Impacts of flupyradifurone on the midgut and brain of the neotropical social bee Scaptotrigona postica and its behavioral effects
Impacts of flupyradifurone on the midgut and brain of the neotropical social bee Scaptotrigona postica and its behavioral effects
Introduction
Bees play a fundamental role in the pollination of cultivated plants and natural ecosystems and can act as pollinators of almost 90 % of the world's flowering plants (D’Avila, Marchini, 2005).
Among the existing bee families, the Apidae stands out for its wide diversity of species and ecological habits (Michener, 2007). Within this family is the Meliponini tribe, which is made up of stingless social bees (meliponids), named after their absence or atrophied sting (Michener, 2007), native to the tropics and subtropics of the planet (Ayala et al., 2013). Scaptotrigona postica (Latreille, 1807), popularly known as ‘mandaguari’, for example, is a meliponid species that lives in tree hollows and is found from Mexico to Brazil (Nogueira-Neto, 1997). It is responsible for pollinating agricultural crops such as cashew, strawberry, pitanga, açaí, among others (Souza et al., 2015).
Despite the great importance of bees, these pollinators have suffered several threats due to different factors, such as habitat loss and climate change (Jaffé et al., 2019), as well as competition for resources (Hung et al., 2019), resulting in a worldwide decrease in populations (Hung et al., 2019, Jaffé et al., 2019). In addition, human action in conjunction with the inappropriate use of pesticides is among the factors with the greatest impact on the threat to the biodiversity of these insects (Dudley and Alexander, 2017).
Considering the aforementioned information and the importance of guaranteeing crop yields, it´s a necessary attention in the development and discovery of new synthetic substances for pesticides (Godfray et al., 2010). Flupyradifurone, for example, is a systemic insecticide, which belongs to the chemical group butenolides (Nauen et al., 2014). Like neonicotinoids and sulfoximines, this insecticide acts on nAChRs and is used to control agricultural pests such as mites, aphids and whiteflies (Nauen et al., 2014).
Since 2014, flupyradifurone has been registered in more than 50 countries (EFSA Panel on Plant Protection Products and their Residues PPR et al., 2022) and is permitted for use on a wide range of crops such as soybeans, coffee, citrus, cotton, passion fruit, peppers, eggplants and peppers, among others (Nauen et al., 2014, Bayer, 2022). Despite being considered a safer alternative and less toxic to the environment when compared to other neurotoxic insecticides, it is still necessary to understand the real impact of flupyradifurone on pollinators (Siviter et al., 2024). When bees are exposed to different concentrations of this insecticide, they can suffer different effects such as reduced nesting success (Siviter et al., 2024), impaired foraging efficiency (Hesselbach and Scheiner, 2019, Siviter et al., 2024), increased mortality (Al Naggar and Baer, 2019, Hesselbach and Scheiner, 2019, Siviter et al., 2024), altered expression of immune and detoxification genes (Al Naggar; Baer, 2019), among other effects.
In addition, many of the studies with the insecticide flupyradifurone have been carried out with Apis mellifera (Tosi; Nieh, 2019), but there is a possibility that native bees such as Scaptotrigona postica have contact with this substance during pollination of crops such as citrus and strawberries, where this insecticide can be used (Bayer, 2022, Nauen et al., 2014, Souza et al., 2015).
Furthermore, there are still unknown effects of flupyradifurone on pollinating insects. Thus, the present work aims to fill gaps in knowledge regarding the impacts of flupyradifurone on native stingless bees, evaluating the influence of chronic oral exposure to an environmentally relevant concentration of the insecticide on the longevity and locomotion behavior of Scaptotrigona postica, in addition to the impacts of this insecticide on the brain and intestine of bees.
Section snippets
Collection and tagging of Scaptotrigona postica workers
Scaptotrigona postica foraging bees were collected in December 2023, January, March and April 2024, at the entrance to managed and healthy colonies located in Sorocaba, Brazil (23°34'58“S 47°31'27”W). To collect only foraging bees, the entrances to the colonies were closed with their own wax, then the bees were expected to gather at the entrance to the colony so that a 250 mL transparent plastic pot could be positioned for collection, and bees that did not have pollen on their corbiculae
Survival
The presence of the insecticide flupyradifurone did not negatively influence bee survival (Cox regression - coefficient = 0.017; p = 0.857), Hazard Ratio (HR) = 1.017 and 95 % Confidence Interval (CI): 0.844–1.226). Therefore, the bees exposed to insecticide did not show significant differences in the total survival time when compared to the control group (Fig. 1), so that both groups survived for a similar length of time and had a similar mean lethal time (LT50), 8 days for the control group
Discussion
From the results of the present study, it was possible to observe that chronic oral exposure to an environmentally relevant concentration of flupyradifurone (FPF) affects the morphology of the mushroom bodies of the brain of Scaptotrigona postica, considering that this region is related to sensory characteristics, learning, memory, socialization and integration of stimuli of bees (Menzel, 2012), structural changes can compromise the exploratory behavior and memory of bees, resulting in
Conclusion
Under laboratory conditions, exposure to the insecticide flupyradifurone impacts the morphology of the mushroom bodies of the brain of Scaptotrigona postica, increasing the distance between the cells that form its internal neuronal portion. These changes could be reflected in behavioral alterations, where all the locomotion parameters analyzed were reduced. However, exposure to insecticide is not a significant factor in the survival of individuals. Furthermore, exposure to flupyradifurone does
CRediT authorship contribution statement
Rebeca Emanuelle da Silva Castor: Writing – review & editing, Writing – original draft, Resources, Project administration, Methodology, Investigation, Funding acquisition, Formal analysis, Data curation, Conceptualization. Vinícius Martins: Writing – review & editing, Methodology. Elaine Cristina Mathias da Silva: Writing – review & editing, Writing – original draft, Supervision, Funding acquisition, Conceptualization.
Funding
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 (Scolarship for the first author). FAPESP (Grant number: 2017/21097-3)
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors thank Leticia Saraiva and Rafaela Tadei for their support and help during some stages of the work. We would also like to thank Prof. Dr. Letícia Souto (LADIVE, Fapesp 2015/01424–4) for allowing us to use the microtome and photomicroscope during the analysis.
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