Effects of single and simultaneous application of the parasitoid, Lysiphlebus fabarum and the ladybird beetle, Hippodamia variegata on control of Aphis gossypii on cucumber

Document Type : Research paper-Persian

Authors

1 Ph.D student, Shahid Chamran University of Ahvaz

2 Associate Professor, Shahid Chamran University of Ahvaz

3 Professor, Kansas State University

Abstract

Background and objectives
The cotton aphid, Aphis gossypii, is an important pest on greenhouse crops such as the cucumber. Natural enemies have often been used successfully to control greenhouse pests. Among different pests, aphids because of their high reproductive rate are particularly difficult to control biologically. 
Materials and Methods
In this study, the effects of separate and simultaneous application of the parasitoid wasp Lysiphlebus fabarum and the predator ladybird beetle Hippodamia variegata were studied to control A. gossypii on cucumber as an integrated pest management program. The replicates (n= 10) in all treatments included 10 cucumber plants in separate pots and were infected with five winged A. gossypii placed in a cage with a banker plant system of Vicia fabae-Aphis fabae. With the introduction of mummified aphids on a bean shoot (every two days), a pair of male and female adult ladybird beetles (every three days) or simultaneous application of both biocontrol agents, the numbers of aphids were counted in the three treatments.
Results
The results revealed that the parasitoid wasp L. fabarum alone was unable to control A. gossypii, but H. variegata performed better. The best performance was observed for simultaneous application of both biocontrol agents. Moreover, in the combined agents’ treatment, the number of A. gossypii on the both lower and upper cucumber leaves was not significantly different compare to other treatments that biological agentswere used seperatly. The number of mummified aphids did not differ between treatments at the end of the experiments. This is indicative of the tendency for ladybird beetles to feed on different growth stages of non-parasitized aphids compare to parasitized aphids containing immature stages of L. fabarum.
Discussion
The results indicate thatthe simultaneous application of both biocontrol agents is effective for the control of A. gossypii, although more research under greenhouse condition is needed.

Keywords


Acheampong, S., and Stark, J.D. 2007. Can reduced rates of pymetrozine and natural enemies control the cabbage aphid, Brevicoryne brassicae (Homoptera: Aphididae), on broccoli? International Journal of Pest Management, 50: 275-279.
Almasi, A., Rasekh, A., Esfandiari, M., Askari-Seyahooei, M., and Ziaee, M. 2017. Evaluation of efficiency the parasitoid wasp, Lysiphlebus fabarum (Hymenoptera: Braconidae), reared on Aphis fabae, against the melon aphid, Aphis gossypii. Journal of Applied Researches in Plant Protection, 6: 83-95. (in Farsi with English abstract).
Ameri, M., Rasekh, A., and Allahyari, H. 2014. Effect of different nymphal stages of Aphis fabae Scopoli on some biological features of thelytokous population of Lysiphlebus fabarum (Marshall). Plant Protection (Scientific Journal of Agriculture), 35 (4): 83-94. (in Farsi with English abstract). 
Astaraki, M., Rasekh, A., Shishehbor, P., and Mahi, H. 2018. Evaluation of the possibility of using banker plant (Vicia faba-Aphis fabae) to increase parasitism of Aphis gossypii by a parasitoid wasp, Lysiphlebus fabarum. Journal of BioControl in Plant Protection. Accepted. (in Farsi with English abstract). 
Bennison, J.A. 1992. Biological control of aphids on cucumbers: use of open rearing systems or "banker plants" to aid establishment of Aphidius matricariae and Aphidoletes aphidimyza. Mededelingen van de Faculteit Landbouwwetenschappen Universiteit Gent, 57/2b: 457-466.
Bink, F.A., Bink-Moenen, R.M., and Woets, J. 1980. Wittevliegen in Nederland (Homoptera; Aleyrodidae). Entomology Berlin,40: 3-9.
Blackman, R.L., and Eastop, V.F. 1984. Aphids on the world's crops: an identification guide. John Wiley & Sons, Chichester.
Cichocka, E., Goszczynski, W., and Chacinska, M. 1992. The effect of aphids on host plants. I. Effect on photosynthesis, respiration and transpiration. Aphids and Other Homopterous Insects 3: 59-64.
Farhadi, R., Allahyari, H., Rasekh, A., Aldaghi, M., and 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: 209-215. (in Farsi with English abstract).
Frazer, B.D. 1988. Predators. In Minks, A.K. & Harrewijn, P. (Eds.). Aphids: their biology, natural enemies and control. Volume B. Elsevier, Amsterdam, pp: 217-230.
Fritz, R. S. 1982. Selection for host modification by insect parasitoids. Evolution, 36: 283-288.
Hansen, L.S. 1983. Introduction of Aphidoletes aphidimyza (Rond.) (Diptera: Cecidomyiidae) from an open rearingsecondary parasitism in the banker plant system unit for the control of aphids in glasshouses. IOBC-WPRS Bulletin, 6: 146-150.
Hindayana, D., Meyhofer, R., Scholz, D., and Poehling, H.M. 2001. Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biological Control, 20: 236-246.
Jandricic, S.E., Dale, A.G., Bader, A., and Frank, S.D. 2014. The effect of banker plant species on the fitness of Aphidius colemani Viereck and its aphid host (Rhopalosiphum padi L.). Biological Control, 76: 28-35.
Kontodimas, D.C., and Stathas, G.J. 2005. Phenology, fecundity and life table parameters of thepredator Hippodamia variegata reared on Dysaphis crataegi. Biocontrol, 50 : 223-233.
Lucas, E., Coderre, D., and Brodeur, J. 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology, 79: 1084-1092.
Mahi, H., Rasekh, A., Michaud, J.P., and Shishehbor, P. 2014. The biology of Lysiphlebus fabarum (Braconidae, Aphidiinae) following cold storage of larvae and pupae. Entomologia Expermentalis et Applicata, 153: 10-19.
Mahmoudi, M., Sahragard, A., and Jalali Sendi, J. 2010. Foraging efficiency of Lysiphlebus fabarum Marshall (Hymenoptera: Aphidiidae) parasitizing the black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae), under laboratory conditions. Journal of Asia-pacific Entomology, 3(2): 111-116.
Mohammadi, Z., Rasekh, A., Kocheli, F., and Habibpour, B. 2016. The effect of different instars of black bean aphid, Aphis fabae (Hem.: Aphididae) on fitness of sexual population of Lysiphlebus fabarum (Hym.: Braconidae). Plant Protection (Scientific Journal of  Agriculture), 38 (4): 108-102. (in Farsi with English absract). 
Mossadegh, M.S., Stary, P., and Salehipour, H. 2011. Aphid parasitoids in a dry lowland area of Khuzestan, Iran (Hymenoptera, Braconidae, Aphidiinae). Asian Journal of Biological Sciences, 4: 175-181.
Prado, S.G., and Frank, S. 2014. Optimal foraging by an aphid parasitoid affects the outcome of apparent competition. Ecological Entomology, 39: 236-244.
Prado, S.G.S., Jandricic, E., and Frank, S.D. 2015. Ecological interactions affecting the efficacy of Aphidius colemani in greenhouse crops. Insects, 6: 538-575.
Provost, C., Coderre, D., Lucas, E., and Bostanian, N. J. 2003. Impacts of Lambda cyhalothrin on intraguild predation among three mite predators. Environmental Entomology, 32: 256-263.
Rakhshani, E., Talebi, A.A., Manzari, S., Rezwani, A., and 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: 1-14.
Rasekh, A., Kharazi-Pakdel, A., Michaud, J.P., Allahyari, H., and Rakhshani, E. 2011. Report of a thelytokous population of Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae) from Iran. Journal of Entomological Society of Iran, 30: 83-84.
Rasekh, A., Michaud, J.P., Allahyari H., and 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.
Rasekh A., Michaud, J.P., Mohseni, L., and Kocheili, F. 2018. An asexual strain of Lysiphlebus fabarum (Hymenoptera: Braconidae) gains fitness in superparasitised hosts, but a sexual strain pays costs. Ecological Entomology, 43: 93-101.
Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J., and Jaffee, B.A. 1995. Intraguild predation among biological-control agents: theory and practice. Biological Control, 5: 303-335.
Sadeghi, A. 1991. An investigation on the coccinellids fauna of alfalfa fields and determination of species at Karaj. M.Sc. Thesis, University of Tehran, Karaj, Iran (in Persian)
SPSS. 1998. SPSS 8.0 for Windows. Prentice Hall, Upper Saddle River, NJ, USA.
Stacey, D.L. 1977. ‘‘Banker’’ plant production of Encarsia formosa Gahan and its use in the control of glasshouse whitefly on tomatoes. Plant Pathology, 26: 63-66.
Stary, P. 1986. Specificity of parasitoids (Hymenoptera: Aphidiidae) to the black bean aphid Aphis fabae complex in agroecosystems. Acta Entomologica Bohemoslov, 83: 24-29.
Stary, P. 1988. Aphidiidae. In Minks, A.K., Harrewijn, P. (Eds.). Aphids: their biology, natural enemies and control. Volume B. Elsevier, Amsterdam, pp: 171-184.
Sunderland, K.D., Axelsen, J.A., Dromph, K., Freier, B., Hemptinne, J.L., Holst, N.H., Mols, P.J.M., Petersen, M.K., Powell, W., Ruggle, P., Triltsch, H., and Winder, L. 1997. Pest control by a community of natural enemies. Acta Jutlandica, 72: 271-326.
Toosi, M. 2016. Investigation on intraguild predation between ladybird, Hippodamia variegata and a parasitoid wasp, Lysiphlebus fabarum natural enemies of Aphis gossypii on cucumber plant. M.Sc. Thesis, Shahid Chamran University of Ahvaz, Ahvaz, Iran. 
Toosi, M., Rasekh, A., and Osawa, N. 2016. Intraguild predation by Hippodamia variegata (Col.: Coccinellidae) on the parasitoid wasp, Lysiphlebus fabarum (Hym.: Braconidae). Journal of Entomological Society of Iran, 36: 205-216. (in Farsi with English abstract).
Toosi, M., Rasekh, A., and Osawa, N. 2019. Effects of intraguild predation on the life history traits in the ladybird beetle Hippodamia variegata (Coleoptera: Coccinellidae) and its progeny. Bulletin of Insectology, (Submitted).
van Driesche, R.G., Lyon, S., Sanderson, J.P., Bennett, K.C., Stanek, E.J., and Zhang, R. 2008. Greenhouse trials of Aphidius colemani (Hymenoptera: Braconidae) banker plants for control of aphids (Hemiptera: Aphididae) in greenhouse spring floral crops. Florida Entomologist, 91: 583-591.
van Emden, H.F. 1988. The potential for managing indigenous natural enemies of aphids on field crops. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 318: 183-201.
van Lenteren, J.C., and Woets, J. 1988. Biological and integrated pest control in greenhouses. Annual Review of Entomology, 33: 239-269.
van Schelt, J. Douma, J.B., and Ravensberg, W.J. 1990. Recent developments in the control of aphids in sweet peppers and cucumbers. SROP-WPRS Bulletin, XIII/5: 190-193.
van Steenis, M. 1995. Evaluation and application of parasitoids for biological control of Aphis gossypii in glasshouse cucumber crops. Ph.D. Thesis, Wageningen University. Wageningen, Netherland.    
Yu, D.S., van Achterberg, C., and Horstmann, K. 2013. World Ichneumonoidea 2011. Taxonomy, Biology, Morphology and Distribution. Taxapad (Scientific Names for Information Management), Interactive Catalogue, Ottawa. Available on: http://www.taxapad.com.