Pesticide and resource stressors additively impair wild bee reproduction

Abstract

Bees and other beneficial insects experience multiple stressors within agricultural landscapes that act together to impact their health and diminish their ability to deliver the ecosystem services on which human food supplies depend. Disentangling the effects of coupled stressors is a primary challenge for understanding how to promote their populations and ensure robust pollination and other ecosystem services. We used a crossed design to quantify the individual and combined effects of food resource limitation and pesticide exposure on the survival, nesting, and reproduction of the blue orchard bee Osmia lignaria . Nesting females in large flight cages accessed wildflowers at high or low densities, treated with or without the common insecticide, imidacloprid. Pesticides and resource limitation acted additively to dramatically reduce reproduction in free-flying bees. Our results emphasize the importance of considering multiple drivers to inform population persistence, management, and risk assessment for the long-term sustainability of food production and natural ecosystems.

Positive Correlation between Pesticide Consumption and Longevity in Solitary Bees: Are We Overlooking Fitness Trade-Offs?

“…While no significant differences in feeding behavior and relative daily consumption were observed across treatments, a significant positive correlation between increased food intake during the first 10 days (i.e., exposure period) and longevity was observed for all treatments and controls. While we have no data to support that fitness may be affected, previous studies using comparable concentrations of neonicotinoid insecticides have revealed a reduced reproduction, but no effects on adult survival [ 10 , 11 ]. Therefore, we postulate that exposed bees may opt for improved longevity over reproductive capacities (i.e., fitness) [ 28 , 51 ].…”

“…Irrespective of the underlying mechanism, the consequence of increased survival is likely to trade-off for other physiological factors [ 69 ], possibly affecting fitness [ 30 , 63 ]. Indeed, ample evidence exists from the laboratory and the field indicating such trade-off scenarios, wherein pesticide exposure decreased fitness parameters while not necessarily affecting survival [ 10 , 11 , 70 ]. Undoubtedly, our experiment would have benefited from directly measuring detoxification capacities and fitness (i.e., production of offspring) or sublethal parameters that adequately reflect fitness (i.e., ovary development in females or sperm quality in males) to confirm a possible trade-off scenario in solitary bees.…”

“…Sublethal effects induced by pesticide exposure can affect a wide spectrum of physiological as well as behavioral traits, including biochemical and enzymatic processes, neurophysiology (i.e., learning and orientation), ontogenesis, immune capacities, or reproductive traits [ 7 ]. In light of evolutionary biology, sublethal effects on fitness are likely to have detrimental consequences [ 8 ], and such effects are known to occur after neonicotinoid exposure [ 9 , 10 , 11 ]. Neonicotinoid insecticides and glyphosate-based herbicides are among the most common and widely applied pesticides in current agricultural practices [ 12 ], and are very likely to be found in combination [ 13 ].…”

Integrating animal behaviour into research on multiple environmental stressors: a conceptual framework

“…If this substantially reduces average offspring survival (e.g., if offspring survival falls over a fitness cliff), then adult exposure to stressors can result in a large indirect cost in terms of both offspring and adult fitness. For example, blue orchard bees (Osmia lignaria ) exposed to resource limitation and the pesticide imidacloprid suffered an additive reduction in reproductive fitness via a lowered probability of successful nesting and a reduced number of offspring produced (Stuligross & Williams 2020). Additionally, offspring sex ratios became male biased, increasing the likelihood of further reductions in reproductive fitness in the future (Stuligross & Williams 2020).…”

No impact of neonicotinoids on male solitary bees Osmia cornuta under semi‐field conditions

“…The few studies addressing the impact of neonicotinoid exposure on reproductive physiology have primarily focused on honey bees or female solitary bees (Williams et al ., 2015; Chaimanee et al ., 2016; Straub et al ., 2016; Wu‐Smart & Spivak, 2018; Azpiazu et al ., 2019), whereas data for male wild bees are currently lacking. However, impaired male reproductive physiology may be a key mechanistic explanation for observed severe negative consequences of field‐realistic neonicotinoid exposure on solitary bee fitness and population density (Sandrock et al ., 2014; Rundlöf et al ., 2015; Stuligross & Williams, 2020).…”