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Foraging behavior of Aphidius matricariae (Hymenoptera: Braconidae) on tobacco aphid, Myzus persicae nicotianae (Hemiptera: Aphididae)

Published online by Cambridge University Press:  10 April 2019

M. Rezaei ,
A.A. Talebi Open the ORCID record for A.A. Talebi [Opens in a new window] ,
Y. Fathipour ,
J. Karimzadeh  and
M. Mehrabadi
M. Rezaei
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box 14115-336 Tehran, Iran
A.A. Talebi*
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box 14115-336 Tehran, Iran
Y. Fathipour
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box 14115-336 Tehran, Iran
J. Karimzadeh
Affiliation:
Department of Plant Protection, Isfahan Research and Education Center for Agriculture and Natural Resources, AREEO, Isfahan, Iran
M. Mehrabadi
Affiliation:
Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, P.O. Box 14115-336 Tehran, Iran
*
*Author for correspondence Phone: 98 21 4480481 Fax: 98 21 44196524 E-mail: talebia@modares.ac.ir, aliasghar.talebi@gmail.com
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Abstract

The aim of this study was to investigate the foraging behavior of Aphidius matricariae (Haliday) (Hymenoptera: Braconidae) as a biological control agent of Myzus persicae nicotianae Blackman (Hemiptera: Aphididae), a key and cosmopolitan pest of tobacco fields. To achieve a strategy for the control of this pest and a mass-rearing program of the parasitoid, host stage preference, switching, functional response, and mutual interference of A. matricariae were investigated at 25 ± 1°C, 70 ± 5% RH and 16:8 h L:D photoperiod. The parasitoid showed a preference for third- and fourth-instar nymphs of tobacco aphid in both choice and no-choice experiments. Using the Murdach's model, switching behavior was observed in A. matricariae between different density proportions of third- and fourth-instar nymphs. Further, the parasitoid exhibited a type II functional response when it was offered to third-instar nymphs of M. persicae nicotianae at six densities (2, 4, 8, 16, 32, and 64). Based on the linear regression analysis, there was a significance difference between the logarithm of per capita searching efficiency and the logarithm of parasitoid density. As the wasp density increased, per capita searching efficiency decreased. The result of this study revealed that A. matricariae is an effective agent in the integrated management of M. persicae nicotianae. In addition, application of these results can be important in mass-rearing program of A. matricariae.

Keywords

preferenceswitchingfunctional responsemutual interferencemass rearingbiocontrol
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 109 , Issue 6 , December 2019 , pp. 840 - 848
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Copyright
Copyright © Cambridge University Press 2019 

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References

Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World's Herbaceous Plants and Shrubs. Chichester, USA, John Wiley & Sons.Google Scholar
Brown, D. & Rothery, P. (1993) Models in Biology: Mathematics, Statistics and Computing. Chichester, USA, John Wiley & Sons.Google Scholar
Byeon, Y.W., Tuda, M., Kim, J.H. & Choi, M.Y. (2011) Functional responses of aphid parasitoids, Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae). Biocontrol Science and Technology 21, 57–70.Google Scholar
Cornell, H. & Pimentel, D. (1978) Switching in the parasitoid Nasonia vitripennis and its effects on host competition. Ecology 59, 297–308.Google Scholar
De Clercq, P., Mohaghegh, J. & Tirry, L. (2000) Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biological Control 18, 65–70.Google Scholar
Farhad, A., Talebi, A.A. & Fathipour, Y. (2011) Foraging behavior of Praon volucre (Hymenoptera: Braconidae) a parasitoid of Sitobion avenae (Hemiptera: Aphididae) on wheat. Psyche: A Journal of Entomology 2011, 1–7.Google Scholar
Fathipour, Y & Maleknia, B. (2016) Mite predators. Ecofriendly Pest Management for Food Security San Diego, USA, Elsevier. Management for Food Security San Diego, USA, Elsevier, pp. 329–366.Google Scholar
Fathipour, Y., Hosseini, A., Talebi, A.A. & Moharramipour, S. (2006) Functional response and mutual interference of Diaeretiella rapae (Hymenoptera: Aphidiidae) on Brevicoryne brassicae (Homoptera: Aphididae). Entomologica Fennica 17, 90–97.Google Scholar
Field, L.M., Javed, N., Stribley, M.F. & Devonshire, A.L. (1994) The peach-potato aphid Myzus persicae and the tobacco aphid Myzus nicotianae have the same esterase-based mechanisms of insecticide resistance. Insect Molecular Biology 3, 143–148.Google Scholar
Free, C.A., Beddington, J.R. & Lawton, J.H. (1977) On the inadequacy of simple models of mutual interference for parasitism and predation. Journal of Animal Ecology 46, 543–554.Google Scholar
Hart, J.T., De Jonge, J., Colle, C., Dicke, M., van Lenteren, J.C. & Ramakers, P. (1978) Host selection, host discrimination and functional response of Aphidius matricariae Haliday (Hymenoptera: Braconidae), a parasite of the green peach aphid, Myzus persicae (Sulz.). Meded Fac Landbouwwet Univ Gent 43, 441–453.Google Scholar
Hassell, M.P. (1971) Mutual interference between searching insect parasites. Journal of Animal Ecology 40, 473–486.Google Scholar
Hassell, M.P. & Varley, G.C. (1969) New inductive population model for insect parasites and its bearing on biological control. Nature 223, 1133–1137.Google Scholar
He, X.Z., Wang, Q. & Teulon, D.A.J. (2005) Host stage preference and reproductive fitness of Aphidius eadyi (Hymenoptera: Aphidiidae) on Acyrthosiphon pisum (Hemiptera: Aphididae). New Zealand Journal of Agricultural Research 48, 157–163.Google Scholar
Heidarian, M., Fathipour, Y. & Kamali, K. (2012) Functional response, switching, and prey-stage preference of Scolothrips longicornis (Thysanoptera: Thripidae) on Schizotetranychus smirnovi (Acari: Tetranychidae). Journal of Asia-Pacific Entomology 15, 89–93.Google Scholar
Holling, C.S. (1959) Some characteristics of simple types of predation and parasitism. Canadian Entomologist 91, 385–398.Google Scholar
Jervis, M. & Kidd, N. (1996) Insect Natural Enemies, Practical Approaches to Their Study and Evaluation. London, UK, Chapman & Hall.Google Scholar
Jokar, M., Zarabi, M., Shahrokhi, S. & Rezapanah, M. (2012) Host-stage preference and functional response of aphid parasitoid Diaeretiella rapae (McIntosh) (Hym.: Braconidae) on greenbug, Schizaphis graminum (Rondani) (Hem: Aphididae). Archives of Phytopathology and Plant Protection 45, 2223–2235.Google Scholar
Juliano, S.A. (2001) Nonlinear curve fitting: predation and functional response curves. pp. 178–196 in Cheiner, S.M. & Gurven, J. (Eds) Design and Analysis of Ecological Experiments. New York, Chapman & Hall.Google Scholar
Katsarou, I., Margaritopoulos, J.T., Tsitsipis, J.A., Perdikis, D.C. & Zarpas, K.D. (2005) Effect of temperature on development, growth and feeding of Coccinella septempunctata and Hippodamia convergens reared on the tobacco aphid, Myzus persicae nicotianae. Biocontrol 50, 565–588.Google Scholar
Khodayari, S., Fathipour, Y. & Sedaratian, A. (2016) Prey stage preference, switching and mutual interference of Phytoseius plumifer (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae). Systematic and Applied Acarology 21, 347–355.Google Scholar
Lin, L.A. & Ives, A.R. (2003) The effect of parasitoid host-size preference on host population growth rates: an example of Aphidius colemani and Aphis glycines. Ecological Entomology 28, 542–550.Google Scholar
Lykouressis, D.P. & Mentzos, G.V. (1995) Effects of biological control agents and insecticides on the population development of Myzus nicotianae Blackman (Homoptera: Aphididae) on tobacco. Agriculture, Ecosystems & Environment 52, 57–64.Google Scholar
Margaritopoulos, J.T., Shigehara, T., Takada, H. & Blackman, R.L. (2007) Host-related morphological variation within Myzus persicae group (Homoptera: Aphididae) from Japan. Applied Entomology and Zoology 42, 329–335.Google Scholar
Montoya, P., Liedo, P., Benrey, B., Barrera, J.F., Cancino, J. & Aluja, M. (2000) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 93, 47–54.Google Scholar
Murdoch, W.W. (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecological Monographs 39, 335–354.Google Scholar
Murdoch, W.W. & Marks, J.R. (1973) Predation by coccinellid beetles: experiments on switching. Ecology 54, 160–167.Google Scholar
Murdoch, W.W., Avery, S. & Smyth, M.E.B. (1975) Switching in predatory fish. Ecology 56, 1094–1105.Google Scholar
Nachman, G. & Skovga, H. (2015) Effect of mutual interference on the ability of Spalangia cameroni (Hymenoptera: Pteromalidae) to attack and parasitize pupae of Stomoxys calcitrans (Diptera: Muscidae). Environmental Entomology 44, 1076–1084.Google Scholar
Nicholson, A.J. (1933) Supplement: the balance of animal populations. Journal of Animal Ecology 2, 131–178.Google Scholar
Pasandideh, A., Talebi, A.A., Hajiqanbar, H. & Tazerouni, Z. (2015) Host stage preference and age-specific functional response of Praon volucre (Hymenoptera: Braconidae, Aphidiinae) a parasitoid of Acyrthosiphon pisum (Hemiptera: Aphididae). Journal of Crop Protection 4, 563–575.Google Scholar
Perdikis, D.C., Lykouressis, D.P., Garantonakis, N.G. & Iatrou, S.A. (2004) Instar preference and parasitization of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) by the parasitoid Aphidius colemani (Hymenoptera: Aphidiidae). European Journal of Entomology 101, 333–336.Google Scholar
Poncio, S., Montoya, P., Cancino, J. & Nava, D.E. (2016) Determining the functional response and mutual interference of Utetes anastrephae (Hymenoptera: Braconidae) on Anastrepha obliqua (Diptera: Tephritidae) Larvae for mass rearing purposes. Annals of the Entomological Society of America 109, 518–525.Google Scholar
Rakhshani, E., Talebi, A.A., Kavallieratos, N. & Fathipour, Y. (2004) Host stage preference, juvenile mortality and functional response of Trioxys pallidus (Hymenoptera: Braconidae, Aphidiinae). Biologia 59, 197–204.Google Scholar
Reed, T.D. & Semtner, P.J. (1992) Effects of tobacco aphid (Homoptera: Aphididae) populations on flue-cured tobacco production. Journal of Economic Entomology 85, 1963–1971.Google Scholar
Rezaei, M., Karimzadeh, J. & Shakarami, J. (2014) The influences of space and plant-host biomass on some biological key factors of Cotesia vestalis in mass-rearing conditions. Journal of Entomology and Zoology Studies 2, 31–34.Google Scholar
Rezaei, M., Karimzadeh, J. & Shakarami, J. (2018) Size of interacting resource-host-parasitoid populations influences mass rearing of Cotesia vestalis. Journal of the Entomological Research Society 20, 23–32.Google Scholar
Rogers, D. (1972) Random search and insect population models. Journal of Animal Ecology 41, 369–383.Google Scholar
SAS Institute, (2003) GLM: A Guide to Statistical and Data Analysis, version 9.1. SAS Institute, Cary, NC, USA.Google Scholar
Stacconi, V.R.M., Buffington, M., Daane, K.M., Dalton, D.T., Grassi, A., Kaçar, G., Miller, B., Miller, J.C., Baser, N., Ioriatti, C., Walton, V.M., Wiman, N.G., Wang, X. & Anfora, G. (2015) Host stage preference, efficacy and fecundity of parasitoids attacking Drosophila suzukii in newly invaded areas. Biological Control 84, 28–35.Google Scholar
Stary, P. (1988) Aphidiidae. pp. 171–184 in Aphids, Their Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.Google Scholar
Tahriri, S., Talebi, A.A., Fathipour, Y. & Zamani, A.A. (2007) Host stage preference, functional response and mutual interference of Aphidius matricariae (Hym.: Braconidae: Aphidiinae) on Aphis fabae (Hom.: Aphididae). Entomological Science 10, 323–331.Google Scholar
Takalloozadeh, H.M., Kamali, K., Talebi, A.A. & Fathipour, Y. (2005) Alfalfa Black Aphid, Aphis craccivora Koch (Hom. Aphididae) stage preference by Lysiphlebus fabarum Marshall (Hym. Aphidiidae). Journal of Science and Technology of Agriculture and Natural Resources 7, 225–233.Google Scholar
Talebi, A.A., Zamani, A.A., Fathipour, Y., Baniameri, V., Kheradmand, K. & Haghani, M. (2006) Host stage preference by Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae) as parasitoids of Aphis gosoypii (Hemiptera: Aphididae) on greenhouse cucumber. IOBC-WPRS Bulletin 29, 181.Google Scholar
Talebi, A.A., Rakhshani, E., Fathipour, Y., Starý, P., Tomanović, Ž & Rajabi-Mazhar, N. (2009) Aphids and their parasitoids (Hym., Braconidae: Aphidiinae) associated with medicinal plants in Iran. International Journal of Agricultural Sustainability 3, 205–219.Google Scholar
Tazerouni, Z., Talebi, A.A. & Rakhshani, E. (2011) The foraging behavior of Diaeretiella rapae (Hymenoptera: Braconidae) on Diuraphis noxia (Hemiptera: Aphididae). Archives of Biological Sciences 63, 225–234.Google Scholar
Tazerouni, Z., Talebi, A.A., Fathipour, Y. & Soufbaf, M. (2016 a) Interference competition between Aphidius matricariae and Praon volucre (Hymenoptera: Braconidae) attacking two common aphid species. Biocontrol Science and Technology 26, 1552–1564.Google Scholar
Tazerouni, Z., Talebi, A.A., Fathipour, Y. & Soufbaf, M. (2016 b) Age-specific functional response of Aphidius matricariae and Praon volucre (Hymenoptera: Braconidae) on Myzus persicae (Hemiptera: Aphididae). Neotropical Entomology 45, 642–651.Google Scholar
Van Den Bosch, R., Hom, R., Matteson, P., Frazer, B., Messenger, P. & Davis, C. (1979) Biological control of the walnut aphid in California: impact of the parasite, Trioxys pallidus. California Agriculture 47, 1–13.Google Scholar
Van Emden, H.F. & Harrington, R. (2007) Aphids as Crop Pests. Wallingford, CABI Publishing.Google Scholar
Van Lenteren, J.C. & Bakker, K. (1977) Behavioural aspects of the functional responses of a parasite (Pseudeucoila bochei Weld) to its host (Drosophila melanogaster). The Netherlands Journal of Zoology 28, 213–233.Google Scholar
Vucetic, A., Petrovic-Obradovic, O. & Stanisavljevic, L.Z. (2010) The morphological variation of Myzus persicae (Hemiptera: Aphididae) from peach and tobacco in Serbia and Montenegro. Archives of Biological Sciences 62, 767–774.Google Scholar
Yang, X.-B., Campos-Figueroa, M., Silva, A. & Henne, D.C. (2015) Functional response, prey stage preference, and mutual interference of the Tamarixia triozae (Hymenoptera: Eulophidae) on tomato and bell pepper. Journal of Economic Entomology 108, 414–424.Google Scholar
Yazdani, M. & Keller, M. (2016) The shape of the functional response curve of Dolichogenidea tasmanica (Hymenoptera: Braconidae) is affected by recent experience. Biological Control 97, 63–69.Google Scholar
Zamani, A., Talebi, A., Fathipour, Y. & Baniameri, V. (2006) Temperature-dependent functional response of two aphid parasitoids, Aphidius colemani and Aphidius matricariae (Hymenoptera: Aphidiidae), on the cotton aphid. Journal of Pest Science 79, 183–188.Google Scholar