Past insecticide exposure reduces bee reproduction and population growth rate

Pesticides are linked to global insect declines, with impacts on biodiversity and essential ecosystem services. In addition to well-documented direct impacts of pesticides at the current stage or time, potential delayed “carryover” effects from past exposure at a different life stage may augment impacts on individuals and populations. We investigated the effects of current exposure and the carryover effects of past insecticide exposure on the individual vital rates and population growth of the solitary bee, Osmia lignaria. Bees in flight cages freely foraged on wildflowers, some treated with the common insecticide, imidacloprid, in a fully crossed design over 2 y, with insecticide exposure or no exposure in each year. Insecticide exposure directly to foraging adults and via carryover effects from past exposure reduced reproduction. Repeated exposure across 2 y additively impaired individual performance, leading to a nearly fourfold reduction in bee population growth. Exposure to even a single insecticide application can have persistent effects on vital rates and can reduce population growth for multiple generations. Carryover effects had profound implications for population persistence and must be considered in risk assessment, conservation, and management decisions for pollinators to mitigate the effects of insecticide exposure.

Adult body size measurement redundancies in Osmia lignaria and Megachile rotundata (Hymenoptera: Megachilidae)

Metrics to assess relative adult bee body size have included both mass and morphometrics, but these metrics may not equally or reliably estimate body size for all bee species and in all situations, due to bee age, diet, and/or environment. Understanding the relationships between different metrics and possible redundancies in the information they afford is important but not always known. Body size measurements provide valuable data for interpreting research outcomes for managed solitary bees, including Osmia lignaria Say and Megachile rotundata F. (Hymenoptera: Megachilidae). Applied studies of these important and readily available U.S. crop pollinators focus on refining commercial management practices, and basic empirical studies in various scientific disciplines (from genomics to ecology) employ them as model systems to study solitary bees. To examine common metrics of body size, we measured head capsule width (HCW), intertegular distance (ITD), and fresh and dry weights of newly emerged adults of both species. Using linear and exponential models, we determined relationships between these body size metrics. For M. rotundata, linear models best described relationships between ITD and all other metrics, and between HCW and fresh and dry weights. For O. lignaria, linear models best fit relationships between all metrics except for fresh weight with both ITD and HCW, which were fitted better with exponential models. For both species, model fits were strongest when males and females were pooled. Depending on the study question, knowing that only one metric may reliably measure body size can simplify evaluations of O. lignaria and M. rotundata responses to artificial or environmental variables.

Eristalis flower flies can be mechanical vectors of the common trypanosome bee parasite, Crithidia bombi

Flowers can be transmission platforms for parasites that impact bee health, yet bees share floral resources with other pollinator taxa, such as flies, that may be hosts or non-host vectors (i.e., mechanical vectors) of parasites. Here, we assessed whether the fecal-orally transmitted gut parasite of bees, Crithidia bombi, can infect Eristalis tenax flower flies. We also investigated the potential for two confirmed solitary bee hosts of C. bombi, Osmia lignaria and Megachile rotundata, as well as two flower fly species, Eristalis arbustorum and E. tenax, to transmit the parasite at flowers. We found that C. bombi did not replicate (i.e., cause an active infection) in E. tenax flies. However, 93% of inoculated flies defecated live C. bombi in their first fecal event, and all contaminated fecal events contained C. bombi at concentrations sufficient to infect bumble bees. Flies and bees defecated inside the corolla (flower) more frequently than other plant locations, and flies defecated at volumes comparable to or greater than bees. Our results demonstrate that Eristalis flower flies are not hosts of C. bombi, but they may be mechanical vectors of this parasite at flowers. Thus, flower flies may amplify or dilute C. bombi in bee communities, though current theoretical work suggests that unless present in large populations, the effects of mechanical vectors will be smaller than hosts.

Eristalis (Diptera: Syrphidae) Flower Flies are Potential Non-host Vectors of the Common Trypanosome Bee Parasite, Crithidia Bombi

Flowers can be transmission platforms for parasites that impact bee health, yet bees share floral resources with other pollinator taxa, such as flies, that could be hosts or non-host vectors (i.e., mechanical vectors) of parasites. Here, we assessed whether the fecal-orally transmitted gut parasite of bees, Crithidia bombi, can infect Eristalis tenax flower flies. We also investigated the potential for two confirmed solitary bee hosts of C. bombi, Osmia lignaria and Megachile rotundata, as well as two flower fly species, Eristalis arbustorum and E. tenax, to transmit the parasite at flowers. We found that C. bombi did not replicate (i.e., cause an active infection) in E. tenax flies. However, 93% of inoculated flies defecated live C. bombi in their first fecal event, and all contaminated fecal events contained C. bombi at concentrations sufficient to infect bumble bees. Flies and bees defecated inside the corolla (flower) more frequently than other plant locations, and flies defecated at volumes comparable to or greater than bees. Our results demonstrate that Eristalis flower flies are not hosts of C. bombi, but they may be mechanical vectors of this parasite at flowers. Thus, flower flies may amplify or dilute C. bombi in bee communities.

Whole-Body Acute Contact Toxicity of Formulated Insecticide Mixtures to Blue Orchard Bees (Osmia lignaria)

Blue orchard bees, [Osmia lignaria (Say) (Hymenoptera: Megachilidae)], have been developed as an important pollinator for orchard crops in North America over the last 40 years. The toxicity of several pesticides to O. lignaria and other Osmia species has been previously reported. However, the field-realistic toxicity of formulated premix insecticides comprised of multiple active ingredients (each with a different mode of action) to O. lignaria has not been assessed. Here, we use a customized spray tower in a laboratory setting to assess adult male and female whole-body direct contact exposure to four formulated pesticide mixtures: thiamethoxam + lambda-cyhalothrin (TLC), imidacloprid + beta-cyfluthrin (IBC), chlorantraniliprole + lambda-cyhalothrin (CLC) and methoxyfenozide + spinetoram (MS) by directly spraying anesthetized bees in Petri dishes. Separately, adult male and female whole-body direct contact exposure to formulated imidacloprid (I), beta-cyfluthrin (BC) and their 1:1 binary combination (IBC) was assessed using the same experimental method. Resulting mortality in each study was screened up to 96 h post-treatment to determine acute whole-body contact toxicity. In the first study, TLC and IBC resulted in statistically higher mortality at 24 and 48 h than the two other insecticide combinations tested. The CLC and MS combinations were slower acting and the highest mortality for O. lignaria exposed to these mixtures was recorded at 96 h. We did observe significant differences in toxicity between CLC and MS. In the second study, exposure to the 1:1 binary combination of IBC caused overall significantly higher mortality than exposure to I or BC alone. Both active ingredients alone, however, demonstrated equivalent levels of mortality to the 1:1 binary combination treatment at the 96 h observation reading, indicating increased speed of kill, but not necessarily increased toxicity. Significant differences in the onset of mortality following acute contact whole-body exposure to the formulated insecticide mixtures and individual active ingredients tested were consistently observed across all experiments in both studies.

Neurotoxic alkaloid in pollen and nectar excludes generalist bees from foraging at death-camas, Toxicoscordion paniculatum (Melanthiaceae)

Many plants produce broadly active toxins to which specialist herbivores—typically insects—have evolved counter-adaptations, sometimes spawning co-evolutionary arms races. Many non-social bee species are likewise taxonomic host specialists, but the specialists’ pollen hosts frequently attract diverse floral generalists as well, even to flowers of plants that are otherwise chemically defended. In this study of foothills death-camas, Toxicoscordion paniculatum (Nutt.) Rydberg (formerly Zigadenus), we show that its pollen and nectar both contain zygacine, the steroidal alkaloid responsible for this plant’s notorious mammalian toxicity. Hungry naïve adults of a generalist solitary bee, Osmia lignaria Say (Megachilidae), would briefly drink death-camas nectar or biologically relevant doses of zygacine in syrup, followed by prolonged bouts of irritable tongue grooming; many became paralyzed and some even died. Larvae fed dosed provision masses likewise often ceased feeding and sometimes died. Prolonged irritation and subsequent deterrence of foraging O. lignaria likely illustrates why it and 50+ other vernal bee species were absent from death-camas flowers in a five-state survey. The sole visiting bee, Andrena astragali, foraged exclusively at death-camas flowers for pollen and nectar. Thus, a toxic alkaloid found in death-camas pollen and nectar deters generalist bees from flowers of this pollinator-dependent monocot, restricting visitation to a single specialist bee that tolerates death-camas toxins and is its likely pollinator.

Pesticide and resource stressors additively impair wild bee reproduction

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.

Diet Breadth Affects Bacterial Identity but Not Diversity in the Pollen Provisions of Closely Related Polylectic and Oligolectic Bees

Mounting evidence suggests that microbes found in the pollen provisions of wild and solitary bees are important drivers of larval development. As these microbes are also known to be transmitted via the environment, most likely from flowers, the diet breadth of a bee may affect the diversity and identity of the microbes that occur in its pollen provisions. Here, we tested the hypothesis that, due to the importance of floral transmission of microbes, diet breadth affects pollen provision microbial community composition. We collected pollen provisions at four sites from the polylectic bee Osmia lignaria and the oligolectic bee Osmia ribifloris. We used high-throughput sequencing of the bacterial 16S rRNA gene to characterize the bacteria found in these provisions. We found minimal overlap in the specific bacterial variants in pollen provisions across the host species, even when the bees were constrained to foraging from the same flowers in cages at one site. Similarly, there was minimal overlap in the specific bacterial variants across sites, even within the same host species. Together, these findings highlight the importance of environmental transmission and host specific sorting influenced by diet breadth for microbes found in pollen provisions. Future studies addressing the functional consequences of this filtering, along with tests for differences between more species of oligoletic and polylectic bees will provide rich insights into the microbial ecology of solitary bees.