Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees

Abstract Bees are essential pollinators that contribute to maintaining biodiversity and increasing agricultural production. However, by foraging on agricultural crops, bees may become contaminated with compounds used for pest control. In this study, we exposed bee (Apis mellifera L.) colonies to the...

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Main Authors: Daiani Rodrigues Moreira, Tuan Henrique Smielevski de Souza, Douglas Galhardo, Cinthia Leão Figueira, Samara Calvi Baulli, Breno Gabriel da Silva, Francieli das Chagas, José Washington Santos Oliveira, Jean Samel Rocha, Angélica de Souza Khatlab, Eliane Gasparino, Vagner de Alencar Arnaut de Toledo, Adriana Aparecida Sinópolis Gigliolli, Maria Claudia Colla Ruvolo-Takasusuki
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Biological Research
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Online Access:https://doi.org/10.1186/s40659-024-00571-5
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author Daiani Rodrigues Moreira
Tuan Henrique Smielevski de Souza
Douglas Galhardo
Cinthia Leão Figueira
Samara Calvi Baulli
Breno Gabriel da Silva
Francieli das Chagas
José Washington Santos Oliveira
Jean Samel Rocha
Angélica de Souza Khatlab
Eliane Gasparino
Vagner de Alencar Arnaut de Toledo
Adriana Aparecida Sinópolis Gigliolli
Maria Claudia Colla Ruvolo-Takasusuki
author_facet Daiani Rodrigues Moreira
Tuan Henrique Smielevski de Souza
Douglas Galhardo
Cinthia Leão Figueira
Samara Calvi Baulli
Breno Gabriel da Silva
Francieli das Chagas
José Washington Santos Oliveira
Jean Samel Rocha
Angélica de Souza Khatlab
Eliane Gasparino
Vagner de Alencar Arnaut de Toledo
Adriana Aparecida Sinópolis Gigliolli
Maria Claudia Colla Ruvolo-Takasusuki
author_sort Daiani Rodrigues Moreira
collection DOAJ
description Abstract Bees are essential pollinators that contribute to maintaining biodiversity and increasing agricultural production. However, by foraging on agricultural crops, bees may become contaminated with compounds used for pest control. In this study, we exposed bee (Apis mellifera L.) colonies to the insecticide imidacloprid (IMD) under field conditions to assess the occurrence of oxidative stress in larvae and pupae and investigate morphological changes in the fat body and midgut of larvae and midgut of adult bees. The apiary area was divided into three groups: control, commercial formulation containing IMD (Evidence® 700WG) (IMDCF), and IMD active ingredient (Sigma–Aldrich) (IMDAI). Treatment groups were fed syrup containing 1 µg L−1 IMD, whereas the control group was fed syrup only. Compared with the control, larvae exposed to IMDCF or IMDAI for 42 days exhibited morphological changes in the external body, midgut, and fat body. The midgut of adult bees contaminated with IMDCF showed only structural remnants of the peritrophic membrane and absence of regenerative cell nests. Oxidative stress analyses revealed that IMDCF-exposed larvae had higher nitrite and carbonylated protein contents and lower catalase and superoxide dismutase activity than control individuals. In pupae, IMDAI decreased catalase activity while increasing superoxide dismutase activity. These findings indicate that IMD has the potential to significantly impact the development of bees and their colonies by disrupting vital organs responsible for normal physiological functioning and overall activities of individuals. Oxidative stress, which was detected at different stages of bee development, may induce lipid, protein, and DNA oxidation, leading to cell death. Graphical Abstract
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spelling doaj-art-c783fd2b2bc74a119d25855747b3fd922025-01-26T12:15:51ZengBMCBiological Research0717-62872025-01-0158111510.1186/s40659-024-00571-5Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult beesDaiani Rodrigues Moreira0Tuan Henrique Smielevski de Souza1Douglas Galhardo2Cinthia Leão Figueira3Samara Calvi Baulli4Breno Gabriel da Silva5Francieli das Chagas6José Washington Santos Oliveira7Jean Samel Rocha8Angélica de Souza Khatlab9Eliane Gasparino10Vagner de Alencar Arnaut de Toledo11Adriana Aparecida Sinópolis Gigliolli12Maria Claudia Colla Ruvolo-Takasusuki13Department of Biotechnology, Genetics and Cell Biology, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Biotechnology, Genetics and Cell Biology, State University of MaringáDepartment of Exact Sciences, Escola Superior de Agricultura “Luiz de Queiroz” - University of São PauloDepartment of Biotechnology, Genetics and Cell Biology, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Animal Science, State University of MaringáDepartment of Biotechnology, Genetics and Cell Biology, State University of MaringáDepartment of Biotechnology, Genetics and Cell Biology, State University of MaringáAbstract Bees are essential pollinators that contribute to maintaining biodiversity and increasing agricultural production. However, by foraging on agricultural crops, bees may become contaminated with compounds used for pest control. In this study, we exposed bee (Apis mellifera L.) colonies to the insecticide imidacloprid (IMD) under field conditions to assess the occurrence of oxidative stress in larvae and pupae and investigate morphological changes in the fat body and midgut of larvae and midgut of adult bees. The apiary area was divided into three groups: control, commercial formulation containing IMD (Evidence® 700WG) (IMDCF), and IMD active ingredient (Sigma–Aldrich) (IMDAI). Treatment groups were fed syrup containing 1 µg L−1 IMD, whereas the control group was fed syrup only. Compared with the control, larvae exposed to IMDCF or IMDAI for 42 days exhibited morphological changes in the external body, midgut, and fat body. The midgut of adult bees contaminated with IMDCF showed only structural remnants of the peritrophic membrane and absence of regenerative cell nests. Oxidative stress analyses revealed that IMDCF-exposed larvae had higher nitrite and carbonylated protein contents and lower catalase and superoxide dismutase activity than control individuals. In pupae, IMDAI decreased catalase activity while increasing superoxide dismutase activity. These findings indicate that IMD has the potential to significantly impact the development of bees and their colonies by disrupting vital organs responsible for normal physiological functioning and overall activities of individuals. Oxidative stress, which was detected at different stages of bee development, may induce lipid, protein, and DNA oxidation, leading to cell death. Graphical Abstracthttps://doi.org/10.1186/s40659-024-00571-5Fat cellsField exposureHoney beeRedox system
spellingShingle Daiani Rodrigues Moreira
Tuan Henrique Smielevski de Souza
Douglas Galhardo
Cinthia Leão Figueira
Samara Calvi Baulli
Breno Gabriel da Silva
Francieli das Chagas
José Washington Santos Oliveira
Jean Samel Rocha
Angélica de Souza Khatlab
Eliane Gasparino
Vagner de Alencar Arnaut de Toledo
Adriana Aparecida Sinópolis Gigliolli
Maria Claudia Colla Ruvolo-Takasusuki
Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees
Biological Research
Fat cells
Field exposure
Honey bee
Redox system
title Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees
title_full Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees
title_fullStr Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees
title_full_unstemmed Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees
title_short Exposure of Apis mellifera (Hymenoptera: Apidae) colonies to imidacloprid impairs larval development, promotes oxidative stress in pupae, and induces changes in the midgut of adult bees
title_sort exposure of apis mellifera hymenoptera apidae colonies to imidacloprid impairs larval development promotes oxidative stress in pupae and induces changes in the midgut of adult bees
topic Fat cells
Field exposure
Honey bee
Redox system
url https://doi.org/10.1186/s40659-024-00571-5
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