Reproductive activity and olfactory response of Lysiphlebus fabarum to the presence of an intraguild predator, Hippodamia variegata, in the host patches

Document Type : Research Paper

Authors

1 M.Sc. Student of Entomology, Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran

2 Associate Professor of Entomology, Department of Plant Protection, College of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran

3 Associate Professor of Entomology, Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, 606-8502 Japan

Abstract

In this study, the reproductive activity and olfactory response of the parasitoid wasp Lysiphlebus fabarum to the presence of an intraguild predator, the ladybird Hippodamia variegata,was investigated on the cotton aphid Aphis gossypii on cucumber plants. For this purpose, in addition to comparing the predator feeding of healthy and parasitized adult aphids, reproductive characteristics of the parasitoid wasp (percent parasitism, percent emergence, and sex ratio) were investigated in three different host patches, including those of only aphids alone, aphids with a female ladybird, and aphids with aphid carcasses. Moreover, the preference of the female wasps to these patches was determined using a Y-tube olfactometer. Ladybirds significantly preferred healthy aphids to previously parasitized ones (F2,27=12.53, P<0.001), and the proportion of parasitism by parasitoid wasps were lower in the patch containing a female ladybird (G2,42=6.99, P=0.03). According to olfactometer test results, the parasitoid wasp significantly avoided the patch containing the intraguild predator ladybird (χ2=6.40, df=19, P=0.01). In conclusion, based upon the findings of the avoidance of ladybirds by female wasps and also preference of healthy aphids by ladybirds, it is expected that female wasps forage more in patches lacking the intraguild predator ladybirds, and that ladybirds prefer feeding on healthy aphids, resulting in a reduction in the intraguild predation and improving the cotton aphid control.

Keywords


  1. Abou-Fakhr, E. M. & Kawar, N. S. (1998). Complex of endoparasitoid of aphids (Hom.: Aphididae) on vegetables other plants. Entomologicheskoe Obozrenie, 77, 753-763.
  2. Attia, A. A. & El-Hamaky, M.A. (1987). The biology of the cotton aphid Aphis gossypii Glover in Egypt (Hom: Aphididae). Bulletin Societe Entomologique Egypte, 85, 359-371.
  3. Belshaw, R., Quicke, D. L., Volkl, W. & Godfray, H. C. J. (1999). Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution, 53, 1189-1199.
  4. Bilu, E. & Coll, M. (2007). The importance of intraguild interaction to the combined effect of a parasitoid and predator on aphid population suppression. Biocontrol, 52, 753-763.
  5. Bilu, E., Hopper, K. R. & Coll, M. (2006). Host choice by Aphidius colemani: effects of plants, plant-aphid combinations and the presence of intraguild predators. Ecological Entomology, 31, 331-336.
  6. Brodeur, J. & Rosenheim, J. A. (2000). Intraguild interactions in aphid parasitoids. Entomologia Experimentalis et Applicata, 97, 93-108.
  7. Carver M. (1984). The potential host ranges in Australia of some imported aphid parasite (Hom., Aphididae). Entomophaga, 29, 351-359.
  8. Chong, J. H. & Oetting, R. D. (2007). Intraguild predation and interference by the mealybug predator Cryptolaemus montrouzieri on the parasitoid Leptomastix dactylopii. Biocontrol Science and Technology, 17(9), 933-944.
  9. Colfer, R. G. & Rosenheim, J. A. (2001). Predation on immature parasitoids and its impact on aphid suppression. Oecologia, 126, 292-304.
  10. Desneux, N., Decourtye, A. & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81-106.
  11. Dicke, M. & Grostal, P. (2001). Chemical detection of natural enemies by arthropods: an ecological perspective. Annual Review of Ecology and Systematics, 32, 1-23.
  12. Djemai, I., Meyhöher, R. & Casas, J. (2000). Geometrical games between a host and a parasitoid. The American Naturalist, 156, 257-265.
  13. Farhadi, R., Allahyari, H., Rasekh, A., Aldaghi, M. & Farhoodi, F. (2012). Comparative study of life table parameters of Hippodamia variegata (Col.: Coccinellidae) and Aphis fabae (Hem.: Aphididae). Iranian Journal of Plant Protection Science, 42(2), 209-215. (in Farsi)
  14. Frazer, B. D., Gilbert, N., Nealis, V. & Raworth, D. A. (1981). Control of aphid density by a complex of predators. The Canadian Entomologist, 113, 1035-1041.
  15. Hindayana, D., Meyhofer, R., Scholz, D. & Poehling, H. M. (2001). Intraguild predation among the hoverfly Episyrphus balteatus deGeer (Diptera: Syrphidae) and other aphidophagous predators. Biological Control, 20, 236-246.
  16. Hoffmeister, T. S. & Roitberg, B. D. (1997). Counterespionage in an insect herbivore-parasitoid system. Naturwissenschaften, 84, 117-119.
  17. Hojjat, S. H. (1993). Iran's list of aphids and their host. Shahid Chamran University of Ahvaz Publication, Ahvaz. (in Farsi)
  18. Holt, R. D. & Polis, G. A. (1997). A theoretical framework for intraguild predation. American Naturalist, 149, 745-764.
  19. Jazzer, C., Meyhofer, R., Ebssa, L. & Poehling, H. M. (2008). Two protagonists on aphidophagous patches: effects of learning and intraguild predation. Entomologia Experimentalis et Applicata, 127, 88-99.
  20. Kats, L. B. & Dill, L. M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience, 5, 361-394.
  21. Kresting, U., Satar, S. & Uygun, N. (1999). Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Homoptera: Aphididae) reared on Gossypium hirsutum. Journal of Applied Entomology, 123(1), 23-27.
  22. Leclant, F. & Deguine, J. P. (1994). Aphids (Hemiptera: Aphididae). pp. 285-323 in Matthews, G. A. & Tunstall, J.P. (Eds). Insect pests of cotton. 593 pp. Wallingford Publishing.
  23. Lima, S. L. & Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology, 68, 619-640.
  24. Lucas, E. (2005). Intraguild predation among aphidophagous predators. European Journal of Entomology, 102, 351-364.
  25. Lucas, E., Coderre, D. & Brodeur, J. (1998). Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology, 79, 1084-1092.
  26. Meyhöfer, R. & Klug, T. (2002). Intraguild predation on the aphid parasitoid Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae): mortality risks and behavioral decisions made under the threats of predation. Biological Control, 25, 239-248.
  27. Mohseni, L., Rasekh, A. & Kocheili, F. (2016). Comparative effect of wasp density in unisexual and bisexual strains of Lysiphlebus fabarum, on superparasitism in the black bean aphid, Aphis fabae. Journal of Plant Protection, 30(2), 251-260. (in Farsi)
  28. Mossadegh, M. S., Stary, P. & Salehipour, H. (2011). Aphid parasitoids in a dry lowland area of Khuzestan, Iran (Hymenoptera, Braconidae, Aphidiinae). Asian Journal of Biological Sciences, 4, 175-181.
  29. Nakashima, Y. & Senoo, N. (2003). Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: active period and effects of prior oviposition experience. Entomologia Experimentalis et Applicata, 109, 163-166.
  30. Nakashima, Y., Birkett, M. A., Pye, B. J. & Powell, W. (2006). Chemically mediated intraguild predation avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. The Journal of Chemical Ecology, 32, 1989-1998.
  31. Nuessly, G. S., Hentz, M. G., Beiriger, R. & Scully, B. T. (2004). Insects associated with faba bean, Vicia faba (Fabales: Fabaceae), in southern Florida. Florida Entomologist, 87(2), 204-211.
  32. Obrycki, J. J. & Orr, C. J. (1990). Suitability of three prey species for Nearctic populations of Coccinella septempunctata, Hippodamia variegata and Propylea quatrodecimpunctata (Coleoptera: Coccinellidae). Journal of Economic Entomology, 83, 1292-1297.
  33. Papaj, D. R. & Lewis, A. C. (1993). Insect Learning. Ecological and Evolutionary Perspectives. Chapman & Hall, New York, NY, USA.
  34. Polis, G. A., Myers, C. A. & Holt, R. D. (1989). The ecology and evolution of intraguild predation: Potential competitors that eat each other. Annual Review of Ecology & Systematics,20, 297-330.
  35. Provost, C., Coderre, D., Lucas, E. & Bostanian, N. J. (2003). Impacts of Lambda cyhalothrin on intraguild predation among three mite predators. Environmental Entomology, 32, 256-263.
  36. Rakhshani, E., Talebi, A. A., Manzari, S., Rezwani, A. & Rakhshani, H. (2006). An investigation on alfalfa aphids and their parasitoids in different parts of Iran, with a key to the parasitoids (Hemiptera: Aphididae; Hymenoptera: Braconidae: Aphidiinae). Journal of Entomological Society of Iran, 25(2), 1-14.
  37. Rasekh, A., Michaud, J. P., Allahyari, H. & Sabahi, Q. (2010). The foraging behavior of Lysiphlebus fabarum (Marshall) a thelytokous parasitoid of the black bean aphid in Iran. Journal of Insect Behavior, 23, 165-179.
  38. Rasekh, A., Kharazi-Pakdel, A., Michaud, J. P., Allahyari, H. & Rakhshani, E. (2011). Report of a thelytokous population of Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae) from Iran. Journal of Entomological Society of Iran, 30(2), 83-84.
  39. Raymond, B., Darby, A. C. & Douglas, A. E. (2000). Intraguild predators and the spatial distribution of a parasitoid. Oecologia, 124, 367-372.
  40. Sadeghi, A. (1991). An investigation on the coccinellids fauna of alfalfa fields and determination of species at Karaj. M. Sc. thesis. Faculty of Agriculture, University of Tehran, Iran. (in Farsi)
  41. SPSS. (1998). SPSS 8.0 for Windows. Prentice Hall, Upper Saddle River, NJ, USA.
  42. Stary, P., Remaudière, G., González, D. & Shahrokhi, S. (2000). A review and host associations of aphid parasitoids (Hym., Braconidae, Aphidiinae) of Iran. Parasitica, 56(1), 15-41.
  43. Taylor, A. J., Müller, C. B. & Godfray, H. C. J. (1998). Effect of aphid predators on oviposition behavior of aphid parasitoids. Journal of Insect Behavior, 11, 297-302.
  44. Turchin, P. & Kareiva, P. (1989). Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology, 70, 1008-1016.
  45. Vet, L. E. M., Lewis, W. J. & Cardé, R. T. (1995). Parasitoid foraging and learning. In: R. T. Cardé & W. J. Bell (Ed), Chemical Ecology of Insects (pp. 65–101.) Chapman & Hall, New York, NY, USA.
  46. Vojdani, S. (1964). The useful and harmful ladybirds of Iran. Plant Protection Publication of University of Tehran. (in Farsi)
  47. Weisser, W. W., Holston, A. I. & Volkl, W. (1994). Foraging strategies in solitary parasitoids: the trade-off between female and offspring mortality risks. Evolutionary Ecology, 8, 587-597.
  48. Yeno, E. (2005). Effects of intraguild predation and interspecific competition among Biological control agents in augmentation biological control in greenhouse. Second international symposium on biological control of arthropods, 12-16 Sep, Davos, Switzerland, pp. 523-531.
  49. Yu, D. S., Van Achterberg, C. & Horstmann, K. (2013). World Ichneumonoidea. Taxonomy, Biology, Morphology and Distribution. Taxapad (Scientific Names for Information Management), Interactive Catalogue, Ottawa. Retrieved May 15, 2016, from http://www.taxapad.com.