Involvement of oxygenase confers higher resistance to neonicotinoid insecticides in estuarine resident sand shrimp Crang

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ORIGINAL ARTICLE Environment

Involvement of oxygenase confers higher resistance to neonicotinoid insecticides in estuarine resident sand shrimp Crangon uritai than in kuruma prawn Penaeus japonicus and mysid Americamysis bahia Takeshi Hano1   · Katsutoshi Ito1 · Nobuyuki Ohkubo1 · Mana Ito1 · Akio Watanabe2 · Hideo Sakaji3 Received: 20 June 2020 / Accepted: 13 September 2020 © Japanese Society of Fisheries Science 2020

Abstract Globally, neonicotinoid contamination in aquatic environments, including estuarine areas, is a prevailing environmental concern. The estuarine resident marine crustacean sand shrimp Crangon uritai was previously found to have a higher tolerance to neonicotinoids than the marine crustaceans kuruma prawn Penaeus japonicus and mysid Americamysis bahia. Based on these findings, we aimed to explore the mechanisms underlying their differences in insecticide sensitivity. We hypothesized that differences in the structures of their nicotinic acetylcholine receptors (nAChRs) and/or the involvement of a metabolizing enzyme may confer sand shrimp resistance to neonicotinoids. No obvious differences were found in the amino acid residue (position 81) of the loop D region of the nAChR β-subunit among the three crustaceans. A synergistic toxicity bioassay was used to explore candidate metabolizing enzymes, esterase, glutathione S-transferase, and oxygenase. The three species were exposed to two neonicotinoids (acetamiprid and clothianidin) at concentrations equivalent to 1/15–1/10 of 96-h L ­ C50 values and synergists (inhibitors of metabolizing enzyme) or combinations of both. Treatments with the oxygenase inhibitor and the neonicotinoids resulted in increased mortality in sand shrimps but not in kuruma prawns or mysids. Consequently, it was determined that oxygenase may explain the higher resistance of the sand shrimp to neonicotinoid insecticides. Keywords  Neonicotinoid insecticide · Sensitivity · Oxygenase · Nicotinic acetylcholine receptors (nAChRs) · Sand shrimp · Kuruma prawn · Mysid

* Takeshi Hano [email protected] Katsutoshi Ito [email protected] Nobuyuki Ohkubo [email protected] Mana Ito [email protected] Akio Watanabe watanabe‑[email protected]

1



Fisheries Research and Education Agency, National Research Institute of Fisheries and Environment of Inland Sea, 2‑17‑5 Maruishi, Hatsukaichi, Hiroshima 739‑0452, Japan

2



Fisheries Research Center, Forestry and Fisheries, Ehime Research Institute of Agriculture, 1611 Tanbara‑chou Ikeda, Saijyo, Ehime 791‑0508, Japan

3



Japan Fisheries Research and Education Agency, National Research Institute of Fisheries Science, 2‑12‑4 Fukuura, Kanazawa, Yokohama 236‑8648, Japan

Hideo Sakaji [email protected]

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Introduction Over the past two decades, environmental concerns regarding neonicotinoid insecticides have increased due to their extreme toxicity to non-target and vulnerable aquatic organisms (Morrissey et  al. 2015). They have been detected in agricultural surface waters and rivers at microgram-per-liter le