<p><strong>Identification key, diversity and host associations of parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids attacking cereal crops in Egypt</strong></p>

NEVEEN S. GADALLAH; AHMED H. EL-HENEIDY; SAMAR M. MAHMOUD; NICKOLAS G. KAVALLIERATOS

doi:10.11646/zootaxa.4312.1.6

Issue: Vol. 4312 No. 1: 28 Aug. 2017

Type: Article

Published: 2017-08-28

DOI: 10.11646/zootaxa.4312.1.6

Page range: 143–154

Abstract views: 87

PDF downloaded: 2

Identification key, diversity and host associations of parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids attacking cereal crops in Egypt

NEVEEN S. GADALLAH⁺⁻
AHMED H. EL-HENEIDY⁺⁻
SAMAR M. MAHMOUD⁺⁻
NICKOLAS G. KAVALLIERATOS⁺⁻

Entomology Department, Faculty of Science, Cairo University, Cairo, Egypt.

Department of Biological Control, Plant Protection Research Institute, Agriculture Research Center, Giza, Egypt.

Laboratory of Agricultural Zoology and Entomology, Department of Crop Science, Agricultural University of Athens, Athens, Attica, Greece.

Hymenoptera Aphidiinae parasitoids aphids cereals Egypt

Requires Subscription or Fee PDF (7MB)

Abstract

In the present study, a total of eleven Aphidiinae parasitoid species belonging to six genera (Aphidius Nees, Binodoxys Mackauer, Diaeretiella Starý, Ephedrus Haliday, Lysiphlebus Foerster and Praon Haliday) were recorded from three aphid species [Rhopalosiphum maidis (Fitch), Rhopalosiphum padi (L.) and Sitobium avenae (F.)] feeding on four cereal plants (Avena sativa L., Hordeum vulgare L., Triticum aestivum L. and Zea mays L.) in Egypt. An illustrated key of the recorded aphidiines, the tritrophic (parasitoid-aphid-plant) associations and their distribution in the target area are also provided. Among the emerged parasitoids, Aphidius ervi Haliday is a new record for the fauna of Egypt. Aphidius transcaspicus Telenga and Binodoxys angelicae (Haliday) are reported for the first time to be associated with aphids infesting cereals in Egypt.

References

Abdel-Rahman, M.A.A. (2005) Ecological studies on cereal aphids and their control in Sohag governorate. Ph.D. Thesis, Faculty of Agriculture, Assiut University, Asyut, 171 pp.
Abdel-Rahman, M.A.A., Nasser, M.A.K. & Ali, A.M. (2000) The incidence of hymenopterous parasitoids attacking cereal aphids in wheat fields in Upper Egypt. Assiut Journal of Agricultural Science, 31, 317−328.
Alikahni, M., Rezwani, A., Starý, P., Kavallieratos, N.G. & Rakhshani, E. (2013) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) on cultivated and non-cultivated areas of Markazi province, Iran. Biologia, 68, 966−973.
https://doi.org/10.2478/s11756-013-0234-y
Barahoei, H.E., Rakhshani, E., Madjdzadeh, S.M., Alipour, A., Taheri, S., Nader, E., Rogdanović, A.M., Petrović-Obradović, O., Starý, P., Kavallieratos, N.G. & Tomanović, Ž. (2013) Aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) of central submountains of Iran. North-Western Journal of Zoology, 9, 70−93.
Barahoei, H., Rakhshani, E., Nader, E., Starý, P., Kavallieratos, N.G., Tomanović, Ž. & Mehrparvar, M. (2014) Checklist of Aphidiinae parasitoids (Hymenoptera, Braconidae, Aphidiinae) and their host aphid associations in Iran. Journal of Crop Protection, 3, 199−232.
Blackman, R.I. & Eastop, V.E. (2000) Aphids on the world’s crops. An identification guide. 2^nd Edition. John Wiley and Sons Ltd., Chichester, 466 pp.
Brewer, M.J. & Elliott, N.C. (2004) Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annual Review of Entomology, 49, 219−242.
https://doi.org/10.1146/annurev.ento.49.061802.123149
El-Fatih, M.M. (2006) Seasonal abundance and certain biological aspects on cereal aphids on barley in Egypt (Giza region). Ph.D. Thesis, Faculty of Agriculture, Cairo University, Giza, 146 pp.
El-Heneidy, A.H. (1991) Seasonal abundance of aphids and their natural enemies in wheat fields in Upper Egypt. Egyptian Journal of Biological Pest Control, 1 (1), 5−10.
El-Heneidy, A.H. (1994) Efficacy of aphidophagous insects against aphids at wheat fields in Egypt, A 5-year evaluation. Egyptian Journal of Biological Pest Control, 4, 113−123.
El-Heneidy, A.H & Abdel-Samad, S.S. (2001) Tritrophic interactions among Egyptian wheat plant, cereal aphids and natural enemies. Egyptian Journal of Biological Pest Control, 11, 119−125.
El-Heneidy, A.H. & Attia, A.A. (1988/1989) Evaluation to the role of parasitoids and predators associated with aphids in wheat fields, Egypt. Bulletin of Entomological Society of Egypt, Economic Series, 17, 137−147.
El-Heneidy, A.H., Gonzalez, D., Starý, P., Adly, D. & El-Kawas, M.A. (2001) A survey of primary and secondary parasite species of cereal aphids in wheat in Egypt. Egyptian Journal of Biological Pest Control, 11, 193−194.
El-Heneidy, A.H., Gozalez, D., Starý, P. & Adly, D. (2002) Significance of hyperparasitization of primary cereal aphid parasitoids in Egypt (Hymenoptera: Parasitica). Egyptian Journal of Biological Pest Control, 12, 109−114.
El-Heneidy, A.H., Agamy, E.A., El-Husseini, M.M. & Adly, D.D. (2003) Seasonal occurrence of the aphid parasitoid, Aphidius matricariae Haliday (Hymenoptera: Aphidiidae) in Egyptian wheat fields. Agricultural Research Journal, Suez Canal University, 2, 103−108.
El-Heneidy, A.H., Sobhy, H.M., Abd-El-Wahed, S.M.N. & Mikhail, W.Z.A. (2004) Biological aspects and life table analysis of cereal aphid species and their parasitoid, Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Egyptian Journal of Biological Pest Control, 14, 43−51.
El-Serafy, H.A. (1999) Population density of cereal aphids parasitoids and their role in suppressing cereal aphids on wheat plantations at Mansoura district. Archives of Phytopathology and Plant Protection, 32, 257−264.
https://doi.org/10.1080/03235409909383295
Ghanim, A. & El-Adl, M. (1983) Aphids infesting wheat and the effect of their predators in suppressing their populations in fields at Mansoura district. Egyptian Journal of Agricultural Science, Mansoura University, 8, 958−968.
Hafez, A.A. (1994) Increasing the role of biocontrol agents against cereal aphids infesting wheat in Qaluobia. Egyptian Journal of Biological Pest Control, 4, 57−71.
Halbert, S.E., Johnson, J.B., Graves, P.L., Marsh, P.M. & Nelson, D. (1996) Aphidius uzbekistanicus (Hymenoptera: Aphidiinae) established in Idaho. Pan Pacific Entomology, 2, 13−16.
Hassan, M.S. (1963) Natural enemies of some root aphids in Egypt. G.O., Govt. printing Offices 5204-1963-1000ex, 22 pp.
Havelka, J., Tomanović, Ž., Kavallieratos, N.G., Rakhshani, E., Pons, X., Pike, K.S. & Starý, P. (2012) Review and key to the world parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Aphis ruborum (Hemiptera: Aphididae) and its role as a host reservoir. Annals of the Entomological Society of America, 105, 386−394.
https://doi.org/10.1603/an11108
Ibrahim, A.M.A. (1990a) Corn leaf aphid, Rhopalosiphum maidis (F.) (Hom., Aphididae) on wheat and associated primary parasitoids and hyperparasitoids. Bulletin of Entomological Society of Egypt, 69, 149−157.
Ibrahim, A.M.A. (1990b) Population dynamics of bird cherry-aphid, Rhopalosiphum padi L. (Hom.: Aphididae) and its primary parasiotids and hyperparasitoids association on wheat in Egypt. Bulletin of the Entomological Society of Egypt, 69, 137−147.
Ibrahim, A.M.A. & Afifi, A.I. (1991) The relationship between cereal aphids and aphidophagous syrphids, coccinellids and chrysopids on wheat and barley in Egypt. Bulletin of the Faculty of Agriculture, Cairo University, 42 (1), 151−166.
Kavallieratos, N.G., Tomanović, Ž., Starý, P., Athanassiou, C.G., Sarlis, G.P. & Petrović, O. (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology, 39, 527−563.
https://doi.org/10.1303/aez.2004.527
Kavallieratos, N.G., Tomanović, Ž., Starý, P., Athanassiou, C.G., Fasseas, C., Petrović, O., Stanisavljević, L.Ž. & Anagnou Veroniki, M. (2005) Praon Haliday (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe: key, host range, and phylogenetic relationship. Zoologischer Anzeiger, 243, 181−209.
https://doi.org/10.1016/j.jcz.2004.11.001
Kavallieratos, N.G., Tomanović, Ž., Starý, P. & Mitrovski Bogdanović, A. (2008) Parasitoids (Hymenoptera: Braconidae: Aphidiinae) attacking aphids feeding on Prunoideae and Maloideae crops in southeast Europe: aphidiine-aphid-plant associations and key. Zootaxa, 1793, 47−64.
Kavallieratos, N.G., Tomanović, Ž., Petrović, A., Janković, M., Starý, P., Yovkova, M. & Athanassiou, C.G. (2013) Review and key for the identification of parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids infesting herbaceous and shrubby ornamental plants in southeastern Europe. Annals of the Entomological Society of America, 106, 294−309.
https://doi.org/10.1603/an12090
Kavallieratos, N.G., Tomanović, Ž., Petrović, A., Kocić, K., Janković, M. & Starý, P. (2016) Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids feeding on ornamental trees in southeastern Europe: key for identification and tritrophic associations. Annals of the Entomological Society of America, 109, 473−487.
https://doi.org/10.1093/aesa/saw003
Kos, K., Petrović, A., Starý, P., Kavallieratos, N.G., Ivanović, A., Toševski, I., Jakše, J., Trdan, S. & Tomanović, Ž. (2011) On the identity of the cereal aphid parasitoid wasps Aphidius uzbekistanicus, Aphidius rhopalosiphi and Aphidius avenaphis (Hymenoptera: Braconidae: Aphidiinae) by examination of the COI mitochondrial gene, genometric morphometrics and morphology. Annals of the Entomological Society of America, 104, 1221−1232.
https://doi.org/10.1603/an11055
Lozier, J.D., Rederick, G.K. & Mills, N.J. (2008) Evolutionary significance units in natural enemies: identifying regional populations of Aphidius transcaspicus (Hymenoptera: Braconidae) for use in biological control of mealy plum aphid. Biological Control, 46, 532−541.
https://doi.org/10.1016/j.biocontrol.2008.05.002
Lumbierres, B., Pons, X. & Starý, P. (2004) Parasitoids and predators of aphids associated with public green areas of Lleida (NE Iberian Peninsula). Advances in Horticultural Science, 19, 69−75.
Megahed, H.E.A. (2000) Studies on aphids. Ph.D. Thesis, Faculty of Agriculture, Zagazig University, Zagazig, 206 pp.
Mills, N.V. (2002) Prune aphids: fall migration, biological control, and impact on prune production 2001. Prune Research Reports, California Prune Board, Sacramento, CA, 13 pp. [pp. 18−30]
Nazari, Y., Zamani, A.A., Masoumi, S.M., Rakhshani, E., Petrović-Obradović, O., Tomanović, S., Starý, P. & Tomanović, Ž. (2012) Diversity and host associations of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in the farmlands of western Iran. Acta Entomologica Musei Nationalis Pragae, 52, 559−584.
Pons, X. & Starý, P. (2003) Spring aphid-parasitoid (Homoptera: Aphididae, Hymenoptera: Braconidae) association and interactions in a Mediterranean arable crop ecosystem, including Bt maize. Journal of Pest Science, 76, 133−138.
https://doi.org/10.1007/s10340-003-0003-8
Pons, X., Lumbierres, B., Antoni, R. & Starý, P. (2011) Parasitoid complex of alfalfa aphids in an IPM intensive crop system in northern Catalonia. Journal of Pest Science, 84, 437−445.
https://doi.org/10.1007/s10340-011-0383-0
Prado, S.G., Jandricic, S.E. & Frank, S.D. (2015) Ecological interactions affecting the efficacy of Aphidius colemani in greenhouse crops. Insects, 6, 538−575.
https://doi.org/10.3390/insects6020538
Rakhshani, E., Tomanović, Ž., Starý, P., Talebi, A.A., Kavallieratos, N.G., Zamani, A.A. & Stamenković, S. (2008) Distribution and diversity of wheat aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Iran. European Journal of Entomology, 105, 863−870.
https://doi.org/10.14411/eje.2008.114
Rakhshani, E., Kazemzadeh, S., Starý, P., Barahoei, H., Kavallieratos, N.G., Ćetković, A., Popović, A., Bodlah, I. & Tomanović, Ž. (2012) Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northeastern Iran: aphidiine-aphid-plant associations, key and description of a new species. Journal of Insect Science, 12, 143.
https://doi.org/10.1673/031.012.14301
Schmidt, M.H., Lauer, A., Purtauf, T., Thies, C., Schaefer, M. & Tscharntke, T. (2003) Relative importance of predators and parasitoids for cereal aphid control. Proceedings of the Royal Society B: Biological Sciences, 270, 1905−1909.
https://doi.org/10.1098/rspb.2003.2469
Sharkey, M.J. & Wharton, R.A. (1997) Morphology and terminology. In: Wharton, R.A., Marsh, P.M. & Sharkey, M.J. (Eds.), Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication 1. International Society of Hymenopterists, Washington, D.C., pp. 19−37.
Slman, F.A.A. (2006) Incidence of cereal aphids and seasonal abundance of their parasitoids in wheat fields in Sohag (Upper Egypt). Assiut Journal of Agricultural Science, 37, 211−220.
Sobhy, H.M., El-Heneidy, A.H., Abd-El-Wahed, S.M.N. & Mikhail, W.Z.A. (2004) Seasonal occurrence of aphid parasitoids, Aphidius colemani Viereck (Hymenoptera: Aphidiidae) in the Middle Delta, Egypt. Egyptian Journal of Biological Pest Control, 14, 213−216.
Starý, P. (1964) Integrated control problems of citrus and peach aphid pests in Italy orchards. Entomophaga, 9, 147–152.
https://doi.org/10.1007/BF02376736
Starý, P. (1966) A review of the parasites of aphids associated with Prunus trees in Czechoslovakia (Hymenoptera: Aphidiidae, Homoptera: Aphidoidea). Acta Entomologica Bohemoslovaca, 63, 67–75.
Starý, P. (1970) Biology of aphid parasites (Hymenoptera: Aphidiidae) with respect to integrated control. Dr. W. Junk, The Hague, 643 pp.
Starý, P. (1972) Relative abundance of parasite species as an area-dependent phenomenon and its possible significance in biological control (Hymenoptera: Aphidiidae). Bolletino del Laboratorio di Entomologia Agraria “Filippo Silvestri” Portici, 30, 19−27.
Starý, P. (1976) Aphid parasites (Hymenoptera: Aphidiidae) of the Mediterranean area. Dr. Junk, B.V., The Hague, 95 pp.
https://doi.org/10.1007/978-94-010-1561-5
Starý, P. (1981) Biosystematic synopsis of parasites on cereal aphids in the Western Palaearctic (Hymenoptera: Aphidiinae, Homoptera: Aphidoidea). Acta Entomologica Bohemoslovaca, 78, 382−396.
Starý, P. & Pike, K.S. (1998) Uses of beneficial insect diversity in agroecosystem management. In: Collins, W.W. & Qualset, C.O. (Eds.), Biodiversity in agroecosystems, Advances in Agroecology Series. CRC Press, Boca Raton, FL, pp. 49–67.
https://doi.org/10.1201/9781420049244.ch4
Starý, P. & Havelka, J. (2008) Fauna and associations of aphid-parasitoids in an up-dated farmland area (Czech Republic). Bulletin of Insectology, 61, 251−276.
Tomanović, Ž., Kavallieratos, N.G., Starý, P., Petrović-Obradović, O., Athanassiou, C.G. & Stanisavljević, L. (2008) Cereal aphids (Hemiptera: Aphidoidea) in Serbia: seasonal dynamics and natural enemies. European Journal of Entomology, 105, 495−501.
https://doi.org/10.14411/eje.2008.064
Tomanović, Ž., Petrović, A., Starý, Kavallieratos, N.G., Žikić, V. & Rakhshani, E. (2009a) Ephedrus Haliday (Hymenoptera: Braconidae: Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomologica Serbica, 14, 39−53.
Tomanović, Ž., Kavallieratos, N.G., Starý, P., Stanisavljević, L.Ž., Četković, A., Stamenković, S., Jovanović, S. & Athanassiou, C.G. (2009b) Regional tritrophic relationship patterns of five aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) in agroecosystem-dominated landscapes of southeastern Europe. Journal of Economic Entomology, 102, 836−854.
https://doi.org/10.1603/029.102.0302
Tomanović, Ž., Starý, P., Kavallieratos, N.G., Gagić, V., Plećaŝ, M., Janković, M., Rakhshani, C., Ćetković, A. & Petrović, A. (2012) Aphid parasitoid (Braconidae: Aphidiinae) in wetland habitats in western Palaearctic: key and associated aphid parasitoid gilds. Annales de la Société Entomologique de France, 48, 189−198.
https://doi.org/10.1080/00379271.2012.10697763
Tomanović, Ž., Kos, K., Petrović, A., Starý, P., Kavallieratos, N.G., Žikić, V., Jakše, J., Trdan, S. & Ivanović, A. (2013) The relationship between molecular variation and variation in the wing shape of three aphid parasitoid species: Aphidius uzbekistanicus Luzhetzki, Aphidius rhopalosiphi De Stefani Perez and Aphidius avenaphis (Fitch) (Hymenoptera: Braconidae: Aphidiinae). Zoologischer Anzeiger, 252, 41−47.
https://doi.org/10.1016/j.jcz.2012.03.003
Tomanović, Ž., Petrović, A., Mitrović, M., Kavallieratos, N.G., Starý, P., Rakhshani, E., Rakhshanipour, M., Popović, A., Shukshuk, A.H. & Ivanović, A. (2014) Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bulletin of Entomological Research, 104, 552−565.
https://doi.org/10.1017/s0007485314000327
Viswanathan, P.R.K. (1972) New record of Aphidius transcaspicus Telenga (Braconidae: Hymenoptera) as a parasitic of Rhopalosiphum maidis (Fitch). Indian Journal of Entomology, 34, 74.
Wang, X.G. & Messing, R.H. (2006) Potential host range of the newly introduced aphid parasitoid Aphidius transcaspicus (Hymenoptera: Braconidae) in Hawaii. Proceedings of Hawaiian Entomological Society, 38, 81−86.
Zuñiga, E. (1987) Biological control of cereal aphids in the Southern Cone of South America. In: Burnett, P.A. (Ed.), World perspectives on barley yellow dwarf. Proceedings of the International Workshop, 6–11 July 1987, Udine, Italy, pp. 362–367.