Effects of Bacillus thuringiensis kurstaki on Midgut Cells of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae), The Pine Processionary Caterpillar

Abstract

In this study effects of Bacillus thuringiensis kurstaki (Btk) on midgut cells of Thaumetopoea pityocampa larvae was investigated by electron microscopy. 3 mg/l Btk was given with food. 1 h, 3 h and 6 h after Btk administration no pathological changes in the midgut epitelial cells were observed. 12 h after Btk administration swelling of mitochondria in midgut epitelial cells were observed. Formation of vacuoles in cytoplasm was seen after 24 h. After 48 h decreasing of microvilli of midgut epithelial cell’s and partial dissolving of cytoplasm, dissolving of nucleoplasm and chromatin clumps were observed. 60 h after Btk administration swelling and dissolving of mitochondria in midgut epithelial cells were detected. 96 h after Btk administration a membrane-body and dissolving in the cytoplasm clumps in midgut cells of T. pityocampa larvae were occurred. Present study shows that Btk is effective to T. pityocampa larvae.

Keywords

• Thaumetopoea pityocampa
• Bacillus thuringiensis kurstaki
• midgut
• ultrastructure
• transmission electron microscope

References

1. Halperin, J., “Life history of Thaumetopoeidae species (Lep., Thaumetopoeidae) in Israel”, J. Appl. Entomol., 110: 1–6 (1990).
2. Petrakis, P.V., Roussis, V. and Ortiz, A., “Host selection by Thaumetopoea pityocampa (Den. & Schif.): the relative importance of needle terpenoid and morpho-anatomical profiles”, In: Radoglou, K. (Ed.), Proceedings of the International Conference on Forest Research: a Challenge for an Integrated European Approach, vol. I. European Commission, Thessalonica (Greece),pp. 343–348 (2001).
3. Mendel, Z., “The phytophagous insect fauna of Pinus halpensis and P. brutia in the Mediterannean”. In: Ne’eman, Biogeography and Management of Pinus halepensis and L. (Eds.), Ecology P. brutia Forest Ecosystems in the Thaumetopoea pityocampa (Lepidoptera, Th. processionea L.
4. Saturniidae)”, Comp. Biochem.
5. Rebollo, S., Moneo, I., Vega, J.M., Herrera, I. and Caballero, M.L., “Pine processionary caterpillar allergenicity increases during larval development”, Int. Arch. Allergy Immunol., 128: 310-314 (2002).
6. Battisti, A., Longo, S., Tiberi, R. and Triggiani, O., “Results and perspectives in the use of Bacillus thuringiensis Berl. var. kurstaki and other pathogens against Thaumetopoea pityocampa (Den. et Schiff.) in Schadlingskde. Pfalanzenschutz, Umweltschutz.,, 71: 77-80 (1998). Anz.
7. Burges, H.D., “Control of insects by bacteria”, Parasitology. 84: 79-117 (1982).
8. Rausell, C., Martinez-Ramirez, A.C., Garcia-Robles, I. and Real, M.D., “The toxicity and physiological effects of Bacillus thuringiensis toxins and formulations on Thaumetopoea pityocampa, the pine processionary caterpillar”, Pest. Biochem. Physiol., 65: 44-54 (1999).

9. Guo, S., Ye, S., Liu, Y., Wei, L., Xue, J., Wub, H., Song, F., Zhang, J., Wuc, X., Huang, D. and Rao, Z., Crystal structure of Bacillus thuringiensis Cry8Ea1: An insecticidal toxin toxic to underground pests, the larvae of Holotrichia parallela. J. Struct. Biol., 168: 259–266 (2009).
10. Martin, P.A.W., Farrar, R.R. and Blackburn, M.B., “Survival of diverse Bacillus thuringiensis strains in gypsy correlated with urease production”, Biol. Control, 51: 147–151 (2009). Lymantriidae) is
11. Tailor, R., Tippett, J., Gibb, G., Pells, S., Pike, D., Jordan, L. and Ely, S., “Identification and characterization of a novel Bacillus thuringiensis delta-endotoxin entomocidal to coleopteran and lepidopteran larvae”, Mol. Microbiol., 6: 1211–1217 (1992).
12. Feitelson, J.S., “The Bacillus thuringiensis family tree”, In: Kim, L. (Ed.), Advanced Engineered Pesticides. Mareel Dekker, Inc., New York, NY, pp. 63–71 (1993).
13. Li, J., Koni, P.A. and Ellar, D.J., “Structure of the mosquitocidal-endotoxin thuringiensis sp. kyushuensis and implications for membrane pore formation” J. Mol. Biol., 257: 129– 152 (1996). CytB from Bacillus
14. Bravo, A., “Phylogenetic relationships of Bacillus thuringiensis deltaendotoxin family proteins and their functional domains”, J. Bacteriol., 179: 2793– 2801 (1997).
15. Higuchi, K., Saitoh, H., Mizuki, E., Hwang, S.H. and Ohba, M., “A novel isolate of Bacillus thuringiensis serovar leesis that specifically exhibits larvicidal activity albipunctatus”, Syst. Appl. Microbiol., 21: 144–150 (1998). Telmatoscopus
16. Ellis, R.T., Stockhoff, B.A., Stamp, L., Schnepf, H.E., Schwab, G.E., Knuth, M., Russell, J., Cardineau, G.A. and Nara, K.E., “Novel Bacillus thuringiensis binary insecticidal crystal proteins active on western corn rootworm, Diabrotica virgifera virgifera LeConte”, Appl. Environ. Microbiol., 68: 1137–1145 (2002).
17. Arnaldo, P.S. and Torres, L.M., “Spatial distribution and sampling of Thaumetopoea pityocampa (Den. & Schiff.) (Lep. Thaumetopoeidea) populations on Pinus pinaster Ait. in Montesinho, N. Portugal”, Forest Ecol. Manag., 210, 1–7 (2005).
18. Kailidis, D.S., “Observations on the Biology and Control of the Pine Processionary Caterpillar (Thaumetopoea pityocampa Schiff.) in Attica”, Athens, Greece, 59 p(1962).
19. Oliveira, P., Arnaldo, P.S., Araujo, M., Ginja, M., Sousa, A.P., Almeida, O. and Colaco, A.,. “Report of poison in five dogs after contact with Thaumetopoea pityocampa”, Revista Portuguesa de Ciencias Clınicas 89 (547): 81–84 (2003).
20. Etkind, P.H., O’Dell, T.M., Canada, A.T., Shama, S.K., Finn, A.M. and Tuthil, R., “The gypsy moth caterpillar: A significant new occupational and public health problem”, J. Occup. Med., 24: 659-662 (1982).
21. Everson, G.W., Chapin, J.B. and Normann, S.A., “Caterpillar envenomations: a prospective study of 112 cases”, Vet. Hum. Toxicol., 32: 114-119 (1990).
22. Kalender Y., Kalender S., Uzunhısarcıklı M., Ogutcu A. and Açıkgoz F., “Effects of Thaumetopoea pityocampa (Lepidoptera: Thaumetopoeidae) larvae on the degranulation of the dermal mast cells in mice; an electron microscopic study”, Folia Biol. (Kraków)., 52: 13-17 (2004).
23. Douma-Petridou, E., “European Thaumetopoea species (Lep., Thaumetopoeidae): characteristics and life-cycles” . In: Schmidt, G.H. (Ed.), Proc. Thaumetopoea Department of Zoology–Entomology, University of Hannover (FRG), pp. 12–19 (1989) 1989,
24. OEPP/EPPO,. Diagnostic protocols for regulated pests Thaumetopoea pityocampa. Bull. OEPP/EPPO 34: 155–157 (2004).
25. Lamy, M., Pastureaud. M.H., Novak, F., Ducombs, G., Vincendeau, P., Maleville, J. and Texier, L., “Thaumetopoein: An urticating protein from the hairs and integument of the pine processionary caterpillar Lepidoptera, Thaumetopoeidae)”, Toxicon ;24: 347–356 (1986). pityocampa Schiff,
26. Vega, J.M., Moneo, I., Armentia, A., Vega, V., de la Fuente, R. and Fernandez, A., “Pine processionary caterpillar as a new cause of immunologic contact urticaria”, Contact Dermat., 43: 129–132 (2000).
27. Delello E.,Hantonw.K.,Bıshoffs. T. and Mıschd.W., “Histopathological effects of Bacillus thuringiensis on the midgut of tobacco hornworm larvae (Manduca sexta): low doses compared with fasting”, J. Invertebr. Pathol. 43: 169-181 (2000).
28. Sıngh G.J.P., Schouest Jr. L.P. and Gıll S.S., “The toxic action israelensis’in Aedes aegypti in vivo. I. The Relevance of midgut lesions to its poisoning syndrome”, Pestic. Biochem. Phys. 26: 36-46 (1986). thuringiensis var.
29. Levy, S.M., Moscardi, F., Falleiros, A.M.F., Silva, R.J. and Gregorio, E.A., “A morphometric study of the midgut in resistant and non-resistant Anticarsia gemmatalis (Hübner) (Lepidoptera: Noctuidae) larvae to its nucleopolyhedrovirus (AgMNPV)”, J. Invertebr. Pathol. 101: 17–22 (2009).
30. Maddrell, S.H.P. and Gardiner, B.O.C., “The permeability of the cuticular lining of the insect alimentary canal”, J. Exp. Biol. 85: 227-237 (1980).
31. Dow, J.A.T., “Advances in Insect Physiology”, Volume 19, Academic Pres. Inc. (London) Ltd. 189- 200. 1986
32. Kalender, Y. and Kalender, S., “Effect of Bacillus thuringiensis var. kurstaki in ileum region of digestion system of Agrotis segetum (Lepidoptera: Noctuidae) larvae”, J. Inst. Sci. Tech. Gazi Uni., 8: 18-32 (1995).
33. Kalender, Y. and Kalender, S., “Effect of Bacillus thuringiensis in Malpighian tubule cells of Pieris rapae (Lepidoptera: Pieridae) larvae”, J. Inst. Sci. Tech. Gazi Uni., 10: 43-55 (1997).
34. Rausell, C., De Decker, N., Garcia-Robles, I., Escriche, B., Van Kerkhove, E., Real, M.D., Martinez-Ramirez thuringiensis toxins on the midgut of the nun moth Lymantria monacha”, J. Invertebr. Pathol., 75: 288- 291 (2000). “Effect of Bacillus
35. Ogutcu, A., Suludere, Z:, Uzunhısarcıklı, M. and Kalender, Y., “Effects of Bacillus thuringiensis kurstaki Thaumetopoea pityocampa Thaumetopoeidae) Larvae”, Folia Biol. (Kraków), 53 (1-2): 7-11 (2005). Tubule Cells (Lepidoptera:
36. Aronson, A.I., Beckman, W. and Dunn, P., “Bacillus thuringiensis Microbiol. Rev., 50: 1-24 (1986). insect pathogens”,
37. Joung, K. and Cote, J., “A review of the environmental impacts of the microbial insecticide Bacillus thuringiensis”, Horticultural Research and Development Centre Technical Bulletin, 29, Canada (2000).
38. Bravo, A., Jansens, S. and Peferoen, M., “Immunocytochemical localization of Bacillus thuringiensis intoxicated insects”, J. Invertebr. Pathol., 60: 237- 246 (1992). crystal proteins in
39. Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J., Feitelson, J., Zeigler, D.R. and Dean, D.H., “Bacillus thuringiensis and its pesticidal crystal proteins”, Microbiol. Mol. Biol. Rev., 62: 775-806 (1998).
40. Lorence, A., Darszon, A., Diaz, C., Lievano, A., Quintero, R. and Bravo, A., “δ-endotoxins induce cation channels in Spodoptera frugiperda brush border membranes in suspension and in planar lipid bilayers”, FEBS Lett., 360: 217-222 (1995).
41. Pietrantonio, P.V. and Gill, S.S., “Bacillus thuringiensis δ-endotoxins: action on the insect midgut, in: M.J. Lehane, P.F. Billingsley (Eds.), Biology of the Insect Midgut, Chapman & Hall, London, pp. 345-372 (1996).
42. Bravo, A., Miranda, R., Gomez, I. and Soberon, M., “Pore formation activity of Cry1Ab toxin from Bacillus thuringiensis in an improved membrane vesicle preparation from Manduca sexta midgut cell microvilli”, B.B.A.,1562: 63-69 (2002).
43. Lacey, L. and Federici, B.A., “Pathogenesis and midgut histopathology of Bacillus thuringiensis in Simulium vittatum (Diptera: Simuliidae)”, J. Invertebr. Pathol., 33: 171-182 (1979).
44. Endo, Y. and Nishiitsutsuji-Uwo, J., “Mode of action of Bacillus Histopathological changes in the silkworm midgut”, J. Invertebr. Pathol., 36: 90-103 (1980). endotoxin:
45. Endo, Y. and Nishiitsutsuji-Uwo, J., “Mode of action of Bacillus thuringiensis δ endotoxin: Ultrastructural changes of midgut epithelium of Pieris, Lymantria and Ephestia larvae”, Appl. Entomol. Zool., 16: 231- 241 (1981).