Population-level variation in pesticide tolerance predicts survival under field conditions in mayflies.

An increasing number of studies have found tolerance variation in populations consistently exposed to contaminants, but few studies have examined whether these laboratory-derived estimates of tolerance have survival implications in field conditions. We examined four populations of the mayfly Stenacron interpunctatum for variation in tolerance to the common agricultural insecticide clothianidin. Using laboratory bioassays, we found a 2.3× range in 96 h EC50 tolerance values to clothianidin between our four populations. We then conducted a common-garden experiment with nymphs from each population placed into the collection stream most heavily impacted by upstream agricultural activities to assess whether our laboratory tolerance estimates predict survival under field conditions. We monitored survival and growth in situ for three weeks during the spring planting season, when clothianidin is applied to croplands upstream of our study site. While growth was similar across all groups, the most tolerant population, which was native to the impacted stream, had higher survival than the more sensitive populations. This suggests that population-level variation in contaminant tolerance as measured in laboratory bioassays could have real-world survival implications for sensitive aquatic macroinvertebrates in contaminated streams.

Exposure to clothianidin and predators increases mortality for heptageniidae.

Neonicotinoids are a class of insecticide with global impacts on natural environments. Due to their high solubility, they are frequently found in stream ecosystems where they have the potential to impact non-target biota. While environmental concentrations are generally below lethal levels for most organisms, there are concerns that sublethal exposures can impact aquatic insects, particularly mayflies, which are highly sensitive to neonicotinoids. Because sublethal doses of neonicotinoids can reduce mobility in mayflies, exposure could indirectly increase mortality due to predation by impairing their ability to avoid initial detection or escape predators. We examined whether exposure to the neonicotinoid clothianidin at a concentration below the 96-h EC50 (7.5 µg/L), would increase the predation risk of Stenacron and Stenonema mayfly nymphs by larval southern two-lined salamanders (Eurycea cirrigera) or eastern dobsonfly nymphs (Corydalus cornutus) using a controlled laboratory experiment. For Stenacron, we found significant interactive effects between pesticide and dobsonfly exposure that increased the hazard ratio (HR). The HR assesses risk relative to a control population, in this case mayflies in similar experimental conditions but without exposure to neonicotinoids or predators. With the addition of clothianidin, the HR of mayflies exposed to a dobsonfly nymph significantly increased from 1.8 to 6.2 while the HR for those exposed to salamanders increased from 7.6 to 12.5. For Stenonema, the HR initially decreased due to dobsonfly exposure (1 to 0.3) but increased when clothianidin and dobsonflies were combined (0.3 to 1.6). Our study shows that aquatic exposure to clothianidin can increase mortality for aquatic insects through predator pressure. Such indirect effects associated with neonicotinoid exposure warrant further investigation to expand our understanding of pesticide impacts to aquatic systems.

Population-level variation in neonicotinoid tolerance in nymphs of the Heptageniidae.

Anthropogenic activities can have significant ecological and evolutionary consequences on populations and communities. In the United States, neonicotinoid insecticides are widespread across the agricultural Midwest and frequently detected in stream systems. Their effect on Heptageniidae mayflies is a major concern because they are highly sensitive to neonicotinoids and have some of the lowest reported tolerance values of any organism. Our objective was to evaluate population-level variation in neonicotinoid sensitivity. We did so by conducting 96 h half maximal effective concentration (EC5096-h) tests for the neonicotinoids clothianidin and thiamethoxam on populations of Stenacron, Stenonema, and Maccaffertium mayflies and testing for associations with agricultural landcover. Additionally, we collected water samples to assess temporal patterns of neonicotinoid presence in stream habitats. We found variation in neonicotinoid tolerance with EC50 values ranging from 4.9 µg/L to 32 µg/L and 19.8 µg/L to 86.5 µg/L for clothianidin and thiamethoxam, respectively. Agricultural landcover was associated with neonicotinoid tolerance for Stenacron and thiamethoxam but not for other comparisons. Moreover, water samples demonstrated that the amount of agricultural landcover was not a strong predictor of neonicotinoids presence in streams. Our data suggest that populations of Heptageniidae mayflies can vary substantially in neonicotinoid tolerance. Population-level variation should be considered in toxicity assessments and presents the potential for evolved tolerance.