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

Para 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). Lo...

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2024
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Universidad del Rosario
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Palabra clave:
Apis mellifera
Bombus impatiens
Kaempferol
Rutina
Ácido p-cumárico
Fipronil
Imidacloprid
PER
Protección cognitiva
Actividad mitocondrial
Seguridad alimentaria
Disminución de polinizadores
Neuropesticidas
Apis mellifera
Bombus impatiens
Kaempferol
Rutin
p-coumaric acid
Fipronil
Imidacloprid
PER
Cognitive protection
Mitochondrial activity
Food security
Pollinator decline
Neuropesticides
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id EDOCUR2_d6f628d00495fb1e81c92a3b3144d070
oai_identifier_str oai:repository.urosario.edu.co:10336/42492
network_acronym_str EDOCUR2
network_name_str Repositorio EdocUR - U. Rosario
repository_id_str
dc.title.none.fl_str_mv Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
dc.title.TranslatedTitle.none.fl_str_mv Cognitive neuropharmacological protection of bees exposed to pesticides: a role for phytochemicals
title Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
spellingShingle Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
Apis mellifera
Bombus impatiens
Kaempferol
Rutina
Ácido p-cumárico
Fipronil
Imidacloprid
PER
Protección cognitiva
Actividad mitocondrial
Seguridad alimentaria
Disminución de polinizadores
Neuropesticidas
Apis mellifera
Bombus impatiens
Kaempferol
Rutin
p-coumaric acid
Fipronil
Imidacloprid
PER
Cognitive protection
Mitochondrial activity
Food security
Pollinator decline
Neuropesticides
title_short Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
title_full Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
title_fullStr Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
title_full_unstemmed Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
title_sort Protección neurofarmacológica cognitiva de abejas expuesta a pesticidas: un papel para los fitoquímicos
dc.contributor.advisor.none.fl_str_mv Riveros Rivera, André Josafat
Ondo Méndez, Alejandro Oyono
dc.contributor.gruplac.none.fl_str_mv CANNON
dc.contributor.none.fl_str_mv Niño Mayorga, Sergio
Caicedo Garzón, Valentina
Seid, Marc
dc.subject.none.fl_str_mv Apis mellifera
Bombus impatiens
Kaempferol
Rutina
Ácido p-cumárico
Fipronil
Imidacloprid
PER
Protección cognitiva
Actividad mitocondrial
Seguridad alimentaria
Disminución de polinizadores
Neuropesticidas
topic Apis mellifera
Bombus impatiens
Kaempferol
Rutina
Ácido p-cumárico
Fipronil
Imidacloprid
PER
Protección cognitiva
Actividad mitocondrial
Seguridad alimentaria
Disminución de polinizadores
Neuropesticidas
Apis mellifera
Bombus impatiens
Kaempferol
Rutin
p-coumaric acid
Fipronil
Imidacloprid
PER
Cognitive protection
Mitochondrial activity
Food security
Pollinator decline
Neuropesticides
dc.subject.keyword.none.fl_str_mv Apis mellifera
Bombus impatiens
Kaempferol
Rutin
p-coumaric acid
Fipronil
Imidacloprid
PER
Cognitive protection
Mitochondrial activity
Food security
Pollinator decline
Neuropesticides
description Para 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.
publishDate 2024
dc.date.accessioned.none.fl_str_mv 2024-05-02T12:53:12Z
dc.date.available.none.fl_str_mv 2024-05-02T12:53:12Z
dc.date.created.none.fl_str_mv 2024-04-29
dc.type.none.fl_str_mv doctoralThesis
dc.type.coar.fl_str_mv http://purl.org/coar/resource_type/c_db06
dc.type.document.none.fl_str_mv Tesis
dc.type.spa.none.fl_str_mv Tesis
dc.identifier.uri.none.fl_str_mv https://repository.urosario.edu.co/handle/10336/42492
url https://repository.urosario.edu.co/handle/10336/42492
dc.language.iso.none.fl_str_mv spa
language spa
dc.rights.*.fl_str_mv Attribution-NonCommercial-ShareAlike 4.0 International
dc.rights.coar.fl_str_mv http://purl.org/coar/access_right/c_f1cf
dc.rights.acceso.none.fl_str_mv Restringido (Temporalmente bloqueado)
dc.rights.uri.*.fl_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
rights_invalid_str_mv Attribution-NonCommercial-ShareAlike 4.0 International
Restringido (Temporalmente bloqueado)
http://creativecommons.org/licenses/by-nc-sa/4.0/
http://purl.org/coar/access_right/c_f1cf
dc.format.extent.none.fl_str_mv 228 pp
dc.format.mimetype.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Universidad del Rosario
dc.publisher.department.none.fl_str_mv Escuela de Medicina y Ciencias de la Salud
dc.publisher.program.none.fl_str_mv Doctorado en Ciencias Biomédicas y Biológicas
publisher.none.fl_str_mv Universidad del Rosario
institution Universidad del Rosario
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spelling Niño Mayorga, SergioCaicedo Garzón, ValentinaSeid, MarcRiveros Rivera, André Josafat79974449600Ondo Méndez, Alejandro Oyono79831981600CANNONGarcía Forero, Lina MaríaDoctor en Ciencias Biomédicas y BiológicasDoctoradoFull time304c1317-a3d8-4b00-a0f6-9ffdc72ef47e-12024-05-02T12:53:12Z2024-05-02T12:53:12Z2024-04-29Para 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.By 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). 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