Carry-Over Effects Across Metamorphosis of a Pesticide on Female Lifetime Fitness Strongly Depend on Egg Hatching Phenology: A Longitudinal Study under Seminatural Conditions

Abstract

Current ecological risk assessment of pesticides fails to protect aquatic biodiversity. For the first time, we tested two potential reasons for this failure with regard to carry-over effects across metamorphosis: their dependence on hatching period, and the lack of studies quantifying adult fitness under seminatural conditions. Using the damselfly Coenagrion puella sampled from six populations, we designed an outdoor longitudinal one-year study starting from the egg stage. We exposed the aquatic larvae to the pesticide esfenvalerate (0.11 μg/L) during the initial microcosm part. Next, we monitored the lifetime fitness of the terrestrial adults in an insectary. Exposure to the pesticide negatively impacted not only larval traits, but also drastically reduced lifetime mating success of adult females. The impact of this postmetamorphic effect of the pesticide on the population level was three times more important than the effects in the larval stage. Importantly, this carry-over effect was only present in females that hatched early in the season, and was not mediated by metamorphic traits (age and mass at emergence). We provide proof-of-principle under seminatural conditions for two potential pitfalls that need to be considered when improving risk assessment: carry-over effects on adult fitness can (i) be much more important than effects during the larval stage and may not be captured by metamorphic traits, and (ii) be strongly modulated by egg hatching dates.