The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages

The red imported fire ant (RIFA), <i>Solenopsis invicta</i>, is an invasive pest that causes damage to agricultural and ecological environments worldwide. Fluralaner is a new isoxazoline pesticide with the potential to become a control agent against RIFA. However, it is not clear whether...

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Main Authors: Leyi Shao, Wei Wang, Xin Gong, Yinghao Yu, Junao Xue, Xinnian Zeng, Jiali Liu
Format: Article
Language:English
Published: MDPI AG 2023-10-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/21/15627
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author Leyi Shao
Wei Wang
Xin Gong
Yinghao Yu
Junao Xue
Xinnian Zeng
Jiali Liu
author_facet Leyi Shao
Wei Wang
Xin Gong
Yinghao Yu
Junao Xue
Xinnian Zeng
Jiali Liu
author_sort Leyi Shao
collection DOAJ
description The red imported fire ant (RIFA), <i>Solenopsis invicta</i>, is an invasive pest that causes damage to agricultural and ecological environments worldwide. Fluralaner is a new isoxazoline pesticide with the potential to become a control agent against RIFA. However, it is not clear whether <i>S. invicta</i> responds the same way to fluralaner at different reproductive stages. The present study firstly evaluated the toxicity of fluralaner to <i>S. invicta</i> at different developmental stages, finding that fourth instar larvae (LD<sub>50</sub>, 1744.23 mg/kg) and worker ants (LD<sub>50</sub>, 8.62 mg/kg) were differently susceptible to fluralaner, while the mortality rate of fourth instar larvae was significantly lower at the same concentration of 10 mg/L (5.56 ± 3.14%) than that of worker ants (62.22 ± 3.14%), demonstrating a greater tolerance to fluralaner. Subsequently, the metabolic responses of worker and larval ants to fluralaner stress (10 mg/L) were investigated using non-targeted metabolomics, which indicated that the amount of differential metabolites and the KEGG metabolic pathways enriched were different between workers and larvae when exposed to the same dose (10 mg/L) of fluralaner. Differential metabolites of larvae and worker ants under fluralaner stress were mainly concentrated in organic acids and their derivatives, lipids and lipid-like molecules, nucleosides, nucleotides, and analogues, combined with the enriched metabolic pathways, revealed that the differential metabolic responses of larvae and worker ants were mainly in energy metabolism, detoxification metabolism, and neurotransmitter ligands. Workers consumed more substrates in the arginine synthesis pathway (<span style="font-variant: small-caps;">l</span>-glutamic acid, <span style="font-variant: small-caps;">l</span>-aspartic acid, and fumaric acid) to provide energy for the detoxification (glutathione) of pesticides when exposed to fluralaner stress, and the high accumulation of <span style="font-variant: small-caps;">l</span>-aspartic acid induced excitotoxicity in the worker ants. Larval ants consumed more arachidonic acid to synthesize PG D2, and changes in the metabolism of antioxidants such as catechins, hesperidin, and <span style="font-variant: small-caps;">l</span>-ascorbic acid suggested that larvae were more capable of scavenging the ROS response than worker ants. The results of non-targeted metabolomics successfully revealed differences in the sensitivity of larvae and workers to fluralaner agents, providing insights into the fluralaner control of <i>Solenopsis invicta</i>.
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spelling doaj.art-cd658b1a0f1e4c4dbe1b6973aff4bd892023-11-10T15:04:41ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-10-0124211562710.3390/ijms242115627The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental StagesLeyi Shao0Wei Wang1Xin Gong2Yinghao Yu3Junao Xue4Xinnian Zeng5Jiali Liu6College of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaCollege of Plant Protection, South China Agricultural University, Guangzhou 510642, ChinaThe red imported fire ant (RIFA), <i>Solenopsis invicta</i>, is an invasive pest that causes damage to agricultural and ecological environments worldwide. Fluralaner is a new isoxazoline pesticide with the potential to become a control agent against RIFA. However, it is not clear whether <i>S. invicta</i> responds the same way to fluralaner at different reproductive stages. The present study firstly evaluated the toxicity of fluralaner to <i>S. invicta</i> at different developmental stages, finding that fourth instar larvae (LD<sub>50</sub>, 1744.23 mg/kg) and worker ants (LD<sub>50</sub>, 8.62 mg/kg) were differently susceptible to fluralaner, while the mortality rate of fourth instar larvae was significantly lower at the same concentration of 10 mg/L (5.56 ± 3.14%) than that of worker ants (62.22 ± 3.14%), demonstrating a greater tolerance to fluralaner. Subsequently, the metabolic responses of worker and larval ants to fluralaner stress (10 mg/L) were investigated using non-targeted metabolomics, which indicated that the amount of differential metabolites and the KEGG metabolic pathways enriched were different between workers and larvae when exposed to the same dose (10 mg/L) of fluralaner. Differential metabolites of larvae and worker ants under fluralaner stress were mainly concentrated in organic acids and their derivatives, lipids and lipid-like molecules, nucleosides, nucleotides, and analogues, combined with the enriched metabolic pathways, revealed that the differential metabolic responses of larvae and worker ants were mainly in energy metabolism, detoxification metabolism, and neurotransmitter ligands. Workers consumed more substrates in the arginine synthesis pathway (<span style="font-variant: small-caps;">l</span>-glutamic acid, <span style="font-variant: small-caps;">l</span>-aspartic acid, and fumaric acid) to provide energy for the detoxification (glutathione) of pesticides when exposed to fluralaner stress, and the high accumulation of <span style="font-variant: small-caps;">l</span>-aspartic acid induced excitotoxicity in the worker ants. Larval ants consumed more arachidonic acid to synthesize PG D2, and changes in the metabolism of antioxidants such as catechins, hesperidin, and <span style="font-variant: small-caps;">l</span>-ascorbic acid suggested that larvae were more capable of scavenging the ROS response than worker ants. The results of non-targeted metabolomics successfully revealed differences in the sensitivity of larvae and workers to fluralaner agents, providing insights into the fluralaner control of <i>Solenopsis invicta</i>.https://www.mdpi.com/1422-0067/24/21/15627contacting activityfluralaner stressinvasive pestmetabolometolerance
spellingShingle Leyi Shao
Wei Wang
Xin Gong
Yinghao Yu
Junao Xue
Xinnian Zeng
Jiali Liu
The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages
International Journal of Molecular Sciences
contacting activity
fluralaner stress
invasive pest
metabolome
tolerance
title The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages
title_full The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages
title_fullStr The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages
title_full_unstemmed The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages
title_short The Toxicity Differences of Fluralaner against the Red Imported Fire Ant (<i>Solenopsis invicta</i>) at Different Developmental Stages
title_sort toxicity differences of fluralaner against the red imported fire ant i solenopsis invicta i at different developmental stages
topic contacting activity
fluralaner stress
invasive pest
metabolome
tolerance
url https://www.mdpi.com/1422-0067/24/21/15627
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