Abstract
The ongoing loss of global biodiversity is endangering ecosystem functioning and human food security. While environmental pollutants are well known to reduce fertility, the potential effects of common neonicotinoid insecticides on insect fertility remain poorly understood. Here, we show that field-realistic neonicotinoid exposure can drastically impact male insect fertility. In the laboratory, male and female solitary bees Osmia cornuta were exposed to four concentrations of the neonicotinoid thiamethoxam to measure survival, food consumption, and sperm traits. Despite males being exposed to higher dosages of thiamethoxam, females revealed an overall increased hazard rate for survival; suggesting sex-specific differences in toxicological sensitivity. All tested sublethal concentrations (i.e., 1.5, 4.5 and 10 ng g−1) reduced sperm quantity by 57% and viability by 42% on average, with the lowest tested concentration leading to a reduction in total living sperm by 90%. As the tested sublethal concentrations match estimates of global neonicotinoid pollution, this reveals a plausible mechanism for population declines, thereby reflecting a realistic concern. An immediate reduction in environmental pollutants is required to decelerate the ongoing loss of biodiversity.
Highlights
There is consensus that the ongoing loss of biodiversity is a defining feature of the Anthropocene (Dirzo et al, 2014; Ceballos et al, 2020; Wagner, 2020) with potentially drastic consequences for human food security and well-being (Díaz et al, 2019; Sala et al, 2000; Cardinale et al, 2012)
The data clearly show that the lowest exposure to a common neonicotinoid insecticide (0.49 ng) impaired male fertility of solitary bees, O. cornuta, by reducing total living sperm quantity by 90%
Our data suggest that male insect fertility can be adversely impacted by exposure to environmentally-relevant concentrations of thiamethoxam (Mitchell et al, 2017), an effect that could have far reaching consequences on insect populations
Summary
There is consensus that the ongoing loss of biodiversity is a defining feature of the Anthropocene (Dirzo et al, 2014; Ceballos et al, 2020; Wagner, 2020) with potentially drastic consequences for human food security and well-being (Díaz et al, 2019; Sala et al, 2000; Cardinale et al, 2012). Human population growth and increasing per capita consumption are considered to be the primary drivers of this decline, for instance through habitat loss (Dirzo et al, 2014; Ceballos et al, 2017), global warming (Soroye et al, 2020; Sales et al, 2018), or species invasions (van Kleunen et al, 2015). Environmental pollutants are another major factor and a notorious side-effect of unsustainable human population growth and food production (Carvalho, 2006; Horejs, 2020; Silva et al, 2019). A male infertility crisis, as suggested for humans over the past decades (Ravitsky and Kimmins, 2019; Agarwal et al, 2020), has been reported in various other taxa due to environmental pollutants (Whorton et al, 1976; Bretveld et al, 2007; Bal et al, 2012; Humann-Guilleminot et al, 2019); offering a plausible key mechanistic pathway contributing to the ongoing decline of biodiversity
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