Biyolojik Mücadelede Kullanılan Entomopatojenlerin Arılar Üzerine Etkileri

Öz

Böceklerde hastalık oluşturan organizmalara entomopatojen denir. Entomopatojenler, virüs, bakteri, protist, fungus ve nematodları içeren geniş bir mikroorganizma grubundan oluşur. Zararlı böcekler ile biyolojik mücadelede çevreye yan etkisi olmayan entomopatojenik organizmaların kullanımı her geçen gün daha popüler hale gelmektedir. Her ne kadar yan etkileri düşük olsa da uygulandıkları alanda bal arıları üzerine etkileri her zaman dikkat çeken konu olmuştur. Literatürde entomopatojenik organizmaların arılar üzerindeki etkileri ile ilgili oldukça fazla çalışma mevcuttur. Ülkemizde yeni yeni kullanılan entomopatojenlerin bal arıları üzerindeki etkisi her zaman tartışılacaktır. Bu derleme makalede, entomopatojenik organizmaların arılar üzerine etkileri ele alınarak, literatür desteğiyle birlikte detaylı bir şekilde irdelenmektedir.

Anahtar Kelimeler

• Bal arısı,Apis mellifera,Entomopatojen,Etki

Kaynakça

1. Al mazra’awi, M.S. 2007. Impact of the Entomopatogenic Fungus Beauveria bassiana on the Honey Bees, Apis mellifera (Hymenoptera: Apidae). World Journal of Agricultural Sciences 3(1):07-11.
2. Andow, D.A., Zwahlen, C. 2006. Assessing environmental risks of transgenic plants. Ecol. Lett. 9, 196-214.
3. Azizoğlu, U., Bulut, S., Yılmaz, S. 2012. Organik tarımda biyolojik mücadele; entomopatojen biyoinsektisitler. Erciyes Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 28(5):375-381.
4. Babendreier, D., Kalberer, N.M., Romeis, J., Fluri, P., Mulligan, E., Bigler, F. 2005. Influence of Bt-transgenic pollen, Bt-toxin and protease inhibitor (SBTI) ingestion on development of the hypopharyngeal glands in honeybees. Apidologie 36, 585-594.
5. Baur, M.E., Kaya, H.K., Peng, Y.S. and Jiang, J. 1995. Nonsusceptibility of the Honey Bee, Apis mellifera (Hymenoptera: Apidae), to Steinernematid and Heterorhabditid. Nematodes Journal of Nematology 27(3):378-381.
6. Ben-Yakir, D., Efron, D., Chen, M. and Glazer, I. 1998. Evaluation of Entomopathogenic Nematodes for Biocontrol of the European corn borer, Ostrinia nubilalis, on Sweet Corn in Israel. Phytoparasitica, 26(2):1-8.
7. Begley, J.W. 1990. Efficacy Against Insects in Habitats Other Than Soil. Entomopathogenic Nematodes in Biological Control, 215-231.
8. Breeze, T.D., Bailey, A.P., Balcombe, K.G., Potts, S.G., 2011. Pollination services in the UK: How important are honeybees? Agric. Ecosyst. Environ. 142, 137-143. Brutscher, L.M., Daughenbaugh, K.F., and Flenniken, M.L., 2015. Antiviral defense mechanisms in honey bees. Current Opinion in Insect Science 10:71-82.

9. Cantwell, G.E., Lehnert, T. and Fowler, J. 1972. Are biological insecticides harmful to the honey bee? American Bee Journal 112: 255-258.
10. Chen, Y.P., Siede, R. 2007. Honey Bee Viruses. In Advances in Virus Research. Elsevier; 33-80. Chen, Y., Zhao, Y., Hammond, J., Hsu, H., Evans, J., Feldlaufer, Mark. 2004. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. Journal of Invertebrate Pathology 87:84-93.
11. DeGrandi-Hoffman, G. and Chen, Y. 2015. Nutrition, immunity and viral infections in honey bees. Curr. Opin. Insect Sci. 10, 170-176, 10.1016/j.cois.2015.05.007.
12. De Miranda, J.R., Ribie`re, G.L, Chen, M.Y.P. 2011. Honey bee viruses and their effects on bee and colony health. In Honey Bee Colony Health: Challenges and Sustainable Solution. Edited by Sammataro, D., Yoder, J.A., CRC Press Taylor & Francis Group; 71-102.
13. Demirci, F., Muştu, M., Kaydan, M.B., Ülgentürk, S. 2011. Laboratory evaluation of the effectiveness of the entomopathogen; Isaria farinosa, on citrus mealybug, Planococcus citri. Journal of Pest Science, 84:337-342.
14. Dillman, A.R., Sternberg, P.W. 2012. Entomopathogenic nematodes. Current Biology 22:R430-R431 DOI 10.1016/j.cub.2012.03.047.
15. Duan, J.J., Marvier, M., Huesing, J., Dively, G., Huang, Z.Y. 2008. A Meta-Analysis of Effects of Bt Crops on Honey Bees (Hymenoptera: Apidae). PLoSONE 3(1): e1415. doi:10.1371/journal.pone.0001415.
16. Dutka, A., McNulty A. and Williamson, S.M. 2015. A new threat to bees? Entomopathogenic nematodes used in biological pest control cause rapid mortality in Bombus terrestris. PeerJ 3:e1413.
17. Ekesi, S., Maniania, N.K. and Ampong-Nyarko, K. 1999. Effect of temperature on germination, radial growth and virulence of Metarhizium anisopliae and Beauveria bassiana on Megalurothrips sjostedti. Biocont. Sci. Technol., 9:177-185.
18. Erkılıç, L. and Uygun, N. 1993. Entomopatojen fungusların biyolojik mücadelede kullanım olanakları. Türk. Entomol. Der. 17(2):117-128.
19. Evans, J.D., Schwarz, R.S., 2011. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol. 19, 614-620.
20. Foley, K., Fazio, G., Jensen, A.B. and Hughes, W.O.H. 2012. Nutritional limitation and resistance to opportunistic Aspergillus parasites in honey bee larvae. Journal of Invertebrate Pathology 111:68-73. Flexner, J.L. and Belnavis, D.L. 2000. Microbial insecticides. Editör: J.E. Rechcigl ve N.A. Rechcigl. Biological and Biotechnological Control of Insect Pests. CRC Press, Boca Raton, USA, 35-62.
21. Gambino, P., Pierluisi, G.J. and Poinar, G.O.Jr. 1992. Field test of the nematode Steinernemafeltiae (Nematoda: Steinernematidae) against yellowjacket colonies (Hym: Vespidae). Entomophaga 37:107-114.
22. Gaugler, R., Kaya, H.K. 1990. Entomopathogenic Nematodes in Biological Control, CRC Press, Boca Raton, FL, 1-365.
23. Goodrich-Blair, H., Clarke, D.J. 2007. Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Molecular Microbiology 64:260-268.
24. Goettel, M.S. and Jaronsky, S.T. 1997. Safety and registration of microbial agenst for control of grasshoppers and locut. Mem. Entomol. Soc. Can., 171:83-99.
25. Han, C.S., Xie, G., Challaconbe, J.F. 2006. Pathogenomic Sequence Analysis of Bacillus cereus and Bacillus thuringiensis Isolates Closely Related to Bacillus anthracis, J. Bacteriol., 188(9), 3382-3390.
26. Hackett, K.J. and Poinar, G.O.Jr. 1973. The ability of Neoaplectana carpocapsae Weiser (Steinernematidae: Rhabditoidea) to infect adult honey bees (Apis Mellifera, Apidae: Hymenoptera). American Bee Journal 113:100.
27. Hazir, S., Kaya, H.K., Stock, S.P., Keskin, N. 2003. Entomopathogenic Nematodes (Steinernematidae and Heterorhabditidae) for Biological Control od Soil Pests, Türk J. Biology, 27, 181-202.
28. Heinz, K.M., McCutchen, B.F., Herrman, R., Parrella, M.P. and Hammock, B.D. 1995. Direct effects of recombinant nuclear polyhedrosis viruses on selected nontarget organisms. J. Econ. Entomol, 88:259-264.
29. Kaya, H.K., Marston, J.M., Lindegren, J.E. and Peng. Y.S. 1982. Low susceptibility of the honey bee, Apis mellifera L. (Hymenoptera: Apidae), to the entomogenous nematode, Neoaplectana carpocapsae Weiser. Environmental Entomology 11:920-924.
30. Kearns, C.A., Inouye D.W. and Waser, N.M. 1998. Endangered Mutualism: the conservation of plant-pollinator interaction. Ann. Rev. Ecol. Syst., 29:83-122.
31. Kevan., P.G. and Viana, B.F. 2003. The global decline of pollination services. Biodiversity, 4:3-8.
32. Lewıs, E.E. 2000. Biology, selection, handling and application of entomopathogenic nematodes. In Gothro, P (ed) Proceedings of beneficial nematode workshop. Application in greenhouse, nursery, and small-fruit operations. Oregon State University; USA; 6-11.
33. Li, J.L., Cornman, R.S., Evans, J.D., Pettis, J.S., Zhao, Y., Murphy, C., Peng, W.J., Wu, J., Hamilton, M., Boncristiani, H.F. 2014. Systemic spread and propagation of a plant-pathogenic virus in European honeybees, Apis mellifera. mBio. 5:e00898-13. doi: 10.1128/mBio.00898-13.
34. Lipa, J.J. and Triggiani, O. 1992. A newly recorded neogregarine (Protozoa, Apicomplexa), parasite in honey bees (Apis mellifera) and bumble bees (Bombus spp). Apidologie (1992) 23:533-536.
35. Lipa, J.J. and Hokkanen, H.M.T. 1992. Safety of Nosema meligethi I. and R. (Microsporida) to Apis mellifera L. and Coccinella septempunctata L.J. Invertebrate Pathol. 60:310-311.
36. Malone, L.A., Pham-Dele`gue, M.H. 2001. Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp). Apidologie 32, 1-18.
37. Medina, A., González, G., Sáez, J.M., Mateo, R. and Jiménez, M. 2004. Bee pollen, a substrate that stimulates ochratoxin a production by Aspergillus ochraceus Wilh. Syst. Appl. Microbiol. 27, 261-267.
38. McCoy, C.W. 1990.Entomogenous fungi as microbial pesticides. In Baker R.R. and Dunn P.E. (eds.), New Direction in Biological Control. A.R. Liss, New York, 139-159.
39. Morse, R.A, Flotum, K. 1997. Honeybee pests, predators, and diseases. A I Root Co.; Medina, OH, USA; 113-116.
40. Nielsen-LeRoux, C., Gaudriault, S., Ramarao, N., Lereclus, D., Givaudan, A., (2012). How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts. Current Opinion in Microbiology 15(3):220–231 DOI 10.1016/j.mib.2012.04.006.
41. Poinar, G.O.Jr. 1990. Taxonomy and biology of Steinernematidae and Heterorhabditidae. In Gaugler, R; Kaya, H K (eds) Entomophatogenic nematodes in biological control. CRC Press; Baca Raton; 23-61.
42. Porcar, M., Go´mez, F., Gruppe, A., Go´mez-Pajuelo, A., Segura, I., Schro¨der, R.2008. Hymenopteran specificity of Bacillus thuringiensis strain PS86Q3. Biological Control 45:427-432.
43. Prabhu, S., Mahalingam, C.A. and Krishnamoorthy, S.V. 2017. Safety Studies of DpNPV (Diaphania pulverulentalis Nuclearpolyhedrosis Virus) Suspension and its Formulation on Non-Target Organisms in Mulberry Ecosystem. Int.J.Curr.Microbiol.App.Sci. 6(6):1903-1913.
44. Ramirez-Romero, R., Desneux, N., Decourtye, A., Chaffiol, A., Pham-Dele`gue, M.H.2008. Does Cry1Ab protein affect learning performances of the honey bee Apis mellifera L. (Hymenoptera, Apidae)?. Ecotoxicology and Environmental Safety 70:327-333.
45. Rinderer, T.E., Rothenbuhler, W.C. and Gochnauer, T.A. 1974. The influence of pollen on the susceptibility of honey-bee larvae to Bacillus larvae. J. Invertebr. Pathol. 23, 347-350.
46. Rosas-García, N.M., Acuña-Jiménez, M., López-Meyer, M., Saínz-Hernández, C.J., Mundo-Ocampo, M. and García-Gutiérrez, C. 2015. Pathogenicity of microencapsulated insecticide from Beauveria bassiana and Metarhizium anisopliae against Tobacco Budworm, Heliothis virescens (Fabricius). Society of Southwestern Entomologists, Southwestern Entomologist, 40(3):531-538.
47. Samson, R.A., Evans, H.C. and Latge, J.P. 1988. Atlas of entomopathogenic fungi. Springer-Verlag, New York.
48. Shannag, H.K., Webb, S.E. and Capinera, J.L. 1994. Entomopathogenic nematode effect on pickleworm (Lepidoptera: Pyralidae) under laboratory and field conditions. Journal of Economic Entomology 87:1205-1212.
49. Sims, S.R. 1995. Bacillus thuringiensis var. kurstaki (CryIA(c)) protein expressed in transgenic cotton: effects on beneficial and other nontarget insects. Southwestern Entomologist 20, 493-500.
50. St Leger, R.J., Screen, S.E., Shams-Pirzadeh, B. 2000. Lack of host specialization in Aspergillus flavus. Appl. Environ. Microbiol. 66, 320-324.
51. Winston, M.L. 1987. The Biology of the Honeybee. Harvard University Press, Cambridge, MA.
52. Yaman, M. 2012. Böcek Patolojisi Atlası, Trabzon.
53. Yaman, M., Radek. R., Linde, A. 2012. A new neogregarine pathogen of Rhizophagus grandis. North-West Journal of Zoology, 8: 353-357.
54. Yaman, M., Acar, K. F., Radek, R. 2015. A Nucleopolyhedrovirus from the Mediterranean flour moth, Ephestia kuehniella (Lepidoptera: Pyralidae). Applied Entomology and Zoology. 50:355–359.
55. Yaman, M., Eroğlu, M., Radek, R. 2016. Occurrence of a microsporidium in the predatory beetle Calosoma sycophanta L. (Coleoptera: Carabidae). Turkish Journal of Agriculture and Forestry, 40: 420-424.
56. Żółtowska, K., Lipiński Z. And Łopieńska E. 2003. Beneficial nematodes: a potential threat to honey bees?. Bee World 84: 125-129.