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Exposure to Cyantraniliprole Adversely Impacts Fitness of Harmonia axyridis: Acute Toxicity and Sublethal Effects on Development, Fecundity and Antioxidant Responses
by
Tianshu Zhang
1,2,†,
Yongda Yuan
1,2,†,
Haiyuan Teng
1,2,
Dongsheng Wang
1,2 and
Haotian Gu
1,2,* 1
Shanghai Key Laboratory of Protected Horticultural Technology, Eco-Environmental Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai 201403, China
2
Shanghai Engineering Research Centre of Low-Carbon Agriculture (SERCLA), Shanghai 201415, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Insects 2024, 15(10), 773; https://doi.org/10.3390/insects15100773 (registering DOI)
Submission received: 16 August 2024
/
Revised: 30 September 2024
/
Accepted: 2 October 2024
/
Published: 6 October 2024
(This article belongs to the Section Insect Physiology, Reproduction and Development)
Simple Summary
CNAP is a novel anthranilic diamide insecticide and its toxicological profiles pertaining to ladybird beetles remain largely uncharacterized. Through dipping method and topical application, we comprehensively evaluated acute toxicity and sublethal effects of CNAP against Harmonia axyridis, a predacious coccinellid commonly utilized in integrated pest management (IPM). Our outcomes indicated that CNAP was moderately toxic to H. axyridis and most noxious to 1st-instar larvae, with the least LC50 of 86.11 mg/L. When eggs and 1st instars were treated with LC30 CNAP, embryonic, larval and pupal durations all significantly dropped, accompanied by reduced pupal weight and pupation rate. Post sublethal treatments on newly emerged females, reproductive proxies displayed dose-effect responses, with daily spawning and vitellin level substantially diminished and the pre-oviposition period retarded. In addition, sublethal exposure to CNAP profoundly disrupted the antioxidant system of females, as evidenced by an induced hormesis effect at LC10 and impaired enzymatic activities at LC30 over time. Taken together, this study revealed the prospective ecological risk of CNAP and its adverse implications for H. axyridis fitness. As such, the practical compatibility of agrochemicals with biocontrol agents should be well assessed before being embraced into IPM for pest control.
Abstract
Extensive utilization of pesticides and their persistent residues inadvertently pose threats to the effectiveness and fitness of biocontrol agents in agroecosystems. However, these ecological consequences are generally disregarded when executing integrated pest management strategies (IPM). Cyantraniliprole (CNAP) serves as a wide-spectrum diamide insecticide and its sublethal effects have been well characterized on multiple insect pests, whereas its impacts on beneficial natural enemies remain unfathomed. Herein we exposed Harmonia axyridis, a predacious generalist, to lethal and sublethal concentrations of CNAP via dipping treatment (egg stage) and topical applications (1st-instar stage + adult stage). The acute toxicity tests revealed that LC50 of CNAP were 90.11, 86.11 and 240.50 mg/L against embryos, 1st instar nymphs and female adults, respectively, with safety factors ranging from 1.14 to 5.34, suggesting its medium toxicity for H. axyridis and larval stage was the most susceptible. The embryonic, larval and pupal durations of coccinellids ecdysed from CNAP-treated eggs and 1st instars were all elongated under sublethal concentrations, of which LC30 triggered more pronounced and significant retardations relative to control. Besides, exposed coccinellids displayed substantially diminished pupal mass and pupation rate, most notably for insects molted from the 1st-instar stage upon CNAP sublethal treatments. With respect to reproductive performance, LC10 and LC30 of CNAP all significantly suppressed female fecundity, as evidenced by reduced vitellin content, a prolonged pre-oviposition period (POP), mitigated laid eggs and the egg hatching rate. Specifically, there existed positive correlations between vitellin level (Vn) and number of eggs deposited by per female, indicative of CNAP affecting fecundity by regulation of Vn. In addition, the antioxidant system was also profoundly disrupted by CNAP, with compromised POD activity at different concentrations over time and induced hormesis of SOD/CAT activities post LC10 exposure. Activities of SOD and TAC were enhanced to exert protective functions during the first 48 h, while defense collapsed at 72 h following LC30 treatments that depleted all enzymatic activities. We speculated that fitness trade-offs may occur between reproductive capacity and antioxidant defenses to sustain physiological homeostasis in response to CNAP stress. Collectively, this study evaluated the ecological risk of CNAP and unmasked its adverse implications for overall fitness of H. axyridis, which highlighted rational application of agrochemicals to conserve biocontrol agents when implementing IPM strategies for sustainable pest control.
