Research Article
Effects of different origins of two pesticides on several bacteria in the microbiota of Bombus terrestris L.
Abstract
This study aimed to evaluate the effects of pesticides from different origins on several bacteria in the microbiota of Bombus terrestris. In the experiments, recommended field doses (1/1) and sublethal doses (1/10, 1/100, 1/1000) of Subtilex Foliar (Bacillus subtilis MBI 600, Bioglobal©) and Pusula (Thiamethoxam, Hektaş©) were used. The experiments were performed with 5 replications (10 worker bees per replication). The worker bees were fed the sugar syrup + pesticide mixture prepared for 5 days in each replication. On the fifth day after applications, 5 random individuals from each trial were selected from the live worker bees and, after being mechanically euthanized, placed in sterilized falcon tubes labeled with experimental group details. The same procedure was applied to the microbiota analysis of the control group as the experimental groups. These individuals were then analyzed to determine microorganism changes. According to the results obtained, the colony development of two different species of bacteria, Staphylococcus xylosus and S. gallinarum, was determined in the control group. Staphylococcus xylosus and S. gallinarum were completely inhibited in 1/1 and 1/10 dose applications of B. subtilis MBI 600, while the dominant species was B. subtilis MBI 600. Staphylococcus xylosus in the control group became dominant after the application of 1/100 dose of B. subtilis MBI 600, and after the application of 1/1000 dose, B. subtilis MBI 600 could not colonize. When Thiamethoxam applications were compared with the control group, Staphylococcus gallinarum colonies and Pseudomonas sp. colonies became dominant in individuals who received 1/1 dose application. The results show that the different origins of the pesticides used cause significant changes in the microbiota of worker bees for life.
References
- Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EAD, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research 22: 35-67.
- Cameron SA, Sadd BM (2020) Global trends in bumble bee health. Annual Review of Entomology 65: 209-232.
- Campa AA, Lehmann DM (2021) Impacts of neonicotinoids on the bumble bees Bombus terrestris and Bombus impatiens Examined through the lens of an adverse outcome pathway framework. Environmental Toxicology and Chemistry 40(2): 309-322.
- Chmiel JA, Daisley BA, Burton JP, Reid G (2019) Deleterious effects of neonicotinoid pesticides on Drosophila melanogaster immune pathways. doi: 10.1128/mBio.01395-19.
- Crall JD, Switzer CM, Oppenheimer RL, Ford Versypt AN, Dey B, Brown A, Eyster M, Guérin C, Pierce NE, Combes SA, de Bivort BL (2018) Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362: 683-686.
- Çakıcı Ö, Uysal M, Demirözer O, Gösterit A (2023a) Sublethal effects of thiamethoxam on immune system cells in the workers of Bombus terrestris (Hymenoptera: Apidae). Springer Science and Business Media LLC 30(37): 87424-87432.
- Çakıcı Ö, Uysal M, Demirözer O, Gösterit A (2023b) Effects of thiamethoxam on brain structure of Bombus terrestris (Hymenoptera: Apidae) workers. doi: 10.1016/j.chemosphere.2023.139595.
- Daisley BA, Chmiel JA, Pitek AP, Thompson GJ, Reid G (2020) Missing microbes in bees: how systematic depletion of key symbionts erodes immunity. doi: 10.1016/j.tim.2020.06.006.
- Dussaubat C, Maisonnasse A, Crauser D, Tchamitchian S, Bonnet M, Cousin M, Kretzschmar A, Brunet JL, Le Conte Y (2016) Combined neonicotinoid pesticide and parasite stress alter honeybee queens’ physiology and survival. Scientific Reports 6: 1-7.
- Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM, Chandler JA, Cornman RS, Dainat J, De Miranda JR, Doublet V, Emery O, Evans JD, Farinelli L, Flenniken ML, Granberg F, Grasis JA, Gauthier L, Hayer J, Koch H, Kocher S Martinson VG, Moran N, Munoz-Torres M, Newton I, Paxton RJ, Powell E, Sadd BM, Schmid-Hempel P, Schmid-Hempel R, Song SJ, Schwarz RS, van Engelsdorpa D, Dain B (2016) The bee microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions. mBio 7: e02164-15.
- Feltham H, Park K, Goulson D (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23: 317-323.
- Gallai N, Salles JM, Settele J (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810-821.
- Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127): 1608-1611.
- Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491: 105-108.
- Gill RJ, Raine NE (2014) Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology 28: 1459-1471.
- Goulson D (2003) Bumblebees: their behavior and ecology. Oxford University Press, New York.
- Hotchkiss MZ, Poulain AJ, Forrest JRK (2022) Pesticide-induced disturbances of bee gut microbiotas. FEMS Microbiology Reviews 46(2): fuab056.
- Johnston PR, Crickmore N (2009) Gut bacteria are not required for the insecticidal activity of Bacillus thuringiensis toward the tobacco hornworm, Manduca sexta. Applied and Environmental Microbiology 75: 5094-5099.
- Kesnerova L, Mars RA, Ellegaard KM, Troilo M, Sauer U, Engel P (2017) Disentangling metabolic functions of bacteria in the honey bee gut. PLOS Biology 15(12): e2003467.
- Killer J, Votavová A, Valterová I, Vlková E, Rada V, Hroncová Z (2014) Lactobacillus bombi sp. nov., from the digestive tract of laboratory-reared bumblebee queens (Bombus terrestris). International Journal of Systematic and Evolutionary Microbiology 64: 2611-2617.
- Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for World crops. doi: 10.1098/rspb.2006.3721.
- Koch H, Cisarovsky G, Schmid-Hempel P (2012) Ecological effects on gut bacterial communities in wild bumblebee colonies. Journal of Animal Ecology 81(6): 1202-1210.
- Kwong WK, Moran NA (2013) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology 63: 2008-2018.
- Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nature Reviews Microbiology 14: 374-384.
- Kwong WK, Mancenido AL, Moran NA (2017) Immune system stimulation by the native gut microbiota of honeybees. Royal Society Open Science 4: 170003.
- Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21: 1937-1945.
- Laycock I, Cotterell KC, O’Shea-Wheller TA, Cresswell JE (2014) Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on micro colonies of Bombus terrestris worker bumblebees. Ecotoxicology and Environmental Safety 100: 153-158.
- Li JL, Powell JE, Guo J, Evans JD, Wu J, Williams P, Lin Q, Moran NA, Zhang, ZG (2015) Two gut community enterotypes recur in diverse bumblebee species. Current Biology 25: R652-653.
- Li K, Wang L, Zhang Z, Guo Y, Guo J, Amjad N, Shaikh HM, Wu J, Li J (2021) Isolation of Bacillus from the gut of Bombus terrestris and its correlation in queen mating. Journal of Agricultural Science 13(9): 155-162.
- Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20: 619-628.
- Mommaerts V, Sterk G, Hofmann L and Smagghe G (2009) A laboratory evaluation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris. Pest Management Science 65: 949-955.
- Mondal S, Somani J, Roy S, Babu A, Pandey AK (2023) Insect Microbial Symbionts: Ecology, Interactions, and Biological Significance. Microorganisms 11(2665): 1-27.
- Motta EVS, Raymann K, Moran NA (2018) Glyphosate perturbs the gut microbiota of honey bees. doi: 10.1073/pnas.1803880115.
- Motta EVS, Mak M, De Jong TK, Powell JE, O'Donnell A, Suhr KJ, Riddington IM, Moran NA (2020) Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. doi: 10.1128/AEM.01150-20.
- Nayak RK, Rana K, Bairwa VK, Singh P, Bharthi VD (2020) A review on role of bumblebee pollination in fruits and vegetables. Journal of Pharmacognosy and Phytochemistry 9: 1328-1334.
- Pincus DH (2002) Microbial identification using the biomérıeux Vitek 2 system, Biomérıeux Inc., Hazelwood, MO, USA.
- Poinar GO, Thomas GM (1978) Diagnostic Manual for the Identification of Insect Pathogens. USA: Plenum Press, New York.
- Praet J, Cnockaert M, Meeus I, Smagghe G, Vandamme P (2017) Gilliamella intestini sp. nov., Gilliamella bombicola sp. nov., Gilliamella bombi sp. nov. and Gilliamella mensalis sp. nov.: Four novel Gilliamella species isolated from the bumblebee gut. Systematic and Applied Microbiology 40(4): 199-204.
- Ragab A, Abd-ElAziz MF, Esmael A, Baz MM (2022) Gut microbial diversity and immunological effects of antibiotics on Spodoptera littoralis feeding on different diets. Benha Journal of Applied Sciences 7(12): 53-61.
- Raymann K, Motta EVS, Girard C, Riddington IM, Dinser JA, Moran NA (2018) Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. doi: 10.1128/AEM.00545-18.
- Richman SK, Muth F, Leonard AS (2021) Measuring foraging preferences in bumble bees: a comparison of popular laboratory methods and a test for sucrose preferences following neonicotinoid exposure. Oecologia 196: 963-976.
- Rouzé R, Moné A, Delbac F, Belzunces L, Blot N (2019) The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae. doi:10.1264/jsme2.ME18169.
- Saranya M, Krishnamoorthy S, Murugesh K (2019) Fortification of mulberry leaves with indigenous probiotic bacteria on larval growth and economic traits of silkworm (Bombyx mori, L.). Journal of Entomology and Zoology Studies 7: 780-784.
- Simon‐Delso N, Amaral‐Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, MIneau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research 22: 5-34.
- Smith DB, Arce AN, Rodrigues AR, Bischoff PH, Burris D, Ahmed F, Gill RJ (2020) Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees. Proceedings of the Royal Society B: Biological Sciences 287: 20192442.
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Effects of different origins of two pesticides on several bacteria in the microbiota of Bombus terrestris L.
Abstract
This study aimed to evaluate the effects of pesticides from different origins on several bacteria in the microbiota of Bombus terrestris. In the experiments, recommended field doses (1/1) and sublethal doses (1/10, 1/100, 1/1000) of Subtilex Foliar (Bacillus subtilis MBI 600, Bioglobal©) and Pusula (Thiamethoxam, Hektaş©) were used. The experiments were performed with 5 replications (10 worker bees per replication). The worker bees were fed the sugar syrup + pesticide mixture prepared for 5 days in each replication. On the fifth day after applications, 5 random individuals from each trial were selected from the live worker bees and, after being mechanically euthanized, placed in sterilized falcon tubes labeled with experimental group details. The same procedure was applied to the microbiota analysis of the control group as the experimental groups. These individuals were then analyzed to determine microorganism changes. According to the results obtained, the colony development of two different species of bacteria, Staphylococcus xylosus and S. gallinarum, was determined in the control group. Staphylococcus xylosus and S. gallinarum were completely inhibited in 1/1 and 1/10 dose applications of B. subtilis MBI 600, while the dominant species was B. subtilis MBI 600. Staphylococcus xylosus in the control group became dominant after the application of 1/100 dose of B. subtilis MBI 600, and after the application of 1/1000 dose, B. subtilis MBI 600 could not colonize. When Thiamethoxam applications were compared with the control group, Staphylococcus gallinarum colonies and Pseudomonas sp. colonies became dominant in individuals who received 1/1 dose application. The results show that the different origins of the pesticides used cause significant changes in the microbiota of worker bees for life.
References
- Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EAD, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research 22: 35-67.
- Cameron SA, Sadd BM (2020) Global trends in bumble bee health. Annual Review of Entomology 65: 209-232.
- Campa AA, Lehmann DM (2021) Impacts of neonicotinoids on the bumble bees Bombus terrestris and Bombus impatiens Examined through the lens of an adverse outcome pathway framework. Environmental Toxicology and Chemistry 40(2): 309-322.
- Chmiel JA, Daisley BA, Burton JP, Reid G (2019) Deleterious effects of neonicotinoid pesticides on Drosophila melanogaster immune pathways. doi: 10.1128/mBio.01395-19.
- Crall JD, Switzer CM, Oppenheimer RL, Ford Versypt AN, Dey B, Brown A, Eyster M, Guérin C, Pierce NE, Combes SA, de Bivort BL (2018) Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362: 683-686.
- Çakıcı Ö, Uysal M, Demirözer O, Gösterit A (2023a) Sublethal effects of thiamethoxam on immune system cells in the workers of Bombus terrestris (Hymenoptera: Apidae). Springer Science and Business Media LLC 30(37): 87424-87432.
- Çakıcı Ö, Uysal M, Demirözer O, Gösterit A (2023b) Effects of thiamethoxam on brain structure of Bombus terrestris (Hymenoptera: Apidae) workers. doi: 10.1016/j.chemosphere.2023.139595.
- Daisley BA, Chmiel JA, Pitek AP, Thompson GJ, Reid G (2020) Missing microbes in bees: how systematic depletion of key symbionts erodes immunity. doi: 10.1016/j.tim.2020.06.006.
- Dussaubat C, Maisonnasse A, Crauser D, Tchamitchian S, Bonnet M, Cousin M, Kretzschmar A, Brunet JL, Le Conte Y (2016) Combined neonicotinoid pesticide and parasite stress alter honeybee queens’ physiology and survival. Scientific Reports 6: 1-7.
- Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM, Chandler JA, Cornman RS, Dainat J, De Miranda JR, Doublet V, Emery O, Evans JD, Farinelli L, Flenniken ML, Granberg F, Grasis JA, Gauthier L, Hayer J, Koch H, Kocher S Martinson VG, Moran N, Munoz-Torres M, Newton I, Paxton RJ, Powell E, Sadd BM, Schmid-Hempel P, Schmid-Hempel R, Song SJ, Schwarz RS, van Engelsdorpa D, Dain B (2016) The bee microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions. mBio 7: e02164-15.
- Feltham H, Park K, Goulson D (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23: 317-323.
- Gallai N, Salles JM, Settele J (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810-821.
- Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127): 1608-1611.
- Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491: 105-108.
- Gill RJ, Raine NE (2014) Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology 28: 1459-1471.
- Goulson D (2003) Bumblebees: their behavior and ecology. Oxford University Press, New York.
- Hotchkiss MZ, Poulain AJ, Forrest JRK (2022) Pesticide-induced disturbances of bee gut microbiotas. FEMS Microbiology Reviews 46(2): fuab056.
- Johnston PR, Crickmore N (2009) Gut bacteria are not required for the insecticidal activity of Bacillus thuringiensis toward the tobacco hornworm, Manduca sexta. Applied and Environmental Microbiology 75: 5094-5099.
- Kesnerova L, Mars RA, Ellegaard KM, Troilo M, Sauer U, Engel P (2017) Disentangling metabolic functions of bacteria in the honey bee gut. PLOS Biology 15(12): e2003467.
- Killer J, Votavová A, Valterová I, Vlková E, Rada V, Hroncová Z (2014) Lactobacillus bombi sp. nov., from the digestive tract of laboratory-reared bumblebee queens (Bombus terrestris). International Journal of Systematic and Evolutionary Microbiology 64: 2611-2617.
- Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for World crops. doi: 10.1098/rspb.2006.3721.
- Koch H, Cisarovsky G, Schmid-Hempel P (2012) Ecological effects on gut bacterial communities in wild bumblebee colonies. Journal of Animal Ecology 81(6): 1202-1210.
- Kwong WK, Moran NA (2013) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology 63: 2008-2018.
- Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nature Reviews Microbiology 14: 374-384.
- Kwong WK, Mancenido AL, Moran NA (2017) Immune system stimulation by the native gut microbiota of honeybees. Royal Society Open Science 4: 170003.
- Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21: 1937-1945.
- Laycock I, Cotterell KC, O’Shea-Wheller TA, Cresswell JE (2014) Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on micro colonies of Bombus terrestris worker bumblebees. Ecotoxicology and Environmental Safety 100: 153-158.
- Li JL, Powell JE, Guo J, Evans JD, Wu J, Williams P, Lin Q, Moran NA, Zhang, ZG (2015) Two gut community enterotypes recur in diverse bumblebee species. Current Biology 25: R652-653.
- Li K, Wang L, Zhang Z, Guo Y, Guo J, Amjad N, Shaikh HM, Wu J, Li J (2021) Isolation of Bacillus from the gut of Bombus terrestris and its correlation in queen mating. Journal of Agricultural Science 13(9): 155-162.
- Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20: 619-628.
- Mommaerts V, Sterk G, Hofmann L and Smagghe G (2009) A laboratory evaluation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris. Pest Management Science 65: 949-955.
- Mondal S, Somani J, Roy S, Babu A, Pandey AK (2023) Insect Microbial Symbionts: Ecology, Interactions, and Biological Significance. Microorganisms 11(2665): 1-27.
- Motta EVS, Raymann K, Moran NA (2018) Glyphosate perturbs the gut microbiota of honey bees. doi: 10.1073/pnas.1803880115.
- Motta EVS, Mak M, De Jong TK, Powell JE, O'Donnell A, Suhr KJ, Riddington IM, Moran NA (2020) Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. doi: 10.1128/AEM.01150-20.
- Nayak RK, Rana K, Bairwa VK, Singh P, Bharthi VD (2020) A review on role of bumblebee pollination in fruits and vegetables. Journal of Pharmacognosy and Phytochemistry 9: 1328-1334.
- Pincus DH (2002) Microbial identification using the biomérıeux Vitek 2 system, Biomérıeux Inc., Hazelwood, MO, USA.
- Poinar GO, Thomas GM (1978) Diagnostic Manual for the Identification of Insect Pathogens. USA: Plenum Press, New York.
- Praet J, Cnockaert M, Meeus I, Smagghe G, Vandamme P (2017) Gilliamella intestini sp. nov., Gilliamella bombicola sp. nov., Gilliamella bombi sp. nov. and Gilliamella mensalis sp. nov.: Four novel Gilliamella species isolated from the bumblebee gut. Systematic and Applied Microbiology 40(4): 199-204.
- Ragab A, Abd-ElAziz MF, Esmael A, Baz MM (2022) Gut microbial diversity and immunological effects of antibiotics on Spodoptera littoralis feeding on different diets. Benha Journal of Applied Sciences 7(12): 53-61.
- Raymann K, Motta EVS, Girard C, Riddington IM, Dinser JA, Moran NA (2018) Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. doi: 10.1128/AEM.00545-18.
- Richman SK, Muth F, Leonard AS (2021) Measuring foraging preferences in bumble bees: a comparison of popular laboratory methods and a test for sucrose preferences following neonicotinoid exposure. Oecologia 196: 963-976.
- Rouzé R, Moné A, Delbac F, Belzunces L, Blot N (2019) The honeybee gut microbiota is altered after chronic exposure to different families of insecticides and infection by Nosema ceranae. doi:10.1264/jsme2.ME18169.
- Saranya M, Krishnamoorthy S, Murugesh K (2019) Fortification of mulberry leaves with indigenous probiotic bacteria on larval growth and economic traits of silkworm (Bombyx mori, L.). Journal of Entomology and Zoology Studies 7: 780-784.
- Simon‐Delso N, Amaral‐Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, MIneau P, Mitchell EAD, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research 22: 5-34.
- Smith DB, Arce AN, Rodrigues AR, Bischoff PH, Burris D, Ahmed F, Gill RJ (2020) Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebees. Proceedings of the Royal Society B: Biological Sciences 287: 20192442.
- Stanley DA, Smith KE, Raine NE (2015) Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Scientific Reports 5: 16508.
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There are 59 citations in total.
Details
| Primary Language | English |
|---|---|
| Subjects | Plant Protection (Other) |
| Journal Section | Makaleler |
| Authors | |
| Publication Date | April 9, 2025 |
| Submission Date | December 10, 2024 |
| Acceptance Date | February 7, 2025 |
| Published in Issue | Year 2025 Volume: 38 Issue: 1 |
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