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Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos

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dc.contributorNiño Mayorga, Sergio
dc.contributorCaicedo Garzón, Valentina
dc.contributorSeid, Marc
dc.contributor.advisorRiveros Rivera, André Josafat
dc.contributor.advisorOndo Méndez, Alejandro Oyono
dc.contributor.gruplacCANNON
dc.creatorGarcía Forero, Lina María
dc.creator.degreeDoctor en Ciencias Biomédicas y Biológicas
dc.creator.degreeLevelDoctorado
dc.creator.degreetypeFull time
dc.date.accessioned2024-05-02T12:53:12Z
dc.date.available2024-05-02T12:53:12Z
dc.date.created2024-04-29
dc.descriptionPara el año 2035, las abejas, responsables de hasta el 75 % de los alimentos consumidos, pueden desaparecer en los Estados Unidos si se mantiene la tasa actual de disminución de la población, con una desaparición fuertemente asociada con la exposición a pesticidas (Benjamin & McCallum, 2008). Los neuropesticidas, incluidos los neonicotinoides y el fipronil, actúan en áreas del cerebro y conducen a comportamientos alterados, a menudo soportados por procesos neurodegenerativos y modificaciones fisiológicas (Rortais et al., 2005). En respuesta a este problema global, y luego de una amplia evidencia, ciertos neonicotinoides, junto con el fipronil, fueron prohibidos en Europa (Kathage et al., 2018) . Sin embargo, las preocupaciones en contra de una prohibición generalizada del mercado apuntan al hecho de que los agricultores pueden depender de pesticidas más antiguos, potencialmente más tóxicos o susceptibles a la evolución de la resistencia de las plagas, lo que lleva a costos más altos de los alimentos (Özkara et al., 2016). Por lo tanto, los enfoques en un futuro cercano deben garantizar la seguridad alimentaria considerando la conservación de los cultivos y de los polinizadores (van der Sluijs & Vaage, 2016). Aquí evaluamos una estrategia de protección neurofarmacológica proporcionada por metabolitos secundarios derivados de plantas contra el fipronil, un neuropesticida ampliamente utilizado en muchos lugares del mundo (Simon-Delso et al., 2015). Las abejas melíferas y los abejorros son considerados polinizadores clave en todo el mundo; sin embargo, otras abejas silvestres también enfrentan amenazas similares (Klein et al., 2018; Potts et al., 2016). En Apis mellifera scutellata y en Bombus impatiens, las dosis subletales de fipronil alteran las funciones cognitivas, lo que reduce el rendimiento individual y de la colonia (Frazier et al., 2015; van der Sluijs & Vaage, 2016). En el cerebro de las abejas, el fipronil se dirige a áreas como los cuerpos pedunculados (CPs), centros subyacentes al aprendizaje, la memoria entre otras funciones cognitivas (Decourtye et al., 2009; El Hassani et al., 2005, 2009; Jacob et al., 2015). Dentro de los CPs, la neurodegeneración de los microglomérulos (MGs; subregiones que exhiben una rica conectividad neuronal y plasticidad) y los cambios bioquímicos en los niveles de ATP neuronal, presumiblemente explican las deficiencias cognitivas y fisiológicas (Cintra-Socolowski et al., 2016; Nicodemo et al., 2014; Peng & Yang, 2016). Por lo tanto, las exposiciones subletales al fipronil disminuyen habilidades clave, como la navegación y la evaluación de recursos (Decourtye et al., 2009; Pisa et al., 2015). En consecuencia, las deficiencias individuales de las abejas afectan el nivel superior de organización y las colonias pueden colapsar (Simon-Delso et al., 2015; Steinhauer et al., 2018). En este contexto, proteger farmacológicamente a las abejas de los efectos negativos del fipronil es un enfoque clave que impacta directamente a su salud y apoya a la seguridad alimentaria. En este trabajo, hemos descubierto que la administración de varios metabolitos secundarios derivados de plantas, como los flavonoles rutina, kaempferol y el ácido p-cumárico (un ácido fenólico), protegen con éxito los procesos cognitivos y neuroestructurales frente a la exposición subletal de fipronil. Además, hemos demostrado que las dosis subletales de fipronil y de imidacloprid, dos clases distintas de neuropesticidas, no solo deterioran el rendimiento cognitivo de las abejas, sino que también alteran y reducen la producción de ATP mitocondrial. Por lo tanto, con base en nuestros hallazgos, proponemos que los fitoquímicos mencionados podrían proteger a nivel fisiológico y mitocondrial a las abejas melíferas y/o abejorros que estén expuestas a dosis subletales de fipronil e imidacloprid. Las abejas forrajeras de B. impatiens y A. mellifera tratadas profilácticamente con rutina, kaempferol, ácido p-cumárico o la mezcla de estos, y posteriormente expuestas a una dosis subletal de fipronil de forma crónica o aguda, tuvieron una protección del aprendizaje y una protección a nivel neuroestructural, que no difirieron de las abejas no expuestas. Por el contrario, y como se ha informado en la literatura, las abejas expuestas al fipronil exhibieron un deterioro significativo en el aprendizaje, la memoria y en la producción de ATP mitocondrial (El Hassani et al., 2009; Nicodemo et al., 2014; Riveros & Gronenberg, 2022). Por lo tanto, es crucial identificar el nivel de acción y los mecanismos que respaldan la protección soportada por los fitoquímicos. La investigación de estos aspectos respaldará el uso y el diseño específico de las dosis, y proporcionará una mayor evidencia de la protección fisiológica, neuroestructural, así como permitirá la evaluación de fitoquímicos adicionales que han sido estudiados en el contexto de las enfermedades neurodegenerativas (Kumar & Khanum, 2012; Nkpaa & Onyeso, 2018). Aquí investigamos la protección en varios niveles: conductual (aprendizaje y memoria), neuroestructural (neurodegeneración/neuroprotección de MGs) e investigamos el deterioro causado por dos neuropesticidas diferentes a nivel fisiológico (producción de niveles de ATP mitocondrial) y cognitivo (aprendizaje y memoria). Nuestra investigación se basó en la abeja melífera A. mellifera y en el abejorro B. impatiens debido a su relevancia como los principales polinizadores y debido a sus ventajas claves como modelos clásicos experimentales (Matsumoto et al., 2012; Riveros & Gronenberg, 2009). Finalmente, esta investigación no solo contribuye a la comprensión de los mecanismos asociados con la protección de las abejas, sino que establece una base sólida para futuros estudios direccionados hacia su conservación.
dc.description.abstractBy 2035, bees, responsible for up to 75% of food consumed, may disappear in the United States if the current rate of population decline continues, with declines strongly associated with pesticide exposure (Benjamin & McCallum, 2008). Neuropesticides, including neonicotinoids and fipronil, act on areas of the brain and lead to altered behaviors, often supported by neurodegenerative processes and physiological modifications (Rortais et al., 2005). In response to this global problem, and after extensive evidence, certain neonicotinoids, along with fipronil, were banned in Europe (Kathage et al., 2018). However, concerns against a widespread market ban point to the fact that farmers may rely on older pesticides, potentially more toxic or susceptible to evolving pest resistance, leading to higher costs of food (Özkara et al., 2016). Therefore, approaches in the near future must guarantee food security considering the conservation of crops and pollinators (van der Sluijs & Vaage, 2016). Here we evaluate a neuropharmacological protection strategy provided by plant-derived secondary metabolites against fipronil, a neuropesticide widely used in many places around the world (Simon-Delso et al., 2015). Honey bees and bumblebees are considered key pollinators around the world; However, other wild bees also face similar threats (Klein et al., 2018; Potts et al., 2016). In Apis mellifera scutellata and Bombus impatiens, sublethal doses of fipronil impair cognitive functions, reducing individual and colony performance (Frazier et al., 2015; van der Sluijs & Vaage, 2016). In the brain of bees, fipronil targets areas such as the Mushroom Bodies (MBs), centers underlying learning, memory among other cognitive functions (Decourtye et al., 2009; El Hassani et al., 2005, 2009; Jacob et al., 2015). Within MBs, neurodegeneration of microglomeruli (MGs; subregions that exhibit rich neuronal connectivity and plasticity) and biochemical changes in neuronal ATP levels presumably explain cognitive and physiological deficits (Cintra-Socolowski et al., 2016 ; Nicodemo et al., 2014; Therefore, sublethal exposures to fipronil decrease key skills, such as navigation and resource evaluation (Decourtye et al., 2009; Pisa et al., 2015). Consequently, individual deficiencies of bees affect the higher level of organization and colonies can collapse (Simon-Delso et al., 2015; Steinhauer et al., 2018). In this context, pharmacologically protecting bees from the negative effects of fipronil is a key approach that directly impacts their health and supports food security. In this work, we have discovered that the administration of several plant-derived secondary metabolites, such as rutin flavonols, kaempferol and p-coumaric acid (a phenolic acid), successfully protects cognitive and neurostructural processes against sublethal fipronil exposure. Furthermore, we have shown that sublethal doses of fipronil and imidacloprid, two different classes of neuropesticides, not only impair the cognitive performance of bees, but also alter and reduce mitochondrial ATP production. Therefore, based on our findings, we propose that the aforementioned phytochemicals could protect at the physiological and mitochondrial level in honey bees and/or bumblebees that are exposed to sublethal doses of fipronil and imidacloprid. B. impatiens and A. mellifera foraging bees prophylactically treated with rutin, kaempferol, p-coumaric acid or a mixture of these, and subsequently exposed to a sublethal dose of fipronil chronically or acutely, had learning protection and protection at a neurostructural level, which did not differ from unexposed bees. On the contrary, and as reported in the literature, bees exposed to fipronil exhibited a significant impairment in learning, memory, and mitochondrial ATP production El Hassani et al., 2009; Nicodemo et al., 2014; Riveros & Gronenberg, 2022). Therefore, it is crucial to identify the level of action and mechanisms supporting the protection supported by phytochemicals. Investigation of these aspects will support the use and specific design of doses, and will provide greater evidence of physiological and neurostructural protection, as well as allow the evaluation of additional phytochemicals that have been studied in the context of neurodegenerative diseases (Kumar & Khanum, 2012; Nkpaa and Onyeso, 2018). Here we investigate protection at several levels: behavioral (learning and memory), neurostructural (neurodegeneration/neuroprotection of MGs) and we investigate the impairment caused by two different neuropesticides at the physiological (production of mitochondrial ATP levels) and cognitive (learning and memory) levels. Our research was based on the honey bee A. mellifera and the bumblebee B. impatiens due to their relevance as the main pollinators and due to their key advantages as classical experimental models (Matsumoto et al., 2012; Riveros & Gronenberg, 2009). Finally, this research not only contributes to the understanding of the mechanisms associated with the protection of bees, but also establishes a solid foundation for future studies aimed at their conservation.
dc.format.extent228 pp
dc.format.mimetypeapplication/pdf
dc.identifier.doihttps://doi.org/10.48713/10336_42492
dc.identifier.urihttps://repository.urosario.edu.co/handle/10336/42492
dc.language.isospa
dc.publisherUniversidad del Rosario
dc.publisher.departmentEscuela de Medicina y Ciencias de la Salud
dc.publisher.programDoctorado en Ciencias Biomédicas y Biológicas
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dc.source.instnameinstname:Universidad del Rosario
dc.source.reponamereponame:Repositorio Institucional EdocUR
dc.subjectApis mellifera
dc.subjectBombus impatiens
dc.subjectKaempferol
dc.subjectRutina
dc.subjectÁcido p-cumárico
dc.subjectFipronil
dc.subjectImidacloprid
dc.subjectPER
dc.subjectProtección cognitiva
dc.subjectActividad mitocondrial
dc.subjectSeguridad alimentaria
dc.subjectDisminución de polinizadores
dc.subjectNeuropesticidas
dc.subject.keywordApis mellifera
dc.subject.keywordBombus impatiens
dc.subject.keywordKaempferol
dc.subject.keywordRutin
dc.subject.keywordp-coumaric acid
dc.subject.keywordFipronil
dc.subject.keywordImidacloprid
dc.subject.keywordPER
dc.subject.keywordCognitive protection
dc.subject.keywordMitochondrial activity
dc.subject.keywordFood security
dc.subject.keywordPollinator decline
dc.subject.keywordNeuropesticides
dc.titleProtección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
dc.title.TranslatedTitleCognitive neuropharmacological protection of bees exposed to pesticides: a role for phytochemicals
dc.typedoctoralThesis
dc.type.documentTesis
dc.type.hasVersioninfo:eu-repo/semantics/acceptedVersion
dc.type.spaTesis
local.department.reportEscuela de Medicina y Ciencias de la Salud
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Doctorado en Ciencias Biomédicas y Biológicas