Biological Activity of Bacillus Thuringiensis (Berliner) Strains on Larvae and Adults of Ceratitis Capitata (Wiedemann) (Diptera: Tephritidae)

Houda Aboussaid, Loubna El-Aouame, Said El-Messoussi, Khalid Oufdou
DOI: 10.4236/jep.2010.14040                

Abstract

The objective of this study was to evaluate the efficiency of Moroccan Bt strains against neonate larvae, third instar larvae and emerged adults of Ceratitis capitata. This Mediterranean fruit fly causes serious damages to Argan forest and other agricultural plants. There is no successful control program of this pest fly in the endemic Argan forest in Morocco. A single-dose test was performed on neonate larvae (25 µL/g) and adult (333.33 µL/g), when three doses of Bt toxins (50 µL/g, 100 µL/g and 150 µL/g) were tested against third instar of C. capitata. Among the twenty-six Bt strains examined, local Bt13.4 and Bt A7 strains showed highest toxicity levels against larvae and adults, when compared to the reference strain, Bacillus thuringiensis subsp. israelensis HD567 “code 4Q1”, and commercial product “Skeetal”. One hundred percent mortality was observed against neonate larvae after 7 days of application by Bt 13.4 toxin. Third instar larvae were very susceptible to Bt A7 and Bt M-Ag 21.6 strains with 68% mortality (Lethal Concentration: LC50 = 1.115) at a dose of 150 µL/g. The Bt A7 strain was also highly toxic to adults with 81.66% of mortality after 7 days of application. This study demonstrated that some of our collection Bt strains can contribute to integrated C. capitata management system with strong biological control components.

Keywords

Argan Forest, Bacillus Thuringiensis, Biological Control, Ceratitis Capitata, Diptera

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. P. Ros, E. Wong, J. Olivero and E. Castillo, “Mejora de los Mosqueros, Atrayentes y Sistemas de Retención Contra la Mosca Mediterránea de la Fruta Ceratitis capitata Wied. Como Hacer de la Técnica del Trampeo Masivo una Buena Herramienta Para Controlar esta Plaga,” Boletín Sanidad Vegetal Plagas, Vol. 28, No. 4, 2002, pp. 591-597.
[2]	C. Maga?a, P. Hernández-Crespo, A. Brun-Barale, F. Couso-Ferrer, J. M. Bride, P. Casta?era, R. Feyereisen and F. Ortego, “Mechanisms of Resistance to Malathion in the Medfly Ceratitis capitata,” Insect Biochemisry and Molecular Biology, Vol. 38, No. 8, 2008, pp. 756-762.
[3]	V. Sanchis, and D. Bourguet, “Bacillus thuringiensis: Applications in Agriculture and Insect Resistance Mana- gement,” Agronomy for Sustainable Development, Vol. 28, No. 1, 2008, pp. 11-20.
[4]	K. van Frankenhuyzen, “Insecticidal Activity of Bacillus thuringiensis Crystal Proteins,” Journal of Invertebrate Pathology, Vol. 101, No. 1, 2009, pp. 1-16.
[5]	N. Crickmore, D. R. Zeigler, J. Feitelson and E. Schnepf, “Revision of the Nomenclature for the Bacillus thurin- giensis Pesticidal Crystal Proteins,” Microbiology and Molecular Biology Reviews, Vol. 62, No. 3, 1998, pp. 807-813.
[6]	M. Porcar and V. M. Juárez-Pérez, “PCR-Based Iden- tification of Bacillus thuringiensis Pesticidal Crystal Genes,” FEMS Microbiology Reviews, Vol. 26, No. 5, 2003, pp. 419-432.
[7]	IPSC-WHO, “Bacillus thuringiensis. Environmental Health Criteria of the International Program on Chemical Safety,” IPCS WHO International Program on Chemical Safety, No. 217. 1999.
[8]	E. Schnepf, N. Crickmore, J. Van Rie and D. Lereclus, “Bacillus thuringiensis and Its Pesticidal Crystal Proteins,” Microbiology and Molecular Biology Reviews, Vol. 62, No. 3, 1998, pp. 775-806.
[9]	K. F. Chak, D. C. Chao, M. Y. Tseng and S. S. Kao, “Determination and Distribution of Cry-Type Genes of Bacillus thuringiensis Isolates from Taiwan,” Applied and Environmental Microbiology, Vol. 60, No. 7, 1994, pp. 2415-2420.
[10]	A. Bravo, S. Sarabia, L. López and H. Ontiveros, “Characterization of Cry Genes in a Mexican Bacillus thuringiensis Strain Collection,” Applied and Environmental Microbiology, Vol. 64, No. 12, 1998, pp. 4965-4972.
[11]	J. E. Ibarra, M. C. Del Rincon, S. Orduz and D. Noriega, “Diversity of Bacillus thuringiensis Strains from Latin America with Insecticidal Activity against Different Mosquito Species,” Applied and Environmental Micro- biology, Vol. 69, No. 9, 2003, pp. 5269-5274.
[12]	E. Quesada-Moraga, E. García-Tovar, P. Valverde-García and C. Santiago-álvarez, “Isolation, Geographical Diversity and Insecticidal Activity of Bacillus thuringiensis from Soils in Spain,” Microbiology Research, Vol. 159, No. 1, 2004, pp. 59-71.
[13]	C. Itoua-Apoyolo, L. Drif, J. M. Vassal, H. DeBarjac, J. P. Bossy, F. Leclant and R. Frutos, “Isolation of Multiple Subspecies of Bacillus thuringiensis from a Population of the European Sunflower Moth, Homoeosoma nebulella,” Applied and Environmental Microbiology, Vol. 61, No. 12, 1995, pp. 4343-4347.
[14]	G. Karamanlidou, A. F. Lambropoulos, S. I. Koliais, T. Manousis, D. Ellar and C. Kastritsis, “Toxicity of Bacillus thuringiensis to Laboratory Populations of the Olive Fruit Fly (Dacus oleae),” Applied and Environmental Microbiology, Vol. 57, No. 8, 1991, pp. 2277-2282.
[15]	T. M. Alberola, S. Aptosoglou, M. Arsenakis, Y. Bel, G. Delrio, D. J. Ellar, J. Ferre, S. P. Gash, F. Granero, S. Koliais, M. J. Martinez-Sebastian, R. Prota, S. Rubino, A. Satta, G. Scarpellini, A. Sivropoulou and E. Vasara, “Insecticidal Activity of Strains of Bacillus thuringiensis on Larvae and Adults of Bactrocera oleae Gmelin (Dipt. Tephritidae),” Journal of Invertebrate Pathology, Vol. 74, No. 2, 1999, pp. 127-136.
[16]	D. C. Robacker, A. J. Martínez, J. A. García, M. Díaz and C. Romero, “Toxicity of Bacillus thuringiensis to Mexican Fruit Fly (Diptera: Tephritidae),” Journal of Economic Entomology, Vol. 89, No. 1, 1996, pp. 104-110.
[17]	J. Toledo, P. Liedo, T. Williams and J. Ibarra, “Toxicity of Bacillus thuringiensis β-Exotoxin to Three Species of Fruit Flies (Diptera: Tephritidae)”, Journal of Economic Entomology, Vol. 92, No. 5, 1999, pp. 1052-1056.
[18]	R. E. Gingrich, “Demonstration of Bacillus thuringiensis as a Potential Control Agent for the Adult Mediterranean Fruit Fly, Ceratitis capitata (Wied.),” Journal of Applied Entomology, Vol. 104, No. 1-5, 1987, pp. 378-385.
[19]	F. Hassani and N. Gaouar Benyelles, “Application of Bacillus thuringiensis (Bti) Struggling Microbiological Control of the Fruit Fly Ceratitis capitata (wied) (Diptera: Tephritidae),” IBSCientific Journal of Science, Vol. 3, No. 1, 2008, pp. 10-13.
[20]	J. C. Vidal-Quist, P. Casta?era and J. González-Cabrera, “Diversity of Bacillus thuringiensis Strains Isolated from Citrus Orchards in Spain and Evaluation of Their Insecticidal Activity against Ceratitis capitata,” Journal of Microbiology and Biotechnology, Vol. 19, No. 8, 2009, pp. 749-759.
[21]	Y. Bel, F. Granero, T. M. Alberola, M. J. Martínez- Sebastian and J. Ferré, “Distribution, Frequency and Diversity of Bacillus thuringiensis in Olive Tree Environments in Spain,” Systematic and Applied Microbiology, Vol. 20, No. 4, 1997, pp. 652-658.
[22]	G. S. A. B. Stewart, K. Johnstone, E. Hagelberg and D. J. Ellar, “Commitment of Bacterial Spores to Germinate,” Biochemistry Journal, Vol. 198, No. 1, 1981, pp. 101-106.
[23]	E. Helgason, O. A. Okstad, D. A. Caugant, H. A. Johansen, A. Fouet, M. Mock, I. Hegna and A. B. Kolsto, “Bacillus Anthracis, Bacillus cereus, and Bacillus thuringiensis - One Species on the Basis of Genetic Evidence,” Applied and Environmental Microbiology, Vol. 66, No. 6, 2000, pp. 2627-2630.
[24]	J. A. Baum and T. Malvar, “Regulation of insecticidal crystal protein production in Bacillus thuringiensis,” Molecular Microbiology, Vol. 18, No. 1, 1995, pp. 1-12.
[25]	C. A. Molina, J. F. Cana-Roca, A. Osuna and S. Vilchez, “Selection of a Bacillus pumilus Strain Highly Active against Ceratitis capitata (Wiedemann) Larvae,” Applied and Environmental Microbiology, Vol. 76, No. 5, 2010, pp. 1320-1327.
[26]	C. Yamvrias and M. Anagnou, “Preliminary Tests on the Sensitivity of the Larvae of Dacus oleae to Bacillus thuringiensis var. israelensis, in Fruit Flies of Economic Importance,” R. Cavalloro, Ed., Balkema, Rotterdam, Vol. 87, 1989, pp. 345-348.