Bee gut microbiota as an emerging endpoint for the environmental risk assessment of pesticides

Bee gut microbiota as an emerging endpoint for the environmental risk assessment of pesticides



Abstract
Pollinator health is increasingly threatened by multiple stressors, including climate change, nutritional imbalances, pathogens, and pesticides. Environmental Risk Assessment (ERA) aims to evaluate the potential environmental harm of pesticides and regulate their use in agriculture. However, current ERA frameworks present significant shortcomings, particularly in addressing sublethal and microbiota-mediated effects. Incorporating bee gut microbiota as a biomarker-based monitoring tool could substantially strengthen pesticide risk assessments. In this work, we advocate for the inclusion of bee gut microbiota as a novel endpoint in ERA of pesticides. Using honey bees as a model, we discuss the robustness of gut microbiota as a comparative basis across laboratory and field environments. We also highlight its potential for early detection of sublethal impacts within shorter timeframes, facilitating more sensitive and cost-effective evaluations. Finally, we propose strategies to integrate microbiota-based endpoints into existing ERA frameworks and discuss recent advances and future research directions.

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Introduction
Environmental Risk Assessment (ERA)1 of agrochemicals is the process of evaluating their potential harm to the environment and regulating their use in agriculture. Conducting an ERA requires a thorough understanding of the effects of chemicals on non-target organisms and the pathways through which these organisms may be exposed (European Food Safety Authority (EFSA)). In Europe, the EFSA is the primary Risk Assessor**, evaluating risks throughout the food chain. Along with risk assessment, Risk Managers (European Commission, Member States, and the European Parliament) are responsible for enacting legislation or making decisions regarding food safety.
EFSA has prioritized advancing pollinator risk assessment (ERA), particularly for Plant Protection Products (PPPs) (Adriaanse et al., 2023; EFSA, 2013; More et al., 2021), with our focus being specifically on pesticides within this broader chemical category. Their recent IPol-ERA roadmap outlines methodological improvements needed to address current knowledge gaps in evaluating chemical impacts on both pollinators and other non-target organisms (NTAs) (Williams et al., 2023).
Among bee species, the honey bee stands out as the most extensively studied due to its well-characterized biology, ecological significance, and global use in research and pollination services. Given their widespread exposure to pesticides and other environmental challenges, honey bees serve as a valuable model for investigating the impacts of these factors on bee populations (Potts et al., 2016; Hull et al., 2021). Their agricultural foraging behaviour makes them particularly vulnerable to pesticides among PPPs, while also serving as valuable bioindicators when considering combined stressors like pathogens and climate change (Krupke et al., 2012; Ward et al., 2022). Notably, bee health is closely tied to ecosystem stability, ultimately influencing human well-being, an essential principle of the One Health approach (Todorov et al., 2024).
In the search for protective measures against these stressors, the gut microbiota emerges as a promising alternative to be used as a biomarker-based monitoring tool in ERAs. The gut microbiota plays a crucial role in honey bee health by supporting their immune system, development, behaviour, metabolism, and detoxification processes (Motta and Moran, 2024a, Motta and Moran, 2024b). A growing body of evidence suggests that maintaining a healthy gut microbiota is fundamental for NTAs and especially for bee health, as it influences immunity, metabolism, behaviour, and resilience to stressors, including pesticide exposure (Fernandez De Landa et al., 2023; Graystock et al., 2017; Holley et al., 2022; Kueneman et al., 2023).
Consequently, understanding its composition and functions, as well as exploring its manipulation, has emerged as a promising strategy for improving hive management. This includes advancements in diagnosis and prognosis, along with the development of novel and effective approaches to protect honey bees from stressors and diseases (Daisley et al., 2020). Despite this, the role of the gut microbiota in ERA of pesticides has not yet been integrated into regulatory frameworks.
Here, we propose the conceptual integration of gut microbiota data into environmental risk assessment (ERA) of pesticides for non-target arthropods (NTAs), using honey bees as a model system. We delineate key components and steps for incorporating microbial endpoints within existing ERA frameworks, while critically evaluating both advantages and limitations. Our analysis spans: (1) honey bee gut microbiota characterization, (2) current methodologies and their shortcomings in detecting pesticide-induced dysbiosis, and (3) technical implementation challenges. This work advocates for formal recognition of gut microbiota as a novel ERA endpoint**, providing actionable strategies for its adoption and outlining future research priorities to bridge knowledge gaps.