The sublethal effects of ethiprole on the development, defense mechanisms, and immune pathways of honeybees ( Apis melli

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ORIGINAL PAPER

The sublethal effects of ethiprole on the development, defense mechanisms, and immune pathways of honeybees (Apis mellifera L.) Yueyue Liu . Chen Wang . Suzhen Qi . Jiang He . Yingchen Bai

Received: 17 March 2020 / Accepted: 25 September 2020 Ó Springer Nature B.V. 2020

Abstract Ethiprole has been widely used in agriculture, but there have been few studies on the adverse effects of ethiprole on nontarget organisms. This study focused on the mechanism of the sublethal effects of ethiprole on the development, antioxidation mechanisms, detoxification mechanisms and immune-related gene expression of honeybees (Apis mellifera L.). Honeybee larvae were found to be more sensitive than pupae to ethiprole. It was found that ethiprole inhibited the pupation and eclosion of bee larvae in a dose-dependent manner, with ethiprole doses of 1 9 10–3 mg/L decreasing pupation and eclosion rates to 50.00 ± 8.84% and 20.83 ± 10.62%,

Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10653-020-00736-7) contains supplementary material, which is available to authorized users.

respectively. The activities of antioxidative enzymes (superoxide dismutase and catalase) and detoxification factors (glutathione and glutathione S-transferase) were also significantly increased in ethiprole-exposed honeybees, indicating that a sublethal dose of ethiprole also induced oxidative stress in honeybees. In the 1 9 10–3 mg/L ethiprole-exposure group, the expression of pathogen recognition-related gene PGRP-4300 was upregulated 11.10 ± 0.45-fold, and that of detoxification-related gene CYP4G11 was upregulated 8.84 ± 0.11-fold, indicating that ethiprole induced an immune reaction in honeybees. To the best our knowledge, this study represents the first demonstration that sublethal concentrations of ethiprole inhibit honeybee development and activate honeybee defense and immune systems. Keywords Ethiprole  Honeybees  Chronic effects  Detoxification  Immune reaction

Y. Liu  J. He Lab of Environmental Geochemistry, College of Ecology and Environment, Inner Mongolia University, Hohhot 010000, China

Introduction Y. Liu  C. Wang (&)  Y. Bai State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China e-mail: [email protected] S. Qi (&) Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China e-mail: [email protected]

Honeybees are responsible for most of insect pollination of agricultural ecosystems (A. M. Klein et al. 2007), and thus play an essential role in ecosystem functioning and agricultural production (A. Klein et al. 2003). In this context, it is notable and concerning that instances of honeybee colony collapse disorder (CCD) have been frequently reported in the United States and

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Environ Geochem Health

Canada over the past decade (Johnson et al. 2010; Kevan et al. 2007). Recent studies have suggested tha