Imidacloprid toxicity impairs spatial memory of echolocation bats through neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas

Abstract

It has been reported that the decimation of honey bees was because of pesticides of imidacloprid. The imidacloprid is a wildly used neonicotinoid insecticide. However, whether imidacloprid toxicity interferes with the spatial memory of echolocation bats is still unclear. Thus, we compared the spatial memory of Formosan leaf-nosed bats, Hipposideros terasensis, before and after chronic treatment with a low dose of imidacloprid. We observed that stereotyped flight patterns of echolocation bats that received chronic imidacloprid treatment were quite different from their originally learned paths. We further found that neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas of echolocation bats that received imidacloprid treatment was significantly enhanced in comparison with echolocation bats that received sham treatment. Thus, we suggest that imidacloprid toxicity may interfere with the spatial memory of echolocation bats through neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas. The results provide direct evidence that pesticide toxicity causes a spatial memory disorder in echolocation bats. This implies that agricultural pesticides may pose severe threats to the survival of echolocation bats.

The neonicotinoids acetamiprid and imidacloprid impair neurogenesis and alter the microglial profile in the hippocampal dentate gyrus of mouse neonates

“…These findings indicate that neonatal neonicotinoid exposure might have affected neuronal cells in the hippocampal DG, possibly resulting from the promotion of neuronal cell death in the SGZ and granule cell layer of the hippocampal DG. Neonicotinoid toxicity has been shown to induce apoptosis in several mammalian species (Babeìová et al, ; Hsiao, Lin, Lin, Wang, & Wu, ; Wang et al, ; Nakayama, Kagawa, & Hirata, personal communication, March 31, 2016). The population of immature granule cells is rather small compared with that of NeuN‐positive postmitotic neurons (Ohishi et al, ); therefore, a fluctuation in the number of these cells significantly influences the percentage of NeuN‐positive cells.…”

An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

“…In mammals, neurobehavioral effects included diminished learning ability (Kara et al 2015), enhanced social dominance and reduced aggression (Burke 2016), and disrupted spatial memory during echo-location in bats when exposed to imidacloprid (Hsiao et al 2016); deteriorated cognitive function in infants (Ozdemir et al 2014) and increased anxiety-like behavior (Hirano et al 2015) when exposed to clothianidin, and impaired memory following lactational exposure (Montanha et al 2016), disturbed maternal behaviors, such as aggression (Magalhaes et al 2015), and altered reflex development in offspring (Udo et al 2014) when exposed to fipronil. Exposure to imidacloprid also altered the regulation of genes important in mammalian brain development (Kimura-Kuroda et al 2016).…”

Population-level sensitivity to landscape variables reflects individual-based habitat selection in a woodland bat species

“…Direct and indirect effects of agriculture intensification have been proposed as one of the main cause implicated in the decline of various organisms (Bayat et al, 2014;Gibbons et al, 2014;Hallmann et al, 2014) including R. hipposideros (Bontadina et al, 2000;Wickramasinghe et al, 2004). Pesticides can have various additive or synergistic deleterious effects on survival and health of long-lived insectivorous bats (Hsiao et al, 2016). Their use in conventional farmlands reduces insect abundance and diversity (especially three key families for many insectivorous bats: lepidopteran, dipteran, coleopteran) compared to organic farmlands, the latter being more frequently used as foraging sites by R. hipposideros (Wickramasinghe et al, 2004).…”