Aphidophagous coccinellid and parasitoid species determined in the Çanakkale Province with a new record for the parasitoid fauna of Turkey

Abstract

This study was conducted between 2013 - 2015 to determine aphidophagous coccinellid and parasitoid species of aphids, their diversity and tritrophic associations (parasitoid/predator-host aphid-host plant) in the Çanakkale Province. In the course of the investigations, 10 species belonging to six genera of the subfamily Aphidiinae (Hymenoptera: Braconidae) were determined, in addition to 12 species belonging to 10 genera of the family Coccinellidae (Coleoptera). Among the parasitoids, Aphidius hortensis Marshall, 1896 is a new record for the Turkish parasitoid fauna. Lysiphlebus testaceipes (Cresson, 1880) (32.9%) and Lysiphlebus fabarum (Marshall, 1896) (23.0%) were more extensively found compared to other parasitoid species. Similarly, Coccinella septempunctata Linnaeus, 1758 (35.1%) and Adalia bipunctata (Linnaeus, 1758) (22.8%) were recorded as the most common predator species. Aphis fabae Scopoli 1763 had the greatest diversity among the parasitoids (Shannon-Wiener H = 0.658), while Cinara pini (Linnaeus, 1758) had the greatest diversity among the predators (Shannon-Wiener H = 1.386). As for tritrophic associations, 18 parasitoid-aphid associations on 14 host plants and 28 predator-aphid associations on 19 host plants were determined. The A. hortensis - Liosomaphis berberidis (Kaltenbach, 1843) association on Berberis sp. (Berberidaceae) is here newly recorded from Turkey. With the present study, the aphidophagous coccinellid and parasitoid species are determined for the first time in the Çanakkale Province of Turkey.

Keywords

• Aphid,coccinellid,parasitoid,Aphidius hortensis,Çanakkale

Türkiye parazitoit faunası için yeni bir kayıt ile birlikte Çanakkale ilinde belirlenen afidofag coccinellid ve parazitoit türler

Öz

Bu çalışma 2013 ve 2015 yılları arasında Çanakkale ilinde afidofag coccinellid ve parazitoit türleri ile onların çeşitlilikleri ve birbirleri arasındaki tritrofik ilişkilerin (parazitoit/predatör-konukçu yaprakbiti-konukçu bitki) belirlenmesi amacıyla yürütülmüştür. Çalışma boyunca Aphidiinae (Hymenoptera: Braconidae) altfamilyasına ait altı cinse bağlı 10 parazitoit tür ve Coccinellidae (Coleoptera) familyasına ait 10 cinse bağlı 12 predatör tür tespit edilmiştir. Parazitoit türlerden Aphidius hortensis Marshall, 1896 Türkiye parazitoit faunası için yeni kayıttır. Lysiphlebus testaceipes (Cresson, 1880) (%32.9) ve Lysiphlebus fabarum (Marshall, 1896) (%23.0) türleri diğer parazitoit türlerden daha yoğun tespit edilmiştir. Benzer şekilde Coccinella septempunctata Linnaeus, 1758 (%35.1) ve Adalia bipunctata (Linnaeus, 1758) (%22.8) türleri predatör türler içerisinde en yaygın türler olarak belirlenmiştir. Aphis fabae Scopoli 1763 parazitoit türlerin konukçusu olarak en yaygın çeşitliliğe (Shannon-Wiener H = 0.658) sahip iken Cinara pini (Linnaeus, 1758) ise predatör türlerin konukçusu olarak en yaygın çeşitliliğe sahiptir (Shannon-Wiener H = 1.386). Bu çalışmada 14 farklı konukçu bitki üzerinde 18 parazitoit-yaprakbiti ilişkisi ve 19 farklı bitki üzerinde 28 predatör-yaprakbiti ilişkisi belirlenmiştir. Berberis sp. (Berberidaceae) üzerinde A. hortensis - Liosomaphis berberidis (Kaltenbach, 1843) ilişkisi Türkiye'de ilk kez bu çalışma ile kayıt edilmiştir. Mevcut çalışma ile Çanakkale ilinde afidofag coccinellid ve parazitoit türler ilk kez tespit edilmiştir.

Anahtar Kelimeler

• Yaprakbiti,coccinellid,parazitoit,Aphidius hortensis,Çanakkale

References

1. Ashfaquae A. 2012. Taxonomic studies of family Coccinellidae (Coleoptera) of Giglgit-Baltistan, Pakistan. Department of plaant protection. Faculty of Crop Protection Sciences. The University of Agriculture, Peshawar. 196p.
2. Aslan B. and Karaca I. 2005. Fruit tree aphids and their natural enemies in Isparta region, Turkey. Journal of Pest Science, 78: 227-229.
3. Aslan M. M. and Uygun N. 2005. The aphidophagus coccinellid (Coleoptera: Coccinellidae) species in Kahramanmaraş, Turkey. Turkish Journal of Zoology, 29: 1-8.
4. Aslan M. M., Uygun N. and Starý P. 2004. A survey of aphid parasitoids in Kahramanmaras, Turkey (Hymenoptera: Braconidae: Aphidiinae; and Hymenoptera: Aphelinidae). Phytoparasitica, 32 (3): 255-263.
5. Audisio P. and Canepari C. 2016. Fauna Europaea: Coleoptera: Coccinellidae. Fauna Europaea version 2.6, (Web page: http://www.faunaeur.org) (Date accessed: September 2016).
6. Ayyıldız Y. and Atlıhan R. 2006. Balıkesir ili sebze alanlarında görülen yaprakbiti türleri ve doğal düşmanları.Yüzüncü Yıl Üniversitesi Ziraat Fakültesi Tarım Bilimleri Dergisi, 16 (1): 1-5.
7. Aziza M. El-G., Ahmed S. A., El-Bassioni M. N., Mahfouz H. M.and El-Deeb M. G. A. 2014. Survey of aphid species and their associated parasitoids and predators on wild plants in North Sinai Governorate, Egypt. Egyptian Journal of Biological Pest Control, 24 (2): 283-288.
8. Baştuğ G. and Kasap İ. 2015. Çanakkale ili Coccinellidae (Coleoptera) familyası üzerine faunistik çalışmalar. Türkiye Biyolojik Mücadele Dergisi, 6 (1): 41-50.

9. Bielawski R. 1975. Ergebnisse der zoologischen Forschungen von Dr. Z. Kaszab in der Mongolei Nr. 352. Coccinellidae V und VI. Fragmenta Faunistica 20 (16), 247-271.
10. Blackman R. L. and Eastop V. F. 2006. Aphids on the World’s Herbaceous Plants and Shrubs. Wiley & Sons Ltd., London, UK, 1439 pp.
11. Blackman R. L. and. Eastop V. F 2016. Aphids on the World's Plants: an Online Identification and Information Guide, http://www.aphidsonworldsplants.info (Date accessed: June 2016).
12. Bodenheimer F. S. and Swirski E. 1957. The Aphidoidea of the Middle East. Weizmann Science Press of Israel, Jerusalem, 378 pp.
13. Chinery M. 1993, Insects of Britain and Western Europe. Collins, London, 320 pp.
14. Darsouei R., Karimi J. and Modarres-Awal M. 2011. Parasitic wasps as natural enemies of aphid populations in the Mashhad region of Iran: New data from DNA barcodes and SEM. Archives of Biological Sciences, 63 (4):1225-1234.
15. Desneux N. Decourtye A. and Delpuech, J. M. 2007 The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81-106.
16. Desneux N., Pham-Dele`gue M. H. and Kaiser L. 2004. Effects of sublethal and lethal doses of lambda-cyhalothrin on oviposition experience and host searching behaviour of a parasitic wasp Aphidius ervi. Pest Management Science, 60: 381-389.
17. Desneux N., Denoyelle R. and Kaiser L. 2006. A multi-stepbioassay to assess the effect of deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere, 65: 1697-1706.
18. Fursch H. 1965. Die Palearktischen Arten der Scymnus-bipunctatus-Gruppe und die europaeschen Vertreter der Untergattung Sidis (Col. Cocc.). Mitt. Münch. Ent. Gesell. 55. Jahrg. 178-213.
19. Gilabert A., Simon J. C., Mieuzet L., Halkett F., Stoeckel S., Plantegenest M. and Dedryver C.A. 2009. Climate and agricultural context shape reproductive mode variation in an aphid crop pest. Molecular Ecology, 18 (14): 3050-3061.
20. Gordon R. D. 1985. The Coccinellidae of America North of Mexico. Journal of the New York Entomological Society, 93(1), 1-912.
21. Güncan A., Yoldaş Z. and Madanlar N. 2010. İzmir’de şeftali bahçelerinde bulunan yaprakbiti (Hemiptera: Aphididae) türleri ve doğal düşmanları üzerinde araştırmalar. Türkiye Entomoloji Dergisi, 34 (3): 399-408.
22. Güz N. and Kılınçer N. 2005. Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) on weeds from Ankara, Turkey. Phytoparasitica, 33 (4): 359-366.
23. Hagvar E. B. and Hofsvang T. 1991. Aphid parasitoids (Hymenoptera: Aphidiidae): biology, host selection and use in biological control. Biocontrol News and Information, 12: 13-41.
24. Heie O. E. 1986. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark (III), Family Aphididae: Subfamily Pterocommatinae & Tribe Aphidini of Subfamily Aphidinae. E.J. Brill/Scandinavian Science Press Ltd.,Leiden-Copenhagen, 314 pp.
25. Hille Ris Lambers D. 1950. On mounting aphids and other soft-skinned insects. Entomologische Berichten, XIII: 55-58.
26. Horion A. 1961. Faunistif der Mitteleuropäischen Käfer. Band VIII. Überlingen-Bodensee, Komissionsverlag Buchdruckerei Ang. Feysel., 283-365.
27. Hughes R. D. 1989. Biological control in the open field In: Minks A.K. & Harrewijn P. (eds.), Aphids, Their Biology, Natural Enemies and Control, Crop Pests, Vol. 2C, Elsevier, Amsterdam, 167-198 p.
28. Jouraeva, V. A., Johnson D. L., Hassett J. P., Nowak D. J., Shipunova N. A. and Barbarossa D. 2006. Role of sooty mold fungi in accumulation of fine-particle-associated PAHs and metals on deciduous leaves. Environmental Research, 102: 272-282.
29. Kavallieratos N.G. and Tomanović Ž. 2003. Some rare and endemic aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) from the Balkan Peninsula. Acta Entomologica Serbica, 6: 121-129.
30. Kavallieratos N. G., Athanassiou C. G. and Tomanović Ž. 2003. A new species and a key to Greek Praon Haliday (Hymenoptera: Braconidae: Aphidiinae). Deutsche Entomologische Zeitschrift, 50: 13-22.
31. Kavallieratos N.G., Athanassiou C.G., Tomanović Ž., Sciarretta A., Trematerra P. and Žikić V. 2005. Seasonal occurrence, distribution and sampling indices for Myzus persicae (Hemiptera: Aphidoidea) and its parasitoids (Hymenoptera: Braconidae: Aphidiinae) on tobacco. European Journal of Entomology, 102 (3): 459-68.
32. Kavallieratos N. G., Lykouressis D. P., Sarlis G. P., Stathas G. J., Segovia A. S. and Athanassiou C. G. 2001. The Aphidiinae (Hymenoptera: Ichneumonoidea: Braconidae) of Greece. Phytoparasitica, 29: 306-340.
33. Kavallieratos N. G., Tomanović Ž., Starý P., Athanassiou C. G., Sarlis G. P., Petrović O., Niketić M. and Veroniki M. A. 2004. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology, 39 (3): 527-563.
34. Kovar I. 2007. Coccinellidae, pp. 568-631. - In I. Löbl & A. Smetana (ed.): Catalogue of Palaearctic Coleoptera, Vol. 4. Stenstrup: Apollo Books, 935 pp.
35. Kök Ş., Kasap İ. and Özdemir I. 2016. Aphid (Hemiptera: Aphididae) species determined in Çanakkale province with a new record for the aphid fauna of Turkey. Turkish Journal of Entomology, 40 (4): 397-412.
36. Larson D. J. 2013. Key to Lady Beetles (Coleoptera: Coccinellidae) of Saskatchewan, http://www.entsocsask.ca/documents/insect_lists/Coccinellidae_key.pdf (Date accessed: June 2017).
37. Magro A., Lecompte E., Magne F., Hemptinne J. L. and Crouau-Roy B. 2010. Phylogeny of ladybirds (Coleoptera: Coccinellidae): Are the subfamilies monophyletic?. Molecular Phylogenetics and Evolution, 54: 833-848.
38. Ölmez S. and Ulusoy M.R. 2003. A survey of aphid parasitoids (Hymenoptera:Braconidae: Aphidiinae) in Diyarbakır, Turkey. Phytoparasitica, 31 (5): 524-528.
39. Poorani J. 2004. An annotated checklist of the Coccinellidae (Coleoptera) of Indian subregion, (Web page: http://www.angelfire.com/bug2/j_poorani/checklist.pdf) (Date accessed: June 2017).
40. Posada-Flórez F. J., Téllez-Farfán L., Simbaqueba R. and Serna F. 2014. Survey and bionomic observations of Siphaflava damaging kikuyo grass in two Colombian Sites. Revista U.D.C.A Actualidad & Divulgación Científica, 17 (1): 95-104.
41. Sharkey M. J. and Wharton R. A. 1997. Morphology and terminology. In: R. A.Wharton, P. M. Marsh, and M. J. Sharkey (eds.), Manual of the New World Genera of the Family Braconidae (Hymenoptera). Special Publication 1. International Society of Hymenopterists, Washington, DC, 19-37 pp.
42. Smith C. F. 1944. The Aphidiinae of North America. Ohio State University Contributions in Zoology and Entomology Entstitute, No: 6, 1-154 pp.
43. Starý P. 1970. Biology of Aphid Parasites (Hymenoptera: Aphidiidae) with respect to Integrated Control. Series Entomologica, Vol. 6. Dr. W. Junk, the Hague, the Netherlands, 656 pp.
44. Starý P. 1988. Aphidiidae. In: Minks, A. K. and Harrewijn, P. (eds.), Aphids: Their Biology, Enemies and Control. vol. 2B. Elsevier, Amsterdam, the Netherlands. 171-184 pp.
45. Starý P. 2006. Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae: Aphidiinae). Academia, Praha, 292 pp.
46. Şahbaz A. and Uysal M. 2006. Konya ilinde kavaklarda beslenen yaprakbitlerinin (Homoptera: Aphididae) predatör ve parazitoitleri. Selçuk Üniversitesi Ziraat Fakültesi Dergisi, 20 (38): 119-125.
47. Tezcan S. and Uygun N. 2003. İzmir ve Manisa yöresi ekolojik kiraz üretim bahçelerinde saptanan Coccinellidae (Coleoptera) türleri üzerinde bir değerlendirme. Turkiye Entomoloji Dergisi, 27 (1) : 73-79.
48. Tomanović Ž. & N.G. Kavallieratos 2002. Two new aphidiine wasps (Hymenoptera: Braconidae: Aphidiinae) from the southeastern Europe. Reichenbachia, 34: 341-345.
49. Tomanović Ž. and Starý P. 2001. Aphidius linosiphonis sp. n. (Hymenoptera: Braconidae: Aphidiinae), a new member of the aphid parasitoid guild associated with Galium. Zootaxa, 6: 1-4.
50. Tomanović Ž., Beyarslan A., Çetin Erdoğan Ö. and Žikić V. 2008. New records of aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) from Turkey. Periodicum Biologorum, 110 (4): 335-338.
51. Tomanović Ž., Kavallieratos N. G., Athanassiou C. G. and Petrović O. 2003b. A new Praon species (Hymenoptera: Braconidae: Aphidiinae) of the Uroleucon parasitoid complex from the Mediterranean area. Phytoparasitica, 31: 19-26.
52. Tomanović Ž., Kavallieratos N. G., Athanassiou C. G., Stanisavljević L. Z. 2003a. A review of the West Palaearctic Aphidiine (Hymenoptera: Braconidae: Aphidiinae) parasitic on Uroleucon spp. with a description of a new species. Annales Societe Entomologique de France, 39: 343-353.
53. Tomanović Ž., Starý P., Petrović O. 2002. Monoctonus leclanti sp. n. (Hymenoptera: Braconidae: Aphidiinae) from high montane areas of southeastern Europe and key to related species. Entomologica Fennica, 13: 159-162.
54. Uygun N. 1981. Türkiye Coccinellidae (Col.) Faunası üzerine taksonomik araştırmalar. Çukurova Üniversitesi Ziraat Fakültesi Yayınları, No:157, 110 pp. van Emden H. E. 1995. Host-plant-aphidophaga interactions. Agriculture, Ecosystems & Environment, 52 (1): 3-11.
55. van Emden H. F., Harrington R. 2007. Aphids as Crop Pests. CABI Publishing, London, 717 pp.
56. Yousof D. E., Mahmoud M.E.E, Mohamed A.H. 2013. Prospects of biological control of daten palm green pit scale insect Asterolecanium phoenicis Rao (Homoptera: Asterolecaniidae) in Sudan. Persian Gulf crop protection, 2(2), 42-48.
57. Yu D. S., van Achterberg K. and Horstmann K. 2012. World Ichneumonoidea 2011, Taxapad 2012, (Web page: http://www.taxapad.com/global.php) (Date accessed: September 2016).