Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera

Imidacloprid is a global health threat that severely poisons the economically and ecologically important honeybee pollinator, Apis mellifera. However, its effects on developing bee larvae remain largely unexplored. Our pilot study showed that imidacloprid causes developmental delay in bee larvae, bu...

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Main Authors: Zhi Li, Yuedi Wang, Qiqian Qin, Lanchun Chen, Xiaoqun Dang, Zhengang Ma, Zeyang Zhou
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/88772
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author Zhi Li
Yuedi Wang
Qiqian Qin
Lanchun Chen
Xiaoqun Dang
Zhengang Ma
Zeyang Zhou
author_facet Zhi Li
Yuedi Wang
Qiqian Qin
Lanchun Chen
Xiaoqun Dang
Zhengang Ma
Zeyang Zhou
author_sort Zhi Li
collection DOAJ
description Imidacloprid is a global health threat that severely poisons the economically and ecologically important honeybee pollinator, Apis mellifera. However, its effects on developing bee larvae remain largely unexplored. Our pilot study showed that imidacloprid causes developmental delay in bee larvae, but the underlying toxicological mechanisms remain incompletely understood. In this study, we exposed bee larvae to imidacloprid at environmentally relevant concentrations of 0.7, 1.2, 3.1, and 377 ppb. There was a marked dose-dependent delay in larval development, characterized by reductions in body mass, width, and growth index. However, imidacloprid did not affect on larval survival and food consumption. The primary toxicological effects induced by elevated concentrations of imidacloprid (377 ppb) included inhibition of neural transmission gene expression, induction of oxidative stress, gut structural damage, and apoptosis, inhibition of developmental regulatory hormones and genes, suppression of gene expression levels involved in proteolysis, amino acid transport, protein synthesis, carbohydrate catabolism, oxidative phosphorylation, and glycolysis energy production. In addition, we found that the larvae may use antioxidant defenses and P450 detoxification mechanisms to mitigate the effects of imidacloprid. Ultimately, this study provides the first evidence that environmentally exposed imidacloprid can affect the growth and development of bee larvae by disrupting molting regulation and limiting the metabolism and utilization of dietary nutrients and energy. These findings have broader implications for studies assessing pesticide hazards in other juvenile animals.
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spelling doaj.art-8ea0a566357b49fcbbab9c14c435e1202024-03-11T15:16:01ZengeLife Sciences Publications LtdeLife2050-084X2024-03-011210.7554/eLife.88772Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis melliferaZhi Li0https://orcid.org/0000-0003-1611-4873Yuedi Wang1Qiqian Qin2Lanchun Chen3Xiaoqun Dang4Zhengang Ma5Zeyang Zhou6College of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, ChinaCollege of Life Sciences, Chongqing Normal University, Chongqing, China; Key Laboratory of Pollinator Resources Conservation and Utilization of the Upper Yangtze River, Ministry of Agriculture and Rural Affairs, Chongqing, China; Chongqing Key Laboratory of Microsporidia Infection and Control, Chongqing, China; The State Key Laboratory of Resource Insects, Southwest University, Chongqing, ChinaImidacloprid is a global health threat that severely poisons the economically and ecologically important honeybee pollinator, Apis mellifera. However, its effects on developing bee larvae remain largely unexplored. Our pilot study showed that imidacloprid causes developmental delay in bee larvae, but the underlying toxicological mechanisms remain incompletely understood. In this study, we exposed bee larvae to imidacloprid at environmentally relevant concentrations of 0.7, 1.2, 3.1, and 377 ppb. There was a marked dose-dependent delay in larval development, characterized by reductions in body mass, width, and growth index. However, imidacloprid did not affect on larval survival and food consumption. The primary toxicological effects induced by elevated concentrations of imidacloprid (377 ppb) included inhibition of neural transmission gene expression, induction of oxidative stress, gut structural damage, and apoptosis, inhibition of developmental regulatory hormones and genes, suppression of gene expression levels involved in proteolysis, amino acid transport, protein synthesis, carbohydrate catabolism, oxidative phosphorylation, and glycolysis energy production. In addition, we found that the larvae may use antioxidant defenses and P450 detoxification mechanisms to mitigate the effects of imidacloprid. Ultimately, this study provides the first evidence that environmentally exposed imidacloprid can affect the growth and development of bee larvae by disrupting molting regulation and limiting the metabolism and utilization of dietary nutrients and energy. These findings have broader implications for studies assessing pesticide hazards in other juvenile animals.https://elifesciences.org/articles/88772honey beeApis melliferapesticidedevelopmental retardation
spellingShingle Zhi Li
Yuedi Wang
Qiqian Qin
Lanchun Chen
Xiaoqun Dang
Zhengang Ma
Zeyang Zhou
Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera
eLife
honey bee
Apis mellifera
pesticide
developmental retardation
title Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera
title_full Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera
title_fullStr Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera
title_full_unstemmed Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera
title_short Imidacloprid disrupts larval molting regulation and nutrient energy metabolism, causing developmental delay in honey bee Apis mellifera
title_sort imidacloprid disrupts larval molting regulation and nutrient energy metabolism causing developmental delay in honey bee apis mellifera
topic honey bee
Apis mellifera
pesticide
developmental retardation
url https://elifesciences.org/articles/88772
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