A mechanistic framework to explain the immunosuppressive effects of neurotoxic pesticides on bees

Abstract

There is growing concern that declines in some managed and wild bee pollinator populations threaten biodiversity, the functioning of vital ecological processes and sustainable food production on a global scale. In recent years, there has been increasing evidence that sublethal exposure to the neurotoxic class of insecticides (neonicotinoids) can undermine pollinator immunocompetence and amplify the effects of diseases, which have been suspected to be one of the drivers of pollinator declines. However, exactly how neonicotinoids might inhibit pollinator immunity remains elusive. Here, we put forward a mechanistic framework to explain the effects of neurotoxic pesticides on insect immunocompetence. We propose that there is a close ontogenetic connection between the cellular arm (haemocytes) of the insect immune and nervous systems and that this connection makes the immune system of pollinators and other insects inherently susceptible to interference by neurotoxins such as neonicotinoids at sublethal doses. Investigation of this connection is urgently needed to confirm the validity of this framework and develop a clear, mechanistically informed understanding of the interplay between neonicotinoids and disease ecology in pollinators. This in turn may enable us to develop strategies to mitigate impacts of neurotoxins on pollinators and/or enhance their impacts on pests. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13119/suppinfo is available for this article.

Genetic Variation Influences Tolerance to a Neonicotinoid Insecticide in 3 Butterfly Species

“…Even sublethal concentrations of these pesticides may reduce insect survival or ecosystem services, such as pollination. For example, neonicotinoids have a range of sublethal effects in bees, from reduced reproduction (Whitehorn et al 2012) to immune suppression (Pamminger et al 2018), to impaired navigation and foraging (Henry et al 2012; Feltham et al 2014).…”

The effect of agri-environment schemes on bees on Shropshire farms

“…Such services that are provided by and contribute towards healthy, productive ecosystems include soil maintenance, nutrient cycling and pollination (Power, 2010). Intensive farming for high crop yields trade-off with ecosystem well-being, since it degrades the environment and associated services through increased soil erosion, nutrient removal and runoff, greenhouse gas emissions and environmental toxicity (Pamminger et al 2018). Although ecosystem services are the underlying driver to production and environmental regeneration in agricultural systems, research suggests a significant lack of understanding from farmers about how directly land management can manipulate ecosystem services (Teixeira et al 2018).…”

Testing the multiple stressor hypothesis: chlorothalonil exposure alters transmission potential of a bumblebee pathogen but not individual host health

“…Undoubtedly, such factors will not only act in isolation, but stressor combinations may present a greater threat to bee health if effects of co-exposure are additive or worse [6,7]. of pathogens and pesticides may exacerbate the individual negative effects of each stressor alone (for example, through interactions between pesticides and immunity [19][20][21]). Negative effects may also be amplified by co-exposure if each stressor contributes independently or synergistically to a reduction in individual or colony condition.…”

“…Much recent work has focused on systemic neonicotinoids (e.g. [12,20,21]); however, a largely overlooked pesticide in experimental studies, but one that may influence bumblebee health, especially in relation to pathogen interactions, is the non-systemic fungicide chlorothalonil. This fungicide, intended to inhibit enzymatic processes involved with cellular respiration of fungal cells [32,33], has large-scale agricultural application, with many target crops being bumblebee pollinated [34].…”