Abstract
Dragonflies, Sympetrum spp., are indispensable to agriculture and are a central element of culture in Japan. However, S. frequens populations in rice paddy fields have declined in recent decades. Dragonfly larvae are predatory aquatic insects that feed on other organisms found in habitats with slow-moving or standing water. The increasing use of fipronil and neonicotinoid insecticides in agriculture is also increasing exposure to Sympetrum spp. in larval stages through paddy soil and water. The role of fipronil insecticides in the decline of dragonflies is of concern, and we here examine the sublethal effects of this insecticide on the feeding behaviors of two Sympetrum spp. Based on the quantity of prey items consumed and the time to capture prey items, feeding inhibition was determined to be a potential mechanism of the decline of Sympetrum spp. following 48-h exposure to fipronil and fipronil sulfone. Prey consumption by S. infuscatum was significantly reduced for fipronil sulfone at all concentrations (0.01–1000 μg/L). S. frequens exposed to 1, 10, 100 and 1000 μg/L fipronil sulfone had significantly longer prey capture times. Fipronil sulfone was 2.8, 9.7 and 10.5 times more toxic to S. infuscatum than fipronil in terms of acute toxicity, feeding inhibition and delayed toxicity, respectively. In addition, fipronil sulfone was 6.6, 2.9 and 9.1 times more toxic, respectively, to S. frequens than fipronil. Our findings suggest that sublethal effects on feeding inhibition lead to severe mortality at realistic paddy soil and water concentrations. Our results provide the first demonstration that short-term exposure to fipronil and fipronil sulfone can consequently cause significant harm to dragonfly larvae survival due to feeding inhibition. These findings have implications for current pesticide risk assessment and dragonfly protection.
Highlights
The use of insecticides in agriculture is increasing worldwide [1] and is increasing the exposure of non-target aquatic animals through processes like runoff in paddy fields
Body size of instar 2 larvae of S. infuscatum and S. frequens were smaller in head width by 0.6 mm and 0.4 mm, respectively, and in body length by 1.7 mm and 1.6 mm, respectively [43]
S. infuscatum larvae exposed to a sublethal concentration of fipronil sulfone demonstrated insufficient feeding behavior and had high mortality to instar 3 (Fig 3C)
Summary
The use of insecticides in agriculture is increasing worldwide [1] and is increasing the exposure of non-target aquatic animals through processes like runoff in paddy fields. Dragonflies (Sympetrum spp.) are indispensable to agriculture and are a central element of culture in Japan [2]. Sympetrum frequens is important for several reasons. This species is one of the most effective. Effects of sublethal fipronil metabolite on dragonfly feeding activity predators of rice insect pests, such as the beetles Lissorhoptrus oryzophilus and Oulema oryzae, partly because of the high density of this dragonfly species in rice fields during the rice-growing season [3]. S. frequens abundance has declined by 1% over the past 20 years [5], and several reports suggest that nursery-box application of fipronil is a major cause of the decline of dragonfly nymph numbers in rice paddy fields [6,7]
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