott, N.C. (1995) Olfactory responses of the parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) to odor of plants, aphids, and plant-aphid complexes. Journal of Chemical Ecology, 21, 407-418.
40. Sheehan, W. and Shelton, A.M. (1989) The role of experience in plant foraging by the aphid parasitoid Diaeretiella rapae (Hymenoptera, Aphidiidae). Journal of Insect Behavior, 2, 743-759.
41. Shiojiri, K., Takabayashi, J., Yano, S. and Takafuji, A. (2000) Flight response of parasitoids toward plant herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants. Applied Entomology and Zoology, 35, 87-92.
42. Silva, J.W.P., Bento, J.M.S. and Zucchi, R.A. (2007) Olfactory response of three parasitoid species (Hymenoptera: Braconidae) to volatiles of guavas infested or not with fruit fly larvae (Diptera: Tephritidae). Biological Control, 41, 304-311.
43. Sokal, R.R. and Rohlf, F.J. (1995) Biometry: The Principles and Practice of Statistics in Biological Research. Freeman, San Francisco, CA, 880 pp.
44. Souza, B.M., Bueno, V.H.P. and Paes Bueno, V.H. (1992) Parasitoids and hyperparasitoids of mummies of Brevicoryne brassicae (Linnaeus). Revista de Agricultura Piracicaba, 67, 55-62.
45. Takabayashi, J. and Dicke, M. (1992) Response of predatory mites with different rearing histories to volatiles of uninfested plants. Entomologia Experimentalis et Applicata, 64, 187-193.
46. Takemoto, H., Kainoh, Y. and Takabayashi, J. (2011) Learning of plant volatiles by aphid parasitoids: timing to learn. Journal of Plant Interactions, 6, 137-140.
47. Vaughn, T.T., Antolin, M.F. and Bjostad, L.F. (1996) Behavioral and physiological responses of Diaeretiella rapae to semiochemicals. Entomologia Experimentalis et Applicata, 78, 187-196.
48. Verheggen, F., Arnaud, L., Bartram, S., Gohy, M. and Haubruge, E. (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. Journal of Chemical Ecology, 34, 301-307.
49. Vet, L.E.M. and Dicke, M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology, 37, 141-172.
50. Vinson, S.B. (1976) Host selection by insect parasitoids. Annual Review of Entomology, 21, 109-133.
51. Wu, G.M., Boivin, G., Brodeur, J., Giraldeau, L.A. and Outreman, Y. (2010) Altruistic defence behaviours in aphids. BMC Evolutionary Biology, 10, 19-29.