Impact of low temperatures on the immune system of honeybees

Butolo, Nicole Pavan; Azevedo, Patricia; Alencar, Luciano Delmondes de; Malaspina, Osmar; Nocelli, Roberta Cornélio Ferreira

doi:10.1016/j.jtherbio.2021.103082

Cited by 4 publications

(5 citation statements)

References 59 publications

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“…Regarding light intensity, solar radiation, CO 2 , atmospheric pressure, and photoperiod those were scarcely represented. In general, these variables were independently analyzed under both experimental (e.g., Butolo et al., 2021; Medina et al., 2018) and empirical approaches (e.g., Gordo & Sanz, 2006; Jaboor et al., 2022), including different combinations of environmental factors (e.g., Morais et al., 2022; Norrström et al., 2021; Rowland et al., 2021). Likewise was the case for their effects, where studies usually analyze the individual effect on selected response variables (e.g., gene expression, visitation rate, appearance date, and survival) and in some cases are considered the interactive effect only between environmental variables (e.g., temperature + precipitation, temperature + photoperiod; e.g., Becsi et al., 2021; Villagomez et al., 2021; Zhang et al., 2022; Norrström et al., 2021; Maluf et al., 2022; Anderson & Maes, 2022) or with other stressors such as pesticides and diseases (e.g., Aldea‐Sánchez et al., 2021; Gonzalez et al., 2022); those studies provide an important insight as the climate impacts can be also exacerbated in different ways by their interaction with other stressors.…”

Section: Discussionmentioning

confidence: 99%

“…Instead, most studies were based on weather data, as well as experimental indoor and outdoor environments (e.g., Butolo et al., 2021; Jaworski et al., 2022; Maluf et al., 2022; Martín‐Hernández et al., 2009). It is important also to note that several studies only declare the environmental variables employed but do not provide details on the temporal scales considered in their analysis (e.g., Cánovas et al., 2014; Cruz et al., 2022; Hung et al., 2018).…”

Section: Discussionmentioning

confidence: 99%

“…In general, temperature increase could exert a series of negative impacts on food reserves (e.g., honey production, colony weight gain, and honey sugar composition; Nürnberger et al., 2019; Gajardo‐Rojas et al., 2022; Langowska et al., 2017; Quinlan et al., 2022; Bordier et al., 2017), plant–pollinator interactions (e.g., a decrease in visiting rate and strength of interactions; Rader et al., 2013; Giannini et al., 2015; Bar‐Shai et al., 2022; Maluf et al., 2022), mortality of colonies (e.g., longevity, survival, winter resistance; Medina et al., 2018; McAfee et al., 2020; Aldea‐Sánchez et al., 2021; Cebotari et al., 2019), gene expression (e.g., up‐regulation or expression changes; Ma et al., 2019; McAfee et al., 2020; Bordier et al., 2017; Bach et al., 2021), and thermal biology (e.g., thermal tolerance, desiccation, body temperature; Sánchez‐Echeverría et al., 2019; Burdine & McCluney, 2019; Lima et al., 2019). However, a decrease in temperatures could also result in increased colony mortality (Becsi et al., 2021), affect the immunity (Butolo et al., 2021) and microbiome (Castelli et al., 2022), as well as changes in temperature patterns are expected to contribute to pest spread through changes in thermal suitability (Hosni et al., 2022; Tihelka et al., 2021).…”

Section: Discussionmentioning

confidence: 99%

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Advances and knowledge gaps on climate change impacts on honey bees and beekeeping: A systematic review

Zapata‐Hernández,

Gajardo‐Rojas,

Calderón‐Seguel

et al. 2024

Global Change Biology

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The Western honey bee Apis mellifera is a managed species that provides diverse hive products and contributing to wild plant pollination, as well as being a critical component of crop pollination systems worldwide. High mortality rates have been reported in different continents attributed to different factors, including pesticides, pests, diseases, and lack of floral resources. Furthermore, climate change has been identified as a potential driver negatively impacting pollinators, but it is still unclear how it could affect honey bee populations. In this context, we carried out a systematic review to synthesize the effects of climate change on honey bees and beekeeping activities. A total of 90 articles were identified, providing insight into potential impacts (negative, neutral, and positive) on honey bees and beekeeping. Interest in climate change's impact on honey bees has increased in the last decade, with studies mainly focusing on honey bee individuals, using empirical and experimental approaches, and performed at short‐spatial (<10 km) and temporal (<5 years) scales. Moreover, environmental analyses were mainly based on short‐term data (weather) and concentrated on only a few countries. Environmental variables such as temperature, precipitation, and wind were widely studied and had generalized negative effects on different biological and ecological aspects of honey bees. Food reserves, plant‐pollinator networks, mortality, gene expression, and metabolism were negatively impacted. Knowledge gaps included a lack of studies at the apiary and beekeeper level, a limited number of predictive and perception studies, poor representation of large‐spatial and mid‐term scales, a lack of climate analysis, and a poor understanding of the potential impacts of pests and diseases. Finally, climate change's impacts on global beekeeping are still an emergent issue. This is mainly due to their diverse effects on honey bees and the potential necessity of implementing adaptation measures to sustain this activity under complex environmental scenarios.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Advances and knowledge gaps on climate change impacts on honey bees and beekeeping: A systematic review

Zapata‐Hernández,

Gajardo‐Rojas,

Calderón‐Seguel

et al. 2024

Global Change Biology

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“…Cox-Foster et al [ 12 ] already presented a meta-genomic survey to assess the degree of contribution of different risk factors to colony collapse disorder. However, temperature changes [ 57 ], the order of exposure to risk factors, and its duration are also required to have a comprehensive view. Since CYP450 production affects imidacloprid toxicity [ 19 , 20 ] and metabolism affects amitraz toxicity [ 51 ], it is implied that the effect of imidacloprid and amitraz co-exposure may be different from the effect of single exposures, as found in this study.…”

Section: Discussionmentioning

confidence: 99%

Differential Production of Nitric Oxide and Hydrogen Peroxide among Drosophila melanogaster, Apis mellifera, and Mamestra brassicae Immune-Activated Hemocytes after Exposure to Imidacloprid and Amitraz

Sukkar

Laval-Gilly

Bonnefoy

et al. 2023

Insects

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Invertebrates have a diverse immune system that responds differently to stressors such as pesticides and pathogens, which leads to different degrees of susceptibility. Honeybees are facing a phenomenon called colony collapse disorder which is attributed to several factors including pesticides and pathogens. We applied an in vitro approach to assess the response of immune-activated hemocytes from Apis mellifera, Drosophila melanogaster and Mamestra brassicae after exposure to imidacloprid and amitraz. Hemocytes were exposed to the pesticides in single and co-exposures using zymosan A for immune activation. We measured the effect of these exposures on cell viability, nitric oxide (NO) production from 15 to 120 min and on extracellular hydrogen peroxide (H2O2) production after 3 h to assess potential alterations in the oxidative response. Our results indicate that NO and H2O2 production is more altered in honeybee hemocytes compared to D. melanogaster and M. brassicae cell lines. There is also a differential production at different time points after pesticide exposure between these insect species as contrasting effects were evident with the oxidative responses in hemocytes. The results imply that imidacloprid and amitraz act differently on the immune response among insect orders and may render honeybee colonies more susceptible to infection and pests.

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“…A função de cada hemócito ainda não está totalmente esclarecida, mas de maneira geral, são responsáveis pelos processos fundamentais de defesa imunológica, como a fagocitose, nodulação e encapsulação no momento em que alguns patógenos como bactérias, vírus e protozoários conseguem invadir a hemocele (cavidade do corpo) dos insetos . Essa perspectiva se torna mais importante a ser avaliada se considerado a possibilidade dos impactos da alta variação térmica global em decorrência das mudanças climáticas com variações significativas de temperatura, sobre o número de hemócitos circulantes em diferentes espécies (BUTOLO et al, 2021;HANSEN et al, 2006).…”

Section: Hemócitosunclassified

Caracterização dos hemócitos de subcastas de operárias da formiga-cortadeira Atta sexdens rubropilosa (Hymenoptera: formicidae)

Dourado

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As formigas são insetos sociais que possuem sistema imune inato eficiente como mecanismo de defesa, sendo constituído por componentes humorais e celulares da hemolinfa, denominados hemócitos. Diferentes hemócitos foram identificados nos insetos, no entanto, na formiga-cortadeira Atta sexdens rubropilosa (Forel, 1908) (Hymenoptera: Formicidae), inexiste a caracterização celular dessa natureza para a espécie em estudo. Essa formiga de importância ambiental e econômica, possui colônia organizada e a divisão de trabalho é realizada por castas, sendo as operárias divididas nas subcastas jardineiras, lixeiras, forrageiras e soldados. As jardineiras desempenham o cultivo do fungo simbionte e cuidados da prole; as lixeiras gerenciam o lixo e higienizam o ninho; as forrageiras auxiliam na construção do ninho, executando o corte e transporte de folhas para o interior do ninho; e os soldados realizam a proteção da colônia e auxiliam as forrageiras. Nesse sentido, o presente estudo tem como objetivo caracterizar morfológica e funcionalmente os hemócitos circulantes na hemolinfa das subcastas de operárias da formiga Atta sexdens rubropilosa de diferentes subcastas. Foram realizadas as técnicas de medição da cápsula cefálica, microscopia de luz, fluorescência, confocal a laser, eletrônica de varredura, contagem diferencial e contagem total de hemócitos, assim como citometria de fluxo. O comportamento das formigas dentro do ninho, assim como o tamanho da cápsula cefálica confirmou as subcastas de operárias. Na hemolinfa da formiga foram identificados cinco tipos morfológicos de hemócitos, denominados como pró-hemócitos, oenocitóides, esferulócitos, plasmatócitos e granulócitos, comum em todas subcastas. Os granulócitos e os pró-hemócitos são os tipos mais abundantes circulando na hemolinfa. As maiores quantidades de hemócitos foram obtidas nas subcastas forrageiras e soldados. Os soldados e jardineiras apresentam maiores quantidades de células fagocíticas. Granulócitos e plasmatócitos fagocitaram bactérias E. coli em maior quantidade. Cinco subpopulações foram encontradas na hemolinfa das formigas, mas duas foram predominantes, que provavelmente sejam os granulócitos e plasmatócitos. Os soldados apresentaram células e intensidade de fluorescência maior em relação às subcastas jardineira, lixeira e forrageira, por outro lado, com complexidade interna/granulosidade estatisticamente diferente apenas em relação às células da subcasta jardineira. Dessa maneira, esses resultados indicam que os soldados apresentam sistema imunológico mais desenvolvido. A caracterização e descrição celular dos hemócitos dessa espécie, fornece dados para estudos futuros com finalidade de melhor compreender a fisiologia deste importante inseto. Palavras-chave: Formiga. Hemócitos. Morfologia. Microscopia. Citometria.

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Impact of low temperatures on the immune system of honeybees

Cited by 4 publications

References 59 publications

Advances and knowledge gaps on climate change impacts on honey bees and beekeeping: A systematic review

Advances and knowledge gaps on climate change impacts on honey bees and beekeeping: A systematic review

Differential Production of Nitric Oxide and Hydrogen Peroxide among Drosophila melanogaster, Apis mellifera, and Mamestra brassicae Immune-Activated Hemocytes after Exposure to Imidacloprid and Amitraz

Caracterização dos hemócitos de subcastas de operárias da formiga-cortadeira Atta sexdens rubropilosa (Hymenoptera: formicidae)

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