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Differential side-effects of Bacillus thuringiensis bioinsecticide on non-target Drosophila flies

  • 1.

    United Nations, Department of Economic and Social Affairs, Population Division. World Population Prospects 2019—Data Booklet (ST/ESA/ SER.A/377), (2019). https://population.un.org/wpp/Publications/Files/WPP2019_DataBooklet.pdf

  • 2.

    Pimentel, D. & Burgess, M. Environmental and economic costs of the application of pesticides primarily in the United States. In Integrated Pest Management: Innovation-Development Process (eds Peshin, R. & Dhawan, A. K.) 47–71 (Springer, Dordrecht, 2014). https://doi.org/10.1007/978-1-4020-8992-3_4

    Google Scholar 

  • 3.

    Devine, G. J. & Furlong, M. J. Insecticide use: Contexts and ecological consequences. Agric. Hum. Values 24(3), 281–306. https://doi.org/10.1007/s10460-007-9067-z (2007).

    Article  Google Scholar 

  • 4.

    Sanchis, V. & Bourguet, D. Bacillus thuringiensis: Applications in agriculture and insect resistance management. A review. Agron. Sustain. Dev. 28(1), 11–20. https://doi.org/10.1051/agro:2007054 (2008).

    Article  Google Scholar 

  • 5.

    WHO report. WHO specifications and evaluations for public health pesticides: Bacillus thuringiensis subspecies israelensis strain AM65-52. (World Health Organization, Geneva, 2007).

  • 6.

    Rizzati, V., Briand, O., Guillou, H. & Gamet-Payrastre, L. Effects of pesticide mixtures in human and animal models: An update of the recent literature. Chem. Biol. Interact. 254, 231–246. https://doi.org/10.1016/j.cbi.2016.06.003 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 7.

    Lacey, L. A. et al. Insect pathogens as biological control agents: Back to the future. J. Invertebr. Pathol. 132, 1–41. https://doi.org/10.1016/j.jip.2015.07.009 (2015).

    Article  PubMed  CAS  Google Scholar 

  • 8.

    Adang, M. J., Crickmore, N. & Jurat-Fuentes, J. L. Diversity of Bacillus thuringiensis Crystal Toxins and Mechanism of Action. Adv. Insect Physiol. 47, 39–87. https://doi.org/10.1016/B978-0-12-800197-4.00002-6 (2014).

    Article  Google Scholar 

  • 9.

    Crickmore, N. Bacillus thuringiensis toxin classification. In Bacillus thuringiensis and Lysinibacillus sphaericus. (eds Fiuza, L.M. et al.) ISBN 978-3-319-56677-1, 41-52, (Spinger, Cham, 2017).

  • 10.

    WHO report. Guideline specification for bacterial larvicides for public health use. WHO document WHO/CDS/CPC/WHOPES/99.2 (World Health Organization, Geneva, 1999).

  • 11.

    Bravo, A., Pacheco, S., Gomez, I., Garcia-Gomez B., Onofre, J., Soberon, M. Insecticidal Proteins from Bacillus thuringiensis and their Mechanism of Action. In Bacillus thuringiensis and Lysinibacillus sphaericus (eds Fiuza, L.M. et al.) ISBN 978-3-319-56677-1, 53–66, (Spinger, Cham, 2017).

  • 12.

    Palma, L., Muñoz, D., Berry, C., Murillo, J. & Caballero, P. Bacillus thuringiensis toxins: An overview of their biocidal activity. Toxins 6(12), 3296–3325. https://doi.org/10.3390/toxins6123296 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 13.

    Ben-Dov, E. et al. Extended screening by PCR for seven cry-group genes from field-collected strains of Bacillus thuringiensis. Appl. Environ. Microb. 63(12), 4883–4890. https://doi.org/10.1128/aem.63.12.4883-4890.1997 (1997).

    CAS  Google Scholar 

  • 14.

    Berry, C. et al. Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl. Environ. Microbiol. 68(10), 5082–5095. https://doi.org/10.1128/aem.68.10.5082-5095.2002 (2002).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 15.

    Bravo, A., Gill, S. S. & Soberon, M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49, 423–435. https://doi.org/10.1016/j.toxicon.2006.11.022 (2007).

    Article  PubMed  CAS  Google Scholar 

  • 16.

    Wei, J. et al. Activation of Bt protoxin Cry1Ac in resistant and susceptible cotton bollworm. PLoS ONE 11(6), e0156560. https://doi.org/10.1371/journal.pone.0156560 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 17.

    Bravo, A., Likitvivatanavong, S., Gill, S. S. & Soberon, M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41(7), 423–431. https://doi.org/10.1016/j.ibmb.2011.02.006 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 18.

    Caccia, S. et al. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proc. Natl. Acad. Sci. USA 113(34), 9486–9491. https://doi.org/10.1073/pnas.1521741113 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 19.

    Glare, T.R., O’Callaghan, M. Bacillus thuringiensis: Biology, Ecology and Safety. ISBN: 9780471496304, 350, (Wiley, New York, 2000).

  • 20.

    Rubio-Infante, N. & Moreno-Fierros, L. An overview of the safety and biological effects of Bacillus thuringiensis Cry toxins in mammals. J. Appl. Toxicol. 36, 630–648. https://doi.org/10.1002/jat.3252 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 21.

    EFSA Panel on Biological Hazards (BIOHAZ). Risks for public health related to the presence of Bacillus cereus and other Bacillus spp. including Bacillus thuringiensis in foodstuffs. EFSA J. https://doi.org/10.2903/j.efsa.2016.4524 (2016).

    Article  Google Scholar 

  • 22.

    Amichot, M., Curty, C., Benguettat-Magliano, O., Gallet, A. & Wajnberg, E. Side effects of Bacillus thuringiensis var. kurstaki on the hymenopterous parasitic wasp Trichogramma chilonis. Environ. Sci. Pollut. Res. Int. 23, 3097–3103. https://doi.org/10.1007/s11356-015-5830-7 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 23.

    Renzi, M. T. et al. Chronic toxicity and physiological changes induced in the honey bee by the exposure to fipronil and Bacillus thuringiensis spores alone or combined. Ecotoxicol. Environ. Saf. 127, 205–213. https://doi.org/10.1016/j.ecoenv.2016.01.028 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 24.

    Caquet, T., Roucaute, M., Le Goff, P. & Lagadic, L. Effects of repeated field applications of two formulations of Bacillus thuringiensis var. israelensis on non-target saltmarsh invertebrates in Atlantic coastal wetlands. Ecotoxicol. Environ. Saf. 74, 1122–1130. https://doi.org/10.1016/j.ecoenv.2011.04.028 (2011).

    Article  PubMed  CAS  Google Scholar 

  • 25.

    Duguma, D. et al. Microbial communities and nutrient dynamics in experimental microcosms are altered after the application of a high dose of Bti. J. Appl. Ecol. 52, 763–773. https://doi.org/10.1111/1365-2664.12422 (2015).

    Article  CAS  Google Scholar 

  • 26.

    Venter, H. J. & Bøhn, T. Interactions between Bt crops and aquatic ecosystems: A review. Environ. Toxicol. Chem. 35(12), 2891–2902. https://doi.org/10.1002/etc.3583 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 27.

    van Frankenhuyzen, K. Specificity and cross-order activity of Bacillus thuringiensis pesticidal proteins. In Bacillus thuringiensis and Lysinibacillus sphaericus (eds Fiuza, L.M. et al.) ISBN 978-3-319-56677-1, 127–172, (Springer, Cham, 2017).

  • 28.

    Bizzarri, M. F. & Bishop, A. H. The ecology of Bacillus thuringiensis on the phylloplane: Colonization from soil, plasmid transfer, and interaction with larvae of Pieris brassicae. Microb. Ecol. 56(1), 133–139. https://doi.org/10.1007/s00248-007-9331-1 (2008).

    Article  PubMed  CAS  Google Scholar 

  • 29.

    Raymond, B., Wyres, K. L., Sheppard, S. K., Ellis, R. J. & Bonsall, M. B. Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathog. 6(5), e1000905. https://doi.org/10.1371/journal.ppat.1000905 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 30.

    Hendriksen, N. B. & Hansen, B. M. Long-term survival and germination of Bacillus thuringiensis var. kurstaki in a field trial. Can. J. Microbiol. 48(3), 256–261. https://doi.org/10.1139/w02-009 (2002).

    Article  PubMed  CAS  Google Scholar 

  • 31.

    Hung, T. P. et al. Persistence of detectable insecticidal proteins from Bacillus thuringiensis (Cry) and toxicity after adsorption on contrasting soils. Environ. Pollut. 208, 318–325. https://doi.org/10.1016/j.envpol.2015.09.046 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 32.

    Hung, T. P. et al. Fate of insecticidal Bacillus thuringiensis Cry protein in soil: Differences between purified toxin and biopesticide formulation. Pest Manag. Sci. 72, 2247–2253. https://doi.org/10.1002/ps.4262 (2016).

    Article  PubMed  CAS  Google Scholar 

  • 33.

    Enger, K. S. et al. Evaluating the long-term persistence of Bacillus spores on common surfaces. Microb. Biotechnol. 11(6), 1048–1059. https://doi.org/10.1111/1751-7915.13267 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 34.

    Couch, T.L. Industrial fermentation and formulation of entomopathogenic bacteria. In Entomopathogenic Bacteria: From Laboratory to Field Application (eds Charles, J.-F. et al.) ISBN 978-90-481-5542-2, 297–316.43, (Springer, Dordrecht, 2000).

  • 35.

    Brar, S. K., Verma, M., Tyagi, R. D. & Valéro, J. R. Recent advances in downstream processing and formulations of Bacillus thuringiensis based biopesticides. Process Biochem. 41(2), 323–342. https://doi.org/10.1016/j.procbio.2005.07.015 (2006).

    Article  CAS  Google Scholar 

  • 36.

    Setlow, P. Spore resistance properties. Microbiol. Spectr. 2(5), TBS-0003-2012. https://doi.org/10.1128/microbiolspec.TBS-0003-2012 (2014).

    Article  CAS  Google Scholar 

  • 37.

    European Food Safety Authority. Conclusion on the peer review of the pesticide risk assessment of the active substance Bacillus thuringiensis subsp. Kurstaki (strains ABTS 351, PB 54, SA 11, SA 12, EG 2348). EFSA J. 10(2), 2540. https://doi.org/10.2903/j.efsa.2012.2540 (2012).

    Article  CAS  Google Scholar 

  • 38.

    Bächli, G. TaxoDros: The database on Taxonomy of Drosophilidae: Database 2020/1.https://www.taxodros.uzh.ch. (1999–2020).

  • 39.

    Tennessen, J. M. & Thummel, C. S. Coordinating growth and maturation—Insights from Drosophila. Curr. Biol. 21(18), R750–R757. https://doi.org/10.1016/j.cub.2011.06.033 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 40.

    Benz, G. & Perron, J. M. The toxic action of Bacillus thuringiensis “exotoxin” on Drosophila reared in yeast-containing and yeast-free media. Experientia 23(10), 871–872 (1967).

    PubMed  CAS  Google Scholar 

  • 41.

    Saadoun, I., Al-Moman, F., Obeidat, M., Meqdam, M. & Elbetieha, A. Assessment of toxic potential of local Jordanian Bacillus thuringiensis strains on Drosophila melanogaster and Culex sp. (Diptera). J. Appl. Microbiol. 90, 866–872. https://doi.org/10.1046/j.1365-2672.2001.01315.x (2001).

    Article  PubMed  CAS  Google Scholar 

  • 42.

    Khyami-Horani, H. Toxicity of Bacillus thuringiensis and B. sphaericus to laboratory populations of Drosophila melanogaster (Diptera: Drosophilidae). J. Basic Microbiol. 42(2), 105–110. https://doi.org/10.1002/1521-4028(200205)42:2<105::AID-JOBM105>3.0.CO;2-S (2002). 

    Article  PubMed  Google Scholar 

  • 43.

    Obeidat, M. Toxicity of local Bacillus thuringiensis isolates against Drosophila melanogaster. WJAS 4(2), 161–167 (2008).

    Google Scholar 

  • 44.

    Obeidat, M., Khymani-Horani, H. & Al-Momani, F. Toxicity of Bacillus thuringiensis β-exotoxins and δ-endotoxins to Drosophila melanogaster, Ephestia kuhniella and human erythrocytes. Afr. J. Biotechnol. 11(46), 10504–10512 (2012).

    Google Scholar 

  • 45.

    Cossentine, J., Robertson, M. & Xu, D. Biological activity of Bacillus thuringiensis in Drosophila suzukii (Diptera: Drosophilidae). J. Econ. Entomol. 109(3), 1–8. https://doi.org/10.1093/jee/tow062 (2016).

    Article  CAS  Google Scholar 

  • 46.

    Biganski, S., Jehle, J. A. & Kleepies, R. G. Bacillus thuringiensis serovar israelensis has no effect on Drosophila suzukii Matsumura. J. Appl. Entomol. 142, 33–36. https://doi.org/10.1111/jen.12415 (2017).

    Google Scholar 

  • 47.

    Haller, S., Romeis, J. X. R. & Meissle, M. Effects of purified or plant-produced Cry proteins on Drosophila melanogaster (Diptera: Drosophilidae) larvae. Sci. Rep. 7(1), 11172. https://doi.org/10.1038/s41598-017-10801-4 (2017).

    ADS  Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 48.

    Benado, M. & Brncic, D. An eight-year phenological study of a local drosophilid community in Central Chile. J. Zool. Syst. Evol. Res. 32, 51–63. https://doi.org/10.1111/j.1439-0469.1994.tb00470.x (1994).

    Article  Google Scholar 

  • 49.

    Nunney, L. The colonization of oranges by the cosmopolitan Drosophila. Oecologia 108, 552–561. https://www.jstor.org/stable/4221451 (1996).

    ADS  PubMed  Google Scholar 

  • 50.

    Mitsui, H. & Kimura, M. T. Coexistence of drosophilid flies: Aggregation, patch size diversity and parasitism. Ecol. Res. 15, 93–100.  https://doi.org/10.1046/j.1440-1703.2000.00328.x (2000).

    Google Scholar 

  • 51.

    Withers, P. & Allemand, R. Les drosophiles de la région Rhône-Alpes (Diptera, Drosophilidae). Bull. Soc. Entomol. Fr. 117(4), 473–482. https://www.persee.fr/doc/bsef_0037-928x_2012_num_117_4_3076 (2012).

    Google Scholar 

  • 52.

    Stevens, T., Song, S., Bruning, J. B., Choo, A. & Baxter, S. W. Expressing a moth abcc2 gene in transgenic Drosophila causes susceptibility to Bt Cry1Ac without requiring a cadherin-like protein receptor. Insect Biochem. Mol. Biol. 80, 61–70. https://doi.org/10.1016/j.ibmb.2016.11.008 (2017).

    Article  PubMed  CAS  Google Scholar 

  • 53.

    George, Z., Crickmore, N. Bacillus thuringiensis applications in agriculture. In Bacillus thuringiensis Biotechnology (ed Sansinenea, E.) 392, (Springer, Dordrecht, 2012).

  • 54.

    Nepoux, V., Haag, C. R. & Kawecki, T. J. Effects of inbreeding on aversive learning in Drosophila. J. Evol. Biol. 23, 2333–2345. https://doi.org/10.1111/j.1420-9101.2010.02094.x (2010).

    Article  PubMed  CAS  Google Scholar 

  • 55.

    Vantaux, A., Ouattarra, I., Lefèvre, T. & Dabiré, K. R. Effects of larvicidal and larval nutritional stresses on Anopheles gambiae development, survival and competence for Plasmodium falciparum. Parasite. Vector. 9, 226. https://doi.org/10.1186/s13071-016-1514-5 (2016).

    Article  CAS  Google Scholar 

  • 56.

    Moret, Y. & Schmid-Hempel, P. Survival for immunity: The price of immune system activation for bumblebee workers. Science 290(5494), 1166–1168. https://doi.org/10.1126/science.290.5494.1166 (2000).

    ADS  Article  PubMed  CAS  Google Scholar 

  • 57.

    Kutzer, M. A. & Armitage, S. A. O. The effect of diet and time after bacterial infection on fecundity, resistance, and tolerance in Drosophila melanogaster. Ecol. Evol. 6(13), 4229–4242. https://doi.org/10.1002/ece3.2185 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  • 58.

    Andersen, L. H., Kristensen, T. N., Loeschcke, V., Toft, S. & Mayntz, D. Protein and carbohydrate composition of larval food affects tolerance to thermal stress and desiccation in adult Drosophila melanogaster. J. Insect Physiol. 56, 336–340. https://doi.org/10.1016/j.jinsphys.2009.11.006 (2010).

    Article  PubMed  CAS  Google Scholar 

  • 59.

    Rion, S. & Kawecki, T. J. Evolutionary biology of starvation resistance: What we have learned from Drosophila. J. Evol. Biol. 20(5), 1655–1664. https://doi.org/10.1111/j.1420-9101.2007.01405.x (2007).

    Article  PubMed  CAS  Google Scholar 

  • 60.

    Burger, J. M. S., Buechel, S. D. & Kawecki, T. J. Dietary restriction affects lifespan but not cognitive aging in Drosophila melanogaster. Aging Cell 9, 327–335. https://doi.org/10.1111/j.1474-9726.2010.00560.x (2010).

    Article  PubMed  CAS  Google Scholar 

  • 61.

    Khazaeli, A. A. & Curtsinger, J. W. Genetic analysis of extended lifespan in Drosophila melanogaster III. On the relationship between artificially selected and wild stocks. Genetica 109, 245–253. https://doi.org/10.1023/a:1017569318401 (2000).

    Article  PubMed  CAS  Google Scholar 

  • 62.

    Atkinson, W. & Shorrocks, B. Breeding site specificity in the domestic species of Drosophila. Oecologia 29(3), 223–232. https://www.jstor.org/stable/4215461 (1977).

    ADS  PubMed  CAS  Google Scholar 

  • 63.

    Walsh, D. B. et al. Drosophila suzukii (Diptera: Drosophilidae): Invasive pest of ripening soft fruit expanding its geographic range and damage potential. J. Integr. Pest Manag. https://doi.org/10.1603/IPM10010 (2011).

    Article  Google Scholar 

  • 64.

    Delbac, L. et al. Drosophila suzukii est-elle une menace pour la vigne?. Phytoma 679, 16–21 (2014).

    Google Scholar 

  • 65.

    Poyet, M. et al. Invasive host for invasive pest: When the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotine) in Europe. Agric. For. Entomol. 16(3), 251–259. https://doi.org/10.1111/afe.12052 (2014).

    Article  Google Scholar 

  • 66.

    Poulin, B., Lefebvre, G. & Paz, L. Red flag for green spray: Adverse trophic effects of Bti on breeding birds. J. Appl. Ecol. 47, 884–889. https://doi.org/10.1111/j.1365-2664.2010.01821.x (2010).

    Article  Google Scholar 

  • 67.

    Zeigler, D.R. Bacillus genetic stock center catalog of strains, 7th edition. Part 2: Bacillus thuringiensis and Bacillus cereus. http://www.bgsc.org/_catalogs/Catpart2.pdf (1999).

  • 68.

    Gonzales, J. M. Jr., Brown, B. J. & Carlton, B. C. Transfer of Bacillus thuringiensis plasmids coding for δ-endotoxin among strains of B. thuringiensis and B. cereus. Proc. Natl Acad. Sci. USA 79, 6951–6955. https://doi.org/10.1073/pnas.79.22.6951 (1982).

    ADS  Article  Google Scholar 

  • 69.

    Santos, M., Borash, D. J., Joshi, A., Bounlutay, N. & Mueller, L. D. Density-dependent natural selection in Drosophila: Evolution of growth rate and body size. Evolution 51(2), 420–432. https://doi.org/10.2307/2411114 (1997).

    Article  PubMed  Google Scholar 

  • 70.

    Bradberry, S. M., Proudfoot, A. T. & Vale, J. A. Glyphosate poisoning. Toxicol. Rev. 23(3), 159–167. https://doi.org/10.2165/00139709-200423030-00003 (2004).

    Article  PubMed  CAS  Google Scholar 

  • 71.

    R Development Core Team. R: A language and environment for statistical computing. ISBN 3-900051-07-0 https://www.R-project.org (R Foundation for Statistical Computing, Vienna, 2008).

  • 72.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).

    Google Scholar 

  • 73.

    Kosmidis I. brglm: Bias Reduction in Binary-Response Generalized Linear Models. R package version 0.6.1, https://www.ucl.ac.uk/~ucakiko/software.html, (2017).

  • 74.

    Horton, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometrical J. 50(3), 346–363. https://doi.org/10.1002/bimj.200810425 (2008).

    MathSciNet  Article  Google Scholar 

  • 75.

    Therneau, T.M., Grambsch, P.M. Modeling Survival Data: Extending The Cox Model. ISBN 0-387-98784-3 (Springer, New York, 2000).

  • 76.

    Therneau, T.M. coxme: Mixed Effects Cox Models. R package version 2.2-5. https://CRAN.R-project.org/package=coxme (2015).


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