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Insecticidal effect of Bacillus pumilus PTB180 and Bacillus subtilis PTB185 used alone and in combination against the foxglove aphid and the melon aphid (Hemiptera: Aphididae)

Published online by Cambridge University Press:  10 September 2021

Mouna Kahia ,
Thi Thuy An Nguyen ,
Frédéric McCune Open the ORCID record for Frédéric McCune [Opens in a new window] ,
Rémi Naasz ,
Hani Antoun  and
Valérie Fournier
Mouna Kahia
Affiliation:
Centre de recherche et d’innovation sur les végétaux, Université Laval, 2480 Boulevard Hochelaga, Québec, Québec, G1V 0A6, Canada Premier Tech, 1 Avenue Premier, Rivière-Du-Loup, Québec, G5R 6C1, Canada
Thi Thuy An Nguyen
Affiliation:
Centre de recherche et d’innovation sur les végétaux, Université Laval, 2480 Boulevard Hochelaga, Québec, Québec, G1V 0A6, Canada
Frédéric McCune*
Affiliation:
Centre de recherche et d’innovation sur les végétaux, Université Laval, 2480 Boulevard Hochelaga, Québec, Québec, G1V 0A6, Canada
Rémi Naasz
Affiliation:
Premier Tech, 1 Avenue Premier, Rivière-Du-Loup, Québec, G5R 6C1, Canada
Hani Antoun
Affiliation:
Centre de recherche et d’innovation sur les végétaux, Université Laval, 2480 Boulevard Hochelaga, Québec, Québec, G1V 0A6, Canada
Valérie Fournier
Affiliation:
Centre de recherche et d’innovation sur les végétaux, Université Laval, 2480 Boulevard Hochelaga, Québec, Québec, G1V 0A6, Canada
*
*Corresponding author. Email: [email protected]
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Abstract

The foxglove aphid, Aulacorthum solani (Kaltenbach) (Hemiptera: Aphididae), and the melon aphid, Aphis gossypii Glover (Hemiptera: Aphididae), are among the serious insect pests found in greenhouses. The efficacy of microbial control against these insects has been demonstrated and can be enhanced by the combination of different microbial agents. This study evaluated the efficacy of Bacillus pumilus Meyer and Gottheil PTB180 and Bacillus subtilis (Ehrenberg) Cohn PTB185, used alone and together, to control these two aphids both in the laboratory and in greenhouse on tomato, Solanum lycopersicum Linnaeus (Solanaceae), and cucumber, Cucumis sativus Linnaeus (Cucurbitaceae), plants. The results from the laboratory tests showed an increase in mortality induced by all biological treatments. In the greenhouse, all treatments induced mortality rates significantly higher than that of the control for A. solani. Similarly, all treatments performed better than the control against A. gossypii, significantly reducing its reproduction. Furthermore, we found no additive effects when mixing products nor negative interactions affecting survival for the bacteria investigated. These microorganisms therefore have potential for use in biological control.

Résumé

Résumé

Les pucerons de la digitale, Aulacorthum solani (Kaltenbach) (Hemiptera : Aphididae), et du melon, Aphis gossypii Glover (Hemiptera : Aphididae), font partie des ravageurs les plus nuisibles en serres. L’efficacité de la lutte microbienne contre ces insectes a été démontrée et pourrait être améliorée par la combinaison de différents agents microbiens. Cette étude a évalué l’efficacité de Bacillus pumilus Meyer and Gottheil PTB180 et Bacillus subtilis (Ehrenberg) Cohn PTB185, utilisés seuls ou ensemble, pour lutter contre ces deux pucerons en laboratoire et en serre sur des plants de tomate, Solanum lycopersicum Linnaeus (Solanaceae), et de concombre, Cucumis sativus Linnaeus (Cucurbitaceae). En laboratoire, les résultats ont montré une augmentation de la mortalité induite par tous les traitements biologiques. En serres, pour A. solani, tous les traitements ont induit un taux de mortalité nettement supérieur au témoin. Tous les traitements ont aussi significativement réduit la reproduction de A. gossypii. De plus, nous ne montrons aucun effet additif lors du mélange des produits ni aucune interaction négative affectant la survie des bactéries. Ces microorganismes ont donc un potentiel intéressant pour la lutte biologique.

Type
Research Paper
Information
The Canadian Entomologist , Volume 153 , Issue 6 , December 2021 , pp. 726 - 740
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Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Rob Johns

References

Agriculture and Agri-Food Canada. 2016. Statistical overview of the Canadian greenhouse vegetable industry, 2015 [online]. Available from https://www.agr.gc.ca/eng/horticulture/horticulture-sector-reports/statistical-overview-of-the-canadian-greenhouse-vegetable-industry-2015/?id=1468861362193 [accessed 20 December 2017].Google Scholar
Blackman, R.L. and Eastop, V.F. 2017. Taxonomic issues. In Aphids as crop pests. Edited by Van Emden, H.F. and Harrington, R.. CABI, Wallingford, Oxfordshire, United Kingdom. Pp. 1–36.Google Scholar
Chandrasekaran, R., Revathi, K., Nisha, S., Kirubakaran, S.A., Sathish-Narayanan, S., and Senthil-Nathan, S. 2012. Physiological effect of chitinase purified from Bacillus subtilis against the tobacco cutworm, Spodoptera litura Fab. Pesticide Biochemistry and Physiology, 104: 65–71. https://doi.org/10.1016/j.pestbp.2012.07.002.CrossRefGoogle Scholar
Chandrasekaran, R., Revathi, K., Thanigaivel, A., Kirubakaran, S.A., and Senthil-Nathan, S. 2014. Bacillus subtilis chitinase identified by matrix-assisted laser desorption/ionization time-of-flight/time-of-flight mass spectrometry has insecticidal activity against Spodoptera litura Fab. Pesticide Biochemistry and Physiology, 116: 1–12. https://doi.org/10.1016/j.pestbp.2014.09.013.CrossRefGoogle ScholarPubMed
Collier, F.A., Elliot, S.L., and Ellis, R.J. 2005. Spatial variation in Bacillus thuringiensis/cereus populations within the phyllosphere of broad-leaved dock (Rumex obtusifolius) and surrounding habitats. FEMS Microbiology Ecology, 54: 417–425. https://doi.org/10.1016/j.femsec.2005.05.005.CrossRefGoogle ScholarPubMed
Cossus, L., Roux-Dalvai, F., Kelly, I., Nguyen, T.T.A., Antoun, H., Droit, A., and Tweddell, R.J. 2021. Interactions with plant pathogens influence lipopeptides production and antimicrobial activity of Bacillus subtilis strain PTB185. Biological Control, 154: 104497. https://doi.org/10.1016/j.biocontrol.2020.104497.CrossRefGoogle Scholar
Costa, S.D., Barbercheck, M.E., and Kennedy, G.G. 2001. Mortality of Colorado potato beetle (Leptinotarsa decemlineata) after sublethal stress with the CryIIIA δ-endotoxin of Bacillus thuringiensis and subsequent exposure to Beauveria bassiana . Journal of Invertebrate Pathology, 179: 173–179. https://doi.org/10.1006/jipa.2001.5017.CrossRefGoogle Scholar
Foster, S.P., Devine, G., and Devonshire, A.L. 2017. Insecticide resistance. In Aphids as crop pests. Edited by Van Emden, H.F. and Harrington, R.. CABI, Wallingford, Oxfordshire, United Kingdom. Pp. 426–447.10.1079/9781780647098.0426CrossRefGoogle Scholar
Furk, C., Powell, D.F., and Heyd, S. 1980. Pirimicarb resistance in the melon and cotton aphid, Aphis gossypii Glover. Plant Pathology, 29: 191–196. https://doi.org/10.1111/j.1365-3059.1980.tb01211.x.CrossRefGoogle Scholar
Gonzalez, F., Tkaczuk, C., Dinu, M.M., Fiedler, Ż., Vidal, S., Zchori-Fein, E., and Messelink, G.J. 2016. New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops. Journal of Pest Science, 89: 295–311. https://doi.org/10.1007/s10340-016-0751-x.CrossRefGoogle ScholarPubMed
Gubran, E.M.E., Delorme, R., Auge, D., and Moreau, J.P. 1993. Pyrethroids and organochlorines resistance in cotton aphid Aphis gossypii (Glov.) (Homoptera: Aphididae) in the Sudan Gezira. International Journal of Pest Management, 39: 197–200. https://doi.org/10.1080/09670879309371790.CrossRefGoogle Scholar
Hu, D.W., Zhang, S., Luo, J.Y., Lü, L.M., Cui, J.J., and Zhang, X. 2017. An example of host plant expansion of host-specialized Aphis gossypii Glover in the field. PLOS One, 12: 1–14. https://doi.org/10.1371/journal.pone.0177981.Google ScholarPubMed
Iqbal, E.Y., Nahiyoon, A.A., Dawar, S., and Fayyaz, S. 2020. Bioremedy of cotton aphid (Aphis gossypii Glov.) (Hemiptera: Aphididae) by the application of different fractions of entomopathogenic bacteria (Xenorhabdus spp.). Pakistan Journal of Zoology, 52: 875–884. https://doi.org/10.17582/journal.pjz/20190828110853.CrossRefGoogle Scholar
Jandricic, S.E. 2013. Investigations of the biology of the pest aphid Aulacorthum solani (Kaltenbach) (Hemiptera: Aphididae) and of biological control agents for control of multi-species aphid outbreaks in greenhouse floriculture crops. PhD Dissertation, Cornell University, Ithaca, New York, United States of America.Google Scholar
Jandricic, S.E., Filotas, M., Sanderson, J.P., and Wraight, S.P. 2014. Pathogenicity of conidia-based preparations of entomopathogenic fungi against the greenhouse pest aphids Myzus persicae, Aphis gossypii, and Aulacorthum solani (Hemiptera: Aphididae). Journal of Invertebrate Pathology, 118: 34–46. https://doi.org/10.1016/j.jip.2014.02.003.CrossRefGoogle Scholar
Jandricic, S.E., Wraight, S.P., Bennett, K.C., and Sanderson, J.P. 2010. Developmental times and life table statistics of Aulacorthum solani (Hemiptera: Aphididae) at six constant temperatures, with recommendations on the application of temperature-dependent development models. Environmental Entomology, 39: 1631–1642. https://doi.org/10.1603/EN09351.CrossRefGoogle ScholarPubMed
Jurkevitch, E.J. and Shapira, G. 2000. Structure and colonization dynamics of epiphytic bacterial communities and of selected component strains on tomato (Lycopersicon esculentum) leaves. Microbial Ecology, 40: 300–308. https://doi.org/10.1007/s002480000023.CrossRefGoogle ScholarPubMed
Kilani-Feki, O., Ben Khedher, S., Dammak, M., Kamoun, A., Jabnoun-Khiareddine, H., Daami-Remadi, M., and Tounsi, S. 2016. Improvement of antifungal metabolites production by Bacillus subtilis V26 for biocontrol of tomato postharvest disease. Biological Control, 95: 73–82. https://doi.org/10.1016/j.biocontrol.2016.01.005.CrossRefGoogle Scholar
Konecka, E., Kaznowski, A., Grzesiek, W., Nowicki, P., Czarniewska, E., and Baranek, J. 2020. Synergistic interaction between carvacrol and Bacillus thuringiensis crystalline proteins against Cydia pomonella and Spodoptera exigua . BioControl, 65: 447–460. https://doi.org/10.1007/s10526-020-10011-4.CrossRefGoogle Scholar
Lacey, L.A., Grzywacz, D., Shapiro-Ilan, D.I., Frutos, R., Brownbridge, M., and Goettel, M.S. 2015. Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology, 132: 1–41. https://doi.org/10.1016/j.jip.2015.07.009.CrossRefGoogle ScholarPubMed
Lewis, L.C. and Bing, A.L. 1991. Bacillus thuringiensis Berliner and Beauveria bassiana (Balsamo) Vuillimen for European corn borer control: programme for immediate and season-long suppression. The Canadian Entomologist, 123: 387–393.10.4039/Ent123387-2CrossRefGoogle Scholar
López-Isasmendi, G., Alvarez, A.E., Petroselli, G., Erra-Balsells, R., and Audisio, M.C. 2019. Aphicidal activity of Bacillus amyloliquefaciens strains in the peach–potato aphid (Myzus persicae). Microbiological Research, 226: 41–47. https://doi.org/10.1016/j.micres.2019.05.006.CrossRefGoogle Scholar
Mascarin, G.M. and Jaronski, S.T. 2016. The production and uses of Beauveria bassiana as a microbial insecticide. World Journal of Microbiology and Biotechnology, 32: 26–26. https://doi.org/10.1007/s11274-016-2131-3.CrossRefGoogle ScholarPubMed
Matsuura, A. and Nakamura, M. 2014. Development of neonicotinoid resistance in the cotton aphid Aphis gossypii (Hemiptera: Aphididae) in Japan. Applied Entomology and Zoology, 49: 535–540. https://doi.org/10.1007/s13355-014-0289-4.CrossRefGoogle Scholar
Mia, B.M.A., Naher, U.A., Panhwar, A.Q., and Islam, M.T. 2016. Growth promotion of nonlegumes by the inoculation of Bacillus species. In Bacilli and agrobiotechnology. Edited by Islam, M.T., Rahman, M., Pandey, P., Jha, C.K., and Aeron, A.. Springer International Publishing, Cham, Switzerland. Pp. 57–76.10.1007/978-3-319-44409-3_3CrossRefGoogle Scholar
Molina, C., Caña-Roca, J.F., Osuna, A., and Vilchez, S. 2010. Selection of a Bacillus pumilus strain highly active against Ceratitis capitata (Wiedemann) larvae. Applied and Environmental Microbiology, 76: 1320–1327. https://doi.org/10.1128/AEM.01624-09.CrossRefGoogle ScholarPubMed
Moussa, S., Shehawy, A.A., Baiomy, F., Taha, A.A., and Ahmed, E.E.K. 2014. Bioactivity of chitinase against the aphids, Aphis craccivora (Koch) and Rhopalosiphum padi L. (Homoptera: Aphididae). Egyptian Journal of Biological Pest Control, 24: 239–245.Google Scholar
Peralta, C. and Palma, L. 2017. Is the insect world overcoming the efficacy of Bacillus thuringiensis? Toxins, 9: 1–5. https://doi.org/10.3390/toxins9010039.CrossRefGoogle ScholarPubMed
Prince, G. and Chandler, D. 2020. Susceptibility of Myzus persicae, Brevicoryne brassicae and Nasonovia ribisnigri to fungal biopesticides in laboratory and field experiments. Insects, 11: 1–16. https://doi.org/10.3390/insects11010055.CrossRefGoogle ScholarPubMed
Rajendran, L., Ramanathan, A., Durairaj, C., and Samiyappan, R. 2011. Endophytic Bacillus subtilis enriched with chitin offer induced systemic resistance in cotton against aphid infestation. Archives of Phytopathology and Plant Protection, 44: 1375–1389. https://doi.org/10.1080/03235408.2010.499719.CrossRefGoogle Scholar
Razmjou, J., Moharramipour, S., Fathipour, Y., and Mirhoseini, S.Z. 2006. Effect of cotton cultivar on performance of Aphis gossypii (Homoptera: Aphididae) in Iran. Journal of Economic Entomology, 99: 1820–1825. https://doi.org/10.1093/jee/99.5.1820.CrossRefGoogle Scholar
Rodríguez, M., Marín, A., Torres, M., Béjar, V., Campos, M., and Sampedro, I. 2018. Aphicidal activity of surfactants produced by Bacillus atrophaeus L193. Frontiers in Microbiology, 9: 3114. https://doi.org/10.3389/fmicb.2018.03114.CrossRefGoogle ScholarPubMed
Saif Ur, R., Zheng, J.Y., Ahmed, N., Feng, J.N., and Wang, D. 2019. Potential of four entomopathogenic fungi isolates as biological control agents against two aphid species under laboratory conditions. Pakistan Journal of Agricultural Sciences, 56: 421–429. https://doi.org/10.21162/pakjas/19.8582.Google Scholar
Szczech, M. and Shoda, M. 2004. Biocontrol of Rhizoctonia damping-off of tomato by Bacillus subtilis combined with Burkholderia cepacia . Journal of Phytopathology, 152: 549–556.CrossRefGoogle Scholar
Takada, H., Ono, T., Torikura, H., and Enokiya, T. 2006. Geographic variation in esterase allozymes of Aulacorthum solani (Homoptera: Aphididae) in Japan, in relation to its outbreaks on soybean. Applied Entomology and Zoology, 41: 595–605. https://doi.org/10.1303/aez.2006.595.CrossRefGoogle Scholar
Trinh, D.N., Ha, T.K.L., and Qiu, D.W. 2020. Biocontrol potential of some entomopathogenic fungal strains against bean aphid Megoura japonica (Matsumura). Agriculture-Basel, 10: 1–10. https://doi.org/10.3390/agriculture10040114.Google Scholar
Veselova, S.V., Burkhanova, G.F., Rumyantsev, S.D., Blagova, D.K., and Maksimov, I.V. 2019. Strains of Bacillus spp. regulate wheat resistance to greenbug aphid Schizaphis graminum Rond. Applied Biochemistry and Microbiology, 55: 41–47. https://doi.org/10.1134/S0003683819010186.CrossRefGoogle Scholar
Wang, K.Y., Liu, T.X., Hu, C.H., Jiang, X.Y., and Yi, M.Q. 2002. Resistance of Aphis gossypii (Homoptera: Aphididae) to fenvalerate and imidacloprid and activities of detoxification enzymes on cotton and cucumber. Journal of Economic Entomology, 95: 407–413. https://doi.org/10.1002/arch.20043.CrossRefGoogle ScholarPubMed
Wang, L., Wang, Q.Q., Wang, Q.Y., Rui, C.H., and Cui, L. 2020. The feeding behavior and life history changes in imidacloprid-resistant Aphis gossypii glover (Homoptera: Aphididae). Pest Management Science, 76: 1402–1412. https://doi.org/10.1002/ps.5653.CrossRefGoogle Scholar
Wang, X., Xue, Y., Han, M., Bu, Y., and Liu, C. 2014. The ecological roles of Bacillus thuringiensis within phyllosphere environments. Chemosphere, 108: 258–264. https://doi.org/10.1016/j.chemosphere.2014.01.050.CrossRefGoogle ScholarPubMed
Weber, M.H.W. and Marahiel, M.A. 2002. Coping with the cold: the cold shock response in the Gram-positive soil bacterium Bacillus subtilis . Philosophical Transactions: Biological Sciences, 357: 895–907.CrossRefGoogle ScholarPubMed
Wei, F., Hu, X., and Xu, X. 2016. Dispersal of Bacillus subtilis and its effect on strawberry phyllosphere microbiota under open-field and protection conditions. Scientific Reports, 6: 22611. https://doi.org/10.1038/srep22611.CrossRefGoogle ScholarPubMed
Wraight, S.P. and Ramos, M.E. 2005. Synergistic interaction between Beauveria bassiana- and Bacillus thuringiensis tenebrionis-based biopesticides applied against field populations of Colorado potato beetle larvae. Journal of Invertebrate Pathology, 90: 139–150. https://doi.org/10.1016/j.jip.2005.09.005.CrossRefGoogle ScholarPubMed
Wraight, S.P. and Ramos, M.E. 2017. Characterization of the synergistic interaction between Beauveria bassiana strain GHA and Bacillus thuringiensis morrisoni strain tenebrionis applied against Colorado potato beetle larvae. Journal of Invertebrate Pathology, 144: 47–57. https://doi.org/10.1016/j.jip.2017.01.007.CrossRefGoogle ScholarPubMed
Xu, X.M., Jeffries, P., Pautasso, M., and Jeger, M.J. 2011. Combined use of biocontrol agents to manage plant diseases in theory and practice. Phytopathology, 101: 1024–1031. https://doi.org/10.1094/phyto-08-10-0216.CrossRefGoogle ScholarPubMed
Yang, S.Y., Lim, D.J., Noh, M.Y., Kim, J.C., Kim, Y.C., and Kim, I.S. 2017. Characterization of biosurfactants as insecticidal metabolites produced by Bacillus subtilis Y9. Entomological Research, 47: 55–59. https://doi.org/10.1111/1748-5967.12200.CrossRefGoogle Scholar
Yaroslavtseva, O.N., Dubovskiy, I.M., Khodyrev, V.P., Duisembekov, B.A., Kryukov, V.Y., and Glupov, V.V. 2017. Immunological mechanisms of synergy between fungus Metarhizium robertsii and bacteria Bacillus thuringiensis ssp. morrisoni on Colorado potato beetle larvae. Journal of Insect Physiology, 96: 14–20. https://doi.org/10.1016/j.jinsphys.2016.10.004.CrossRefGoogle ScholarPubMed