Intraguild Predation on the Parasitoid Wasp Aphidius colemani by the Predator Aphidoletes aphidimyza: Effect of Host Plant Cultivars

Authors
1 Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Islamic Republic of Iran.
2 Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili
3 Department of Horticultural Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Islamic Republic of Iran.
4 Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Islamic Republic of Iran.
Abstract
In a tri-trophic system, guild members may engage in IntraGuild Predation (IGP) and their interactions may be affected by the host plants. We used a system composed of the predatory gall midge, Aphidoletes aphidimyza Rondani, the parasitoid wasp, Aphidius colemani Viereck, and the melon aphid, Aphis gossypii Glover, to test how the outputs of IGP were affected by two cultivars of cucumber (Khasib and Karim). IGP between natural enemies were examined on a single cucumber plant of each cultivar infested with mummified, parasitized or healthy individuals of melon aphid in a controlled environment room at 25±2°C, 65±5% RH, and a photoperiod of 16L: 8D hours. According to the results, A. aphidimyza was the effective predator of parasitized aphids, but not on mummified ones. In treatments with either healthy or parasitized aphids alone, A. aphidimyza consumed significantly less numbers of healthy aphids or parasitized ones on Karim cultivar. When predators were provided with healthy aphids and parasitized aphids together on plants, the risk for parasitized aphids of being predated upon by A. aphidimyza larvae was significantly reduced on Karim cultivar. Manly’s Preference Index for healthy aphids on Karim cultivar was significantly the highest. The results revealed that the strength of IGP on IG-prey on Karim cultivar was less than Khasib cultivar. Therefore, better control of melon aphid population can be expected on this cultivar.

Keywords


1. Almohamad, R., Verheggen, F. J., Francis, F., Hance, T. and Haubruge, E. 2008. Discrimination of Parasitized Aphids by a Hoverfly Predator: Effects on Larval Performance, Foraging, and Oviposition Behavior. Entomol. Exp. Appl., 128: 73-80.
2. Basij, M., Askarianzaeh, A., Asgari, S., Moharramipou, S. and Rafezi, R. 2011. Evaluation of Resistance of Cucumber Cultivars to the Vegetable Leaf Miner (Liriomyza sativae Blanchard) (Diptera: Agromyzidae) in Greenhouse. Chil. J. Agr. Res., 71: 395-400.
3. Bilu, E. and Coll, M. 2009. Parasitized Aphids Are Inferior Prey for a Coccinellid Predator: Implications for Intraguild Predation. Environ. Entomol., 38: 153-158.
4. Blackman, R. L. and Eastop, V. F. 2000. Aphids on the World’s Crops: an Identification and Information Guide. Wiley, London, United Kingdom, 414 PP.
5. Cakmak, I., Janssen, A., Sabelis, M. W. and Baspinar, H. 2009. Biological Control of an Acarine Pest by Single and Multiple Natural Enemies. Biol. Control, 50: 60-65.
6. Chacon, J. M. and Heimpel, G. E. 2010. Density-Dependent Intraguild Predation of an Aphid Parasitoid. Oecologia, 164: 213-220.
7. Colfer, R. G. and Rosenheim, J. A. 2001. Predation on Immature Parasitoids and Its impact on Aphid Suppression. Oecologia, 126: 292-304.
8. Deguince, J. P., Goze, E. and Leclant, F. 1994. Incidence of Early Outbreaks of the Aphid Aphis gossypii Glover in Cotton Growing in Cameroon. Int. J. Pest Manag., 40:132-140.
9. Doryanizadeh, N., Moharramipour, S., Hosseininaveh, V. and Mehrabadi, M. 2016. Effect of Eight Cucumis Genotypes on Life Table and Population Growth Parameters of Melon Aphid: An Approach to Assess Antibiosis Resistance. J. Agr. Sci. Tech., 18: 1819-1832.
10. Enkegaard, A., Christensen, R. K. and Brodsgaard, H. F. 2005. Interspecific Interactions among the Aphid Parasitoid Aphidius colemani and the Aphidophagous gallmidge Aphidoletes aphidimyza. IOBC/WPRS Bulletin, 28: 83-86.
11. Fallahpour, F., Ghorbani1, R., Nassiri Mahallati, M. and Hosseini, M. 2015. Demographic Parameters of Lipaphis erysimi on Canola Cultivars under Different Nitrogen Fertilization Regimes. J. Agr. Sci. Tech., 17: 35-47.
12. Fordyce, J. A. and Agrawal, A. A. 2001. The Role of Plant Trichomes and Caterpillar Group Size on Growth and Defense of the Pipevine Swallowtail Battus philenor. J. Anim. Ecol., 70: 997-1005.
13. Gholami Moghaddam, S., Hosseini, M., Modarres Awal, M. and Allahyari, H. 2013. Effect of Leaf Surface Characteristics of Wheat Cultivars on Functional Response of Orius albidipennis (Reuter) to Barely Aphid Sipha maydis (Passerini). Biol. Control Pest. Plant Dis., 1: 73-85.
14. Helyer, N., Cattlin, N. D. and Brown, K. C. 2003. Biological Control in Plant Protection: a Color Handbook. Second Edition, Timber Press, 126 PP.
15. Hosseini, M., Ashouri, A., Enkegaard, A., Weisser, W. W., Goldansaz, SH., Nassiri Mahalati, M. and Sarraf Moayeri, H. R. 2010. Plant Quality Effects on Intraguild Predation between Orius laevigatus and Aphidoletes aphidimyza. Entomol. Exp. Appl., 135: 208-216.
16. Lucas, E. 2005. Intraguild Predation among Aphidophagous Predators. Eur. J. Entomol., 102: 351-364.
17. Lucas, E. and Brodeur, J. 1999. Oviposition Site Selection of the Predatory Midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environ. Entomol., 28: 622-627.
18. Madadi, H., Enkegaard, A., Brødsgaard, H. F., Kharrazi-Pakdel, A., Ashouri, A. and Mohaghegh-Neishabouri, J. 2008. Orius albidipennis (Heteroptera: Anthocoridae): Intraguild Predation of and Prey Preference for Neoseiulus cucumeris (Acari: Phytoseiidae) on Different Host Plants. Entomol. Fennica, 19: 1-9.
19. Manly, B. F. J. 1974. A Model for Certain Types of Selection Experiments. Biometrics, 30: 281-294.
20. Meyhöfer, R. and Hindayana, D. 2000. Effects of Intraguild Predation on Aphid Parasitoid Survival. Entomol. Exp. Appl., 97: 115-122.
21. Meyhöfer, R. and 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. Biol. Control, 25: 239-248.
22. Mottaghinia, L., Hassanpour, M., Razmjou, J., Hosseini, M. and Chamani, E. 2015. Functional Response of Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae) to Aphis gossypii Glover (Hemiptera: Aphididae): Effects of Vermicompost and Host Plant Cultivar. Neotrop. Entomol., doi 10.1007/s13744-015-0343-0.
23. Naranjo, S. E. 2007. Intraguild Predation on Eretmocerus sp. nr. emiratus, a Parasitoid of Bemisia tabaci, by Three Generalist Predators with Implications for Estimating the Level and Impact of Parasitism. Biosci. Technol., 17: 605-622.
24. Pineda, A., Morales, I., Marcos-Grarcia, M. A. and Fereres, A. 2007. Oviposition Avoidance of Pparasitized Aphid Colonies by the Syrphid Predator Episyrphus balteatus Mediated by Different Cues. Biol. Control, 42: 274-280.
25. Polis, G. A., Myers, C. A. and Holt, R. D. 1989. The Ecology and Evolution of Intraguild Predation: Potential Competitors that Eat Each Other. Annu. Rev. Ecol. Evol. Syst., 20: 297-330.
26. Royer, T. A., Giles, K. L., Lebusa, M. M. and Payton, M. E. 2008. Preference and Suitability of Greenbug, Schizaphis graminum (Hemiptera: Aphididae) Mummies Parasitized by Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) as Food for Coccinella septempunctata and Hippodamia convergens (Coleoptera: Coccinellidae). Biol. Control, 47: 82-88.
27. Schädler, M., Brandl, R. and Kempel, A. 2010. Host Plant Genotype Determines Bottom-up Effects in an Aphid-Parasitoid-Ppredator System. Entomol. Exp. Appl., 135: 162-169.
28. SPSS. 2007. SPSS Base 16.0 User’s Guide. SPSS Incorporation, Chicago, IL.
29. Snyder, W. E. and Ives, A. R. 2001. Generalist Predators Disrupt Biological Control by a Specialist Parasitoid. Ecol., 82: 705-716.
30. Snyder, W. E., Ballard, S. N., Yang, S., Clevenger, G. M., Miller, T. D., Ahn, J. J., Hatten, T. D. and Berryman A. A. 2004. Complementary Biocontrol of Aphids by the Ladybird Beetle Harmonia axyridis and the Parasitoid Aphelinus asychis on Greenhouse Roses. Biol. Control, 30: 229-235.
31. Styrsky, J. D., Kaplan, I. and Eubanks, M. D. 2006. Plant Trichomes Indirectly Enhance Tritrophic Interactions Involving a Generalist Predator, the Red Imported Fire Ant. Biol. Control, 36: 375-384.
32. Tahriri Adabi, S., Talebi, A. A., Fathipour, Y. and Zamani, A. A. 2010. Life History and Demographic Parameters of Aphis fabae (Hymenoptera: Aphididae) and Its Parasitoid, Aphidius matricariae (Hymenoptera: Aphididae) on Four Sugar Beet Cultivars. Acta Entomol. Serb., 15: 61-73.
33. Turlings, T. C. J. and Benrey, B. 1998. Effects of Plant Metabolites on the Behavior and Development of Parasitic Wasps. Ecosci., 5: 321-333.
34. van Lenteren, J. C. 2003. Commercial Availability of Biological Control Agents. In: “Quality Control and Production of Biological Control Agents: Theory and Testing Procedures”, (Ed.): van Lenteren, J. C. CABI, Cambridge, PP. 167-179.
35. Velasco-Hernandez, M. C., Ramirez-Romero, R., Cicero, L., Michel-Rios, C. and Desneux, N. 2013. Intraguild Predation on the Whitefly Parasitoid Eretmocerus eremicus by the Generalist Predator Geocoris punctipes: A Behavioral Approach. PLoS One, 8: e80679. doi:10.1371/journal.pone.0080679
36. White, C. and Eigenbrode, S. D. 2000. Leaf Surface Waxbloom in Pisum sativum Influences Predation and Intra-Guild Interactions between Two Predator Species. Oecologia, 124: 252-259.
37. Yukawa, J., Yamaguchi, D., Mizota, K. and Setokuchi, O. 1998. Distribution and Host Range of an Aphidophagous Species of Cecidomyiidae, Aphidoletes aphidimyza (Diptera), in Japan. Appl. Entomol. Zool., 33: 185-193.