A systematic scoping review of the methodological approaches and effects of pesticide exposure on solitary bees.

BACKGROUND: Pollination services provided by solitary bees, the largest group of bees worldwide, are critical to the vitality of ecosystems and agricultural systems alike. Disconcertingly, bee populations are in decline, and while no single causative factor has been identified, pesticides are believed to play a role in downward population trends. The effects of pesticides on solitary bee species have not been previously systematically cataloged and reviewed. OBJECTIVES: This systematic scoping review examines available evidence for effects of pesticide exposure on solitary bees to identify data gaps and priority research needs. METHODS: A systematic literature search strategy was developed to identify and document reports on solitary bee pesticide exposure-effects investigations. Literature was subsequently screened for relevance using a Population, Exposures, Comparators, and Outcomes (PECO) statement and organized into a systematic evidence map. Investigations were organized by effect category (lethal effects on immatures, lethal effects on adults, sublethal effects on immatures, and sublethal effects on adults), species, pesticide class, and publication year. RESULTS: A comprehensive literature search of Web of Science and ProQuest Agricultural & Environmental Science supplemented by targeted internet searching and reference mining yielded 176 reports and publications for title and abstract screening and 65 that met PECO criteria (22 included lethal and 43 included sublethal effects endpoints). Relevant design details (pesticide, test compound configuration, study type, species, sex, exposure duration) were extracted into literature inventory tables to reveal the extent endpoints have been investigated and areas in need of additional research. CONCLUSIONS: Evidence mapping revealed diversity in the pesticides and endpoints studied across the database. However, dilution across bee species, lack of complementary laboratory work and paucity of replicated investigations complicate efforts to interpret and apply available data to support pesticide risk assessment.

Impacts of Neonicotinoids on the Bumble Bees Bombus terrestris and Bombus impatiens Examined through the Lens of an Adverse Outcome Pathway Framework.

Bumble bees (Bombus sp.) are important pollinators for agricultural systems and natural landscapes and have faced population declines globally in recent decades. Neonicotinoid pesticides have been implicated as one of the reasons for the population reductions in bumble bees and other pollinators due to their widespread use, specificity to the invertebrate nervous system, and toxicity to bees. Adverse outcome pathways (AOPs) are used to describe the mechanism of action of a toxicant through sequential levels of biological organization to understand the key events that occur for a given adverse outcome. We used the AOP framework to organize and present the current literature available on the impacts of neonicotinoids on bumble bees. The present review focuses on Bombus terrestris and B. impatiens, the 2 most commonly studied bumble bees due to their commercial availability. Our review does not seek to describe an AOP for the molecular initiating event shared by neonicotinoids, but rather aims to summarize the current literature and determine data gaps for the Bombus research community to address. Overall, we highlight a great need for additional studies, especially those examining cellular and organ responses in bumble bees exposed to neonicotinoids. Environ Toxicol Chem 2021;40:309-322. © 2020 SETAC. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

Effects of the neonicotinoid acetamiprid in syrup on Bombus impatiens (Hymenoptera: Apidae) microcolony development.

Worldwide, many pollinator populations are in decline. Population reductions have been documented for the agriculturally important honey bee (Apis mellifera), and other bee species such as bumble bees that are also critical for pollinating crops and natural landscapes. A variety of factors contribute to the observed population reductions, including exposure to agrochemicals. In recent decades, neonicotinoid pesticide use has dramatically increased, as have concerns regarding the safety of these chemicals for pollinator health. Here we assessed the toxicity of the neonicotinoid acetamiprid to the bumble bee Bombus impatiens, a species commercially available for use in agricultural settings in North America. Using the microcolony model, we examined nest growth, development and subsequent nest productivity as measured by drone production. We found that high concentrations of acetamiprid in syrup (11,300 µg/L) significantly impacted nest growth and development, and ultimately drone production, and exposure to 1,130 µg/L acetamiprid also significantly decreased drone production. The no observable adverse effect level was 113 µg/L. Overall, acetamiprid delivered in syrup can negatively impact B. impatiens nest development and productivity, however only at concentrations above which would be expected in the environment when used according to label rates.

Effects of the Neonicotinoid Acetamiprid in Pollen on Bombus impatiens Microcolony Development.

Honey bees and other wild bee species including bumble bees have experienced population declines in recent decades. Although many stressors are implicated in bee population declines, much attention has focused on neonicotinoid pesticides, which are widely used and known to be toxic to pollinators. One neonicotinoid, acetamiprid, has been studied very little in bumble bees, despite its use on bumble bee-pollinated crops. We assessed the impacts of acetamiprid to the North American bumble bee Bombus impatiens using the microcolony model. We examined nest growth, development, and subsequent nest productivity as measured by drone production. We found that high concentrations of acetamiprid in pollen (4520 µg/kg) significantly impacted nest growth, development, and, ultimately, reproduction (drone production). We found the no-observable-adverse effect level to be 45.2 µg/kg. Overall, acetamiprid has the potential to negatively impact reproductive endpoints for B. impatiens. However, effects occurred at concentrations substantially higher than expected environmental concentrations that would be achieved when following label rates. Further work is required to assess the effects of this pesticide on B. impatiens via alternate routes of exposure and on queenright colonies. Environ Toxicol Chem 2020;39:2560-2569. © 2020 SETAC. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

The Importance of Males to Bumble Bee (Bombus Species) Nest Development and Colony Viability.

Bumble bee population declines over the last decade have stimulated strong interest in determining causative factors and necessary conservation measures. Research attention has largely been directed toward bumble bee worker and queen health and their contributions to population stability, while male bees (i.e., drones) have typically been overlooked regarding their role in influencing colony fitness and longevity. In this review we assess existing literature on the diverse role of males within bumble bee nests and their importance to queen health and fitness, as well as to overall nest success. The implications of reproductive measures, including sperm transfer, mating behavior, mating plugs, and male immunity, among other topics, are examined. Overall, bumble bee males are found to drive colony function in a unique manner. Current knowledge gaps pertaining to the role of males are discussed. We highlight the importance of drones to queen success and fitness in many ways, and suggest future research exploring impacts of this often-neglected caste.

Involvement of glutamate and serotonin transmitter systems in male sex determination in Daphnia pulex.

Environmental sex determination occurs in many organisms, however the means by which environmental stimuli are translated into endocrine messages remains poorly understood. The N-methyl-ᴅ-aspartate receptor (NMDAR) was evaluated as a candidate neural sensor of environmental signals linking environmental cues to endocrine responses using the crustacean Daphnia pulex. NMDAR agonists, modulators, and antagonists were evaluated for their ability to impact D. pulex male sex determination during early stages of reproductive maturity under conditions that simulated seasonal change. The antagonists MK-801 and desipramine significantly increased male sex determination. Both chemicals are also modulators of serotonergic and noradrenergic systems, thus, we evaluated several modulators of monoamine neurotransmission in an effort to discern which signaling pathways might contribute to male sex determination. Compounds that altered serotonergic signaling also stimulated male sex determination. The involvement of the glutamate and monoamine signaling in male sex determination was supported by the increase in mRNA levels of related receptors and transporters under conditions that stimulate male sex determination. Further, mRNA levels of components of the terminal endocrine pathway responsible for male sex determination were also elevated under stimulatory conditions. Overall, we provide evidence that glutamatergic and serotonergic systems function upstream of the endocrine regulation of male sex determination in early life stage daphnids.

Bombus (Hymenoptera: Apidae) Microcolonies as a Tool for Biological Understanding and Pesticide Risk Assessment.

Bumble bees provide valuable pollination services to many wild and agricultural plants. Populations of some bumble bee species are in decline, prompting the need to better understand bumble bee biology and to develop methodologies for assessing the effects of environmental stressors on these bees. Use of bumble bee microcolonies as an experimental tool is steadily increasing. This review closely examines the microcolony model using peer-reviewed published literature identified by searching three databases through November 2018. Microcolonies have been successfully used for investigating a range of endpoints including behavior, the gut microbiome, nutrition, development, pathogens, chemical biology, and pesticides/xenobiotics. Methods for the initiation and monitoring of microcolonies, as well as the recorded variables were catalogued and described. From this information, we identified a series of recommendations for standardizing core elements of microcolony studies. Standardization is critical to establishing the foundation needed to support use of this model for biological response investigations and particularly for supporting use in pesticide risk assessment.

Complementary roles of photoperiod and temperature in environmental sex determination in Daphnia spp.

Daphnia spp., a keystone genus in freshwater lentic habitats, are subject to environmental sex determination wherein environmental conditions dictate offspring sex and whether they reproduce asexually or sexually. The introduction of males into a population denotes the first step in the switch from asexual parthenogenetic reproduction to sexual reproduction. We tested the hypothesis that photoperiod and temperature co-regulate male sex determination and that these environmental stimuli would activate elements of the male sex determination signaling cascade. The results revealed that photoperiod was a critical cue in creating permissive conditions for male production. Further, under photoperiod-induced permissive conditions, male sex determination was temperature dependent. The two daphnid species evaluated, Daphnia pulex and Daphnia magna, exhibited different temperature dependencies. Daphnia pulex produced fewer males with increasing temperatures between 16 and 22°C, and D. magna exhibited the opposite trend. We found consistent expression patterns of key genes along the male sex-determining signaling pathway in D. pulex independent of environmental stimuli. mRNA levels for the enzyme responsible for synthesis of the male sex-determining hormone, methyl farnesoate, were elevated early in the reproductive cycle, followed by increased mRNA levels of the methyl farnesoate receptor subunits Met and SRC Environmental conditions that stimulated male offspring production significantly increased Met mRNA levels. The results indicate that male sex determination in daphnids is under the permissive control of photoperiod and the regulatory control of temperature. Further, these environmental cues may stimulate male sex determination by increasing levels of the Met subunit of the methyl farnesoate receptor.