RESUMEN
Invasive species events related to globalization are increasing, resulting in parasitic outbreaks. Understanding of host defense mechanisms is needed to predict and mitigate against the consequences of parasite invasion. Using the honey bee Apis mellifera and the mite Varroa destructor, as a host-parasite model, we provide a comprehensive study of a mechanism of parasite detection that triggers a behavioral defense associated with social immunity. Six Varroa-parasitization-specific (VPS) compounds are identified that (1) trigger Varroa-sensitive hygiene (VSH, bees' key defense against Varroa sp.), (2) enable the selective recognition of a parasitized brood and (3) induce responses that mimic intrinsic VSH activity in bee colonies. We also show that individuals engaged in VSH exhibit a unique ability to discriminate VPS compounds from healthy brood signals. These findings enhance our understanding of a critical mechanism of host defense against parasites, and have the potential to apply the integration of pest management in the beekeeping sector.
Asunto(s)
Acetatos/aislamiento & purificación , Abejas/metabolismo , Conducta Animal/fisiología , Mezclas Complejas/química , Cetonas/aislamiento & purificación , Varroidae/química , Acetatos/química , Acetatos/farmacología , Animales , Abejas/citología , Abejas/efectos de los fármacos , Abejas/parasitología , Conducta Animal/efectos de los fármacos , Bioensayo , Mezclas Complejas/farmacología , Femenino , Interacciones Huésped-Parásitos , Cetonas/química , Cetonas/farmacología , Varroidae/patogenicidadRESUMEN
Honey bees play a critical role in the maintenance of plant biodiversity and sustainability of food webs. In the past few decades, bees have been subjected to biotic and abiotic threats causing various colony disorders. Therefore, monitoring solutions to help beekeepers to improve bee health are necessary. Matrix-assisted laser desorption ionization-mass spectrometry (MALDI-MS) profiling has emerged within this decade as a powerful tool to identify in routine micro-organisms and is currently used in real-time clinical diagnosis. MALDI BeeTyping is developed to monitor significant hemolymph molecular changes in honey bees upon infection with a series of entomopathogenic Gram-positive and -negative bacteria. A Serratia marcescens strain isolated from one naturally infected honey bee collected from the field is also considered. A series of hemolymph molecular mass fingerprints is individually recorded and to the authors' knowledge, the first computational model harboring a predictive score of 97.92% and made of nine molecular signatures that discriminate and classify the honey bees' systemic response to the bacteria is built. Hence, the model is challenged by classifying a training set of hemolymphs and an overall recognition of 91.93% is obtained. Through this work, a novel, time and cost saving high-throughput strategy that addresses honey bee health on an individual scale is introduced.
Asunto(s)
Abejas/metabolismo , Espectrometría de Masa por Láser de Matriz Asistida de Ionización Desorción/métodos , Animales , Simulación por Computador , Hemolinfa/metabolismo , Hemolinfa/microbiología , Serratia marcescens/fisiologíaRESUMEN
Many of the physiological traits in insects are shaped by environmental temperatures, which can influence their interactions with pathogens. Therefore, quantifying the thermal responses of the host-pathogen system is crucial for better understanding and predicting their dynamics due to environmental changes. This is particularly important in honey bees, which are experiencing severe colony losses around the world, notably due to infection with the Deformed wing virus (DWV). To investigate the influence of temperature on the honey bee/DWV relationship we exposed adult bees to low or high temperatures and determined the effects on viral titers and bee survival. Emerging bees naturally infected with DWV were reared in vitro at different temperatures ranging from 15⯰C to 37⯰C. In addition, some bees reared at 37⯰C were exposed daily to acute heat treatments (40 and 43⯰C). High temperatures significantly decreased DWV titers close to the initial viral load at emergence but increased bee mortality. The lowest temperature resulted in higher mortality, but virus load was not significantly impacted. In conclusion, our results indicate that temperature could contribute to seasonal variations in viral loads but do not suggest temperature to be used as a tool to eliminate viruses, even given that high temperatures limit viral multiplication.
Asunto(s)
Abejas/virología , Virus ARN/crecimiento & desarrollo , Temperatura , Carga Viral , Animales , Abejas/fisiología , Regulación de la Temperatura Corporal/fisiología , Interacciones Huésped-Parásitos/fisiología , Análisis de Supervivencia , Replicación ViralRESUMEN
BACKGROUND: The parasite Varroa destructor represents a significant threat to honeybee colonies. Indeed, development of Varroa infestation within colonies, if left untreated, often leads to the death of the colony. Although its impact on bees has been extensively studied, less is known about its biology and the functional processes governing its adult life cycle and adaptation to its host. We therefore developed a full life cycle transcriptomic catalogue in adult Varroa females and included pairwise comparisons with males, artificially-reared and non-reproducing females (10 life cycle stages and conditions in total). RESULTS: Extensive remodeling of the Varroa transcriptome was observed, with an upregulation of energetic and chitin metabolic processes during the initial and final phases of the life cycle (e.g. phoretic and post-oviposition stages), whereas during reproductive stages in brood cells genes showing functions related to transcriptional regulation were overexpressed. Several neurotransmitter and neuropeptide receptors involved in behavioural regulation, as well as active compounds of salivary glands, were also expressed at a higher level outside the reproductive stages. No difference was detected between artificially-reared phoretic females and their counterparts in colonies, or between females who failed to reproduce and females who successfully reproduced, indicating that phoretic individuals can be reared outside host colonies without impacting their physiology and that mechanisms underlying reproductive failure occur before oogenesis. CONCLUSIONS: We discuss how these new findings reveal the remarkable adaptation of Varroa to its host biology and notably to the switch from living on adults to reproducing in sealed brood cells. By spanning the entire adult life cycle, our work captures the dynamic changes in the parasite gene expression and serves as a unique resource for deciphering Varroa biology and identifying new targets for mite control.
Asunto(s)
Abejas/parasitología , Transcriptoma , Varroidae/genética , Animales , Proteínas de Artrópodos/genética , Femenino , Perfilación de la Expresión Génica , Interacciones Huésped-Parásitos/genética , Estadios del Ciclo de Vida/genética , Masculino , Reproducción/genética , Varroidae/fisiología , Vitelogeninas/genéticaRESUMEN
Nosema ceranae is a hot topic in honey bee health as reflected by numerous papers published every year. This review presents an update of the knowledge generated in the last 12 years in the field of N. ceranae research, addressing the routes of transmission, population structure and genetic diversity. This includes description of how the infection modifies the honey bee's metabolism, the immune response and other vital functions. The effects on individual honey bees will have a direct impact on the colony by leading to losses in the adult's population. The absence of clear clinical signs could keep the infection unnoticed by the beekeeper for long periods. The influence of the environmental conditions, beekeeping practices, bee genetics and the interaction with pesticides and other pathogens will have a direct influence on the prognosis of the disease. This review is approached from the point of view of the Mediterranean countries where the professional beekeeping has a high representation and where this pathogen is reported as an important threat.
Asunto(s)
Apicultura/métodos , Abejas/parasitología , Interacciones Huésped-Parásitos/fisiología , Nosema/crecimiento & desarrollo , Enfermedades Parasitarias en Animales/transmisión , Animales , Nosema/genéticaRESUMEN
Foraging in honeybees is energetically demanding. Here, we examined whether stressors, which generally increase metabolic demands, can impair foraging performance. A controlled non-pathogenic stressor (immune challenge) resulted in a change in the foraging preferences of bees. It reduced pollen foraging and increased the duration of trips in pollen foragers. Stress also reduced the amount of octopamine in the brain of pollen foragers (a biogenic amine involved in the regulation of foraging and flight behaviour in insects). According to the literature, flight metabolic rate is higher during pollen foraging than during nectar foraging, and nectar gives a higher energetic return relative to the foraging effort when compared with pollen. We thus propose that stress might be particularly detrimental to the performance of pollen foragers, and stressed bees prefer the energy-rich resource of nectar. In conclusion, stress, even at low levels, could have consequences for bee foraging behaviour and thereby the nutritional balance of the colony.
Asunto(s)
Abejas/fisiología , Octopamina/metabolismo , Polinización , Animales , Abejas/inmunología , Encéfalo/metabolismo , Conducta Alimentaria , Nueva Gales del Sur , Polen , Distribución Aleatoria , Estrés Fisiológico/inmunologíaRESUMEN
Nosema ceranae is an intracellular microsporidian parasite that infects epithelial cells of the honey bee (Apis mellifera) midgut. Previous studies have shown that Nosema may alter cell renewal and apoptosis in honey bees. We found that the amount of apoptotic cells progressively declines from the anterior towards posterior regions of the midgut in Nosema-infected sensitive bees. There was no such pattern in the infected Nosema tolerant honey bees and controls. These data provide additional evidence that N. ceranae appears to alter apoptosis in its host cells for its own advantage.
Asunto(s)
Apoptosis , Abejas/parasitología , Microsporidiosis/patología , Nosema/patogenicidad , Animales , Sistema Digestivo , Interacciones Huésped-Parásitos , Nosema/fisiologíaRESUMEN
BACKGROUND: Organisms typically face infection by diverse pathogens, and hosts are thought to have developed specific responses to each type of pathogen they encounter. The advent of transcriptomics now makes it possible to test this hypothesis and compare host gene expression responses to multiple pathogens at a genome-wide scale. Here, we performed a meta-analysis of multiple published and new transcriptomes using a newly developed bioinformatics approach that filters genes based on their expression profile across datasets. Thereby, we identified common and unique molecular responses of a model host species, the honey bee (Apis mellifera), to its major pathogens and parasites: the Microsporidia Nosema apis and Nosema ceranae, RNA viruses, and the ectoparasitic mite Varroa destructor, which transmits viruses. RESULTS: We identified a common suite of genes and conserved molecular pathways that respond to all investigated pathogens, a result that suggests a commonality in response mechanisms to diverse pathogens. We found that genes differentially expressed after infection exhibit a higher evolutionary rate than non-differentially expressed genes. Using our new bioinformatics approach, we unveiled additional pathogen-specific responses of honey bees; we found that apoptosis appeared to be an important response following microsporidian infection, while genes from the immune signalling pathways, Toll and Imd, were differentially expressed after Varroa/virus infection. Finally, we applied our bioinformatics approach and generated a gene co-expression network to identify highly connected (hub) genes that may represent important mediators and regulators of anti-pathogen responses. CONCLUSIONS: Our meta-analysis generated a comprehensive overview of the host metabolic and other biological processes that mediate interactions between insects and their pathogens. We identified key host genes and pathways that respond to phylogenetically diverse pathogens, representing an important source for future functional studies as well as offering new routes to identify or generate pathogen resilient honey bee stocks. The statistical and bioinformatics approaches that were developed for this study are broadly applicable to synthesize information across transcriptomic datasets. These approaches will likely have utility in addressing a variety of biological questions.
Asunto(s)
Abejas/genética , Interacciones Huésped-Patógeno/genética , Animales , Abejas/microbiología , Abejas/parasitología , Abejas/virología , Bases de Datos Genéticas , Evolución Molecular , Regulación de la Expresión Génica , Redes Reguladoras de Genes , Inmunidad Innata/genética , Anotación de Secuencia Molecular , Nosema/fisiología , Virus ARN/fisiología , Varroidae/fisiologíaRESUMEN
Varroa destructor is the most important ectoparasite of Apis mellifera. This review addresses the interactions between the varroa mite, its environment, and the honey bee host, mediated by an impressive number of cues and signals, including semiochemicals regulating crucial steps of the mite's life cycle. Although mechanical stimuli, temperature, and humidity play an important role, chemical communication is the most important channel. Kairomones are used at all stages of the mite's life cycle, and the exploitation of bees' brood pheromones is particularly significant given these compounds function as primer and releaser signals that regulate the social organization of the honey bee colony. V. destructor is a major problem for apiculture, and the search for novel control methods is an essential task for researchers. A detailed study of the ecological interactions of V. destructor is a prerequisite for creating strategies to sustainably manage the parasite.
Asunto(s)
Abejas/fisiología , Abejas/parasitología , Interacciones Huésped-Parásitos , Varroidae/fisiología , Animales , Apicultura , Señales (Psicología) , Feromonas/metabolismoRESUMEN
Over the past fifty years, annual honeybee (Apis mellifera) colony losses have been steadily increasing worldwide. These losses have occurred in parallel with the global spread of the honeybee parasite Varroa destructor. Indeed, Varroa mite infestations are considered to be a key explanatory factor for the widespread increase in annual honeybee colony mortality. The host-parasite relationship between honeybees and Varroa is complicated by the mite's close association with a range of honeybee viral pathogens. The 10-year history of the expanding front of Varroa infestation in New Zealand offered a rare opportunity to assess the dynamic quantitative and qualitative changes in honeybee viral landscapes in response to the arrival, spread and level of Varroa infestation. We studied the impact of de novo infestation of bee colonies by Varroa on the prevalence and titres of seven well-characterised honeybee viruses in both bees and mites, using a large-scale molecular ecology approach. We also examined the effect of the number of years since Varroa arrival on honeybee and mite viral titres. The dynamic shifts in the viral titres of black queen cell virus and Kashmir bee virus mirrored the patterns of change in Varroa infestation rates along the Varroa expansion front. The deformed wing virus (DWV) titres in bees continued to increase with Varroa infestation history, despite dropping infestation rates, which could be linked to increasing DWV titres in the mites. This suggests that the DWV titres in mites, perhaps boosted by virus replication, may be a major factor in maintaining the DWV epidemic after initial establishment. Both positive and negative associations were identified for several pairs of viruses, in response to the arrival of Varroa. These findings provide important new insights into the role of the parasitic mite Varroa destructor in influencing the viral landscape that affects honeybee colonies.
Asunto(s)
Abejas/parasitología , Abejas/virología , Interacciones Huésped-Parásitos , Infestaciones por Ácaros/veterinaria , Varroidae/parasitología , Virosis/veterinaria , Animales , Infestaciones por Ácaros/epidemiología , Infestaciones por Ácaros/parasitología , Nueva Zelanda , Prevalencia , Reacción en Cadena en Tiempo Real de la Polimerasa , Reacción en Cadena de la Polimerasa de Transcriptasa Inversa , Virosis/epidemiología , Virosis/parasitologíaRESUMEN
Host-pathogen coevolution leads to reciprocal adaptations, allowing pathogens to increase host exploitation or hosts to minimise costs of infection. As pathogen resistance is often associated with considerable costs, tolerance may be an evolutionary alternative. Here, we examined the effect of two closely related and highly host dependent intracellular gut pathogens, Nosema apis and Nosema ceranae, on the energetic state in Nosema tolerant and sensitive honeybees facing the infection. We quantified the three major haemolymph carbohydrates fructose, glucose, and trehalose using high-performance liquid chromatography (HPLC) as a measure for host energetic state. Trehalose levels in the haemolymph were negatively associated with N. apis infection intensity and with N. ceranae infection regardless of the infection intensity in sensitive honeybees. Nevertheless, there was no such association in Nosema spp. infected tolerant honeybees. These findings suggest that energy availability in tolerant honeybees was not compromised by the infection. This result obtained at the individual level may also have implications at the colony level where workers in spite of a Nosema infection can still perform as well as healthy bees, maintaining colony efficiency and productivity.
Asunto(s)
Adaptación Fisiológica , Abejas/microbiología , Metabolismo Energético , Interacciones Huésped-Patógeno , Nosema/fisiología , Animales , Abejas/fisiología , Hemolinfa , Estrés FisiológicoRESUMEN
A fundamental problem in meta-analysis is how to systematically combine information from multiple statistical tests to rigorously evaluate a single overarching hypothesis. This problem occurs in systems biology when attempting to map genomic attributes to complex phenotypes such as behavior. Behavior and other complex phenotypes are influenced by intrinsic and environmental determinants that act on the transcriptome, but little is known about how these determinants interact at the molecular level. We developed an informatic technique that identifies statistically significant meta-associations between gene expression patterns and transcription factor combinations. Deploying this technique for brain transcriptome profiles from ca. 400 individual bees, we show that diverse determinants of behavior rely on shared combinations of transcription factors. These relationships were revealed only when we considered complex and variable regulatory rules, suggesting that these shared transcription factors are used in distinct ways by different determinants. This regulatory code would have been missed by traditional gene coexpression or cis-regulatory analytic methods. We expect that our meta-analysis tools will be useful for a broad array of problems in systems biology and other fields.
Asunto(s)
Conducta Animal , Metaanálisis como Asunto , Transcripción Genética , Animales , Abejas/fisiología , Factores de Transcripción/metabolismo , TranscriptomaRESUMEN
Host-parasite interactions are often characterized by changes in the host behaviour, which are beneficial to either the parasite or the host, or are a non-adaptive byproduct of parasitism. These interactions are further complicated in animal society because individual fitness is associated with group performance. However, a better understanding of host-parasite interaction in animal society first requires the identification of individual host behavioural modification. Therefore, we challenged honey bee (Apis mellifera) workers with the parasite Nosema ceranae or an immune stimulation and tracked their flight activity over their lifetime with an optic counter. We found that bees responded differently to each stress: both Nosema-infected and immune-challenged bees performed a lower number of daily flights compared with control bees, but the duration of their flights increased and decreased over time, respectively. Overall, parasitized bees spent more time in the field each day than control bees, and the inverse was true for immune-challenged bees. Despite the stress of immune challenge, bees had a survival similar to that of control bees likely because of their restricted activity. We discuss how those different behavioural modifications could be adaptive phenotypes. This study provides new insights into how biological stress can affect the behaviour of individuals living in society and how host responses have evolved.
Asunto(s)
Conducta Apetitiva/fisiología , Abejas/inmunología , Abejas/microbiología , Vuelo Animal/fisiología , Nosema/fisiología , Animales , Interacciones Huésped-Parásitos , Estrés FisiológicoRESUMEN
Invasive vectors can induce dramatic changes in disease epidemiology. While viral emergence following geographical range expansion of a vector is well known, the influence a vector can have at the level of the host's pathobiome is less well understood. Taking advantage of the formerly heterogeneous spatial distribution of the ectoparasitic mite Varroa destructor that acts as potent virus vector among honeybees Apis mellifera, we investigated the impact of its recent global spread on the viral community of honeybees in a retrospective study of historical samples. We hypothesized that the vector has had an effect on the epidemiology of several bee viruses, potentially altering their transmissibility and/or virulence, and consequently their prevalence, abundance, or both. To test this, we quantified the prevalence and loads of 14 viruses from honeybee samples collected in mite-free and mite-infested populations in four independent geographical regions. The presence of the mite dramatically increased the prevalence and load of deformed wing virus, a cause of unsustainably high colony losses. In addition, several other viruses became more prevalent or were found at higher load in mite-infested areas, including viruses not known to be actively varroa-transmitted, but which may increase opportunistically in varroa-parasitized bees.
RESUMEN
Honey bee colonies have great societal and economic importance. The main challenge that beekeepers face is keeping bee colonies healthy under ever-changing environmental conditions. In the past two decades, beekeepers that manage colonies of Western honey bees (Apis mellifera) have become increasingly concerned by the presence of parasites and pathogens affecting the bees, the reduction in pollen and nectar availability, and the colonies' exposure to pesticides, among others. Hence, beekeepers need to know the health condition of their colonies and how to keep them alive and thriving, which creates a need for a new holistic data collection method to harmonize the flow of information from various sources that can be linked at the colony level for different health determinants, such as bee colony, environmental, socioeconomic, and genetic statuses. For this purpose, we have developed and implemented the B-GOOD (Giving Beekeeping Guidance by computational-assisted Decision Making) project as a case study to categorize the colony's health condition and find a Health Status Index (HSI). Using a 3-tier setup guided by work plans and standardized protocols, we have collected data from inside the colonies (amount of brood, disease load, honey harvest, etc.) and from their environment (floral resource availability). Most of the project's data was automatically collected by the BEEP Base Sensor System. This continuous stream of data served as the basis to determine and validate an algorithm to calculate the HSI using machine learning. In this article, we share our insights on this holistic methodology and also highlight the importance of using a standardized data language to increase the compatibility between different current and future studies. We argue that the combined management of big data will be an essential building block in the development of targeted guidance for beekeepers and for the future of sustainable beekeeping.
RESUMEN
The honeybee is a model system to study learning and memory, and Ca(2+) signals play a key role in these processes. We have cloned, expressed, and characterized the first honeybee Ca(2+) channel subunit. We identified two splice variants of the Apis CaVß Ca(2+) channel subunit (Am-CaVß) and demonstrated expression in muscle and neurons. Although AmCaVß shares with vertebrate CaVß subunits the SH3 and GK domains, it beholds a unique N terminus that is alternatively spliced in the first exon to produce a long (a) and short (b) variant. When expressed with the CaV2 channels both, AmCaVßa and AmCaVßb, increase current amplitude, shift the voltage-sensitivity of the channel, and slow channel inactivation as the vertebrate CaVß2a subunit does. However, as opposed to CaVß2a, slow inactivation induced by Am-CaVßa was insensitive to palmitoylation but displayed a unique PI3K sensitivity. Inactivation produced by the b variant was PI3K-insensitive but staurosporine/H89-sensitive. Deletion of the first exon suppressed the sensitivity to PI3K inhibitors, staurosporine, or H89. Recording of Ba(2+) currents in Apis neurons or muscle cells evidenced a sensitivity to PI3K inhibitors and H89, suggesting that both AmCaVß variants may be important to couple cell signaling to Ca(2+) entry in vivo. Functional interactions with phospho-inositide and identification of phosphorylation sites in AmCaVßa and AmCaVßb N termini, respectively, suggest that AmCaVß splicing promoted two novel and alternative modes of regulation of channel activity with specific signaling pathways. This is the first description of a splicing-dependent kinase switch in the regulation of Ca(2+) channel activity by CaVß subunit.
Asunto(s)
Potenciales de Acción , Abejas/metabolismo , Canales de Calcio/metabolismo , Proteínas de Insectos/metabolismo , Empalme Alternativo , Secuencia de Aminoácidos , Animales , Abejas/química , Abejas/genética , Bloqueadores de los Canales de Calcio/farmacología , Canales de Calcio/química , Canales de Calcio/genética , Células Cultivadas , Exones , Eliminación de Gen , Células HEK293 , Humanos , Proteínas de Insectos/química , Proteínas de Insectos/genética , Datos de Secuencia Molecular , Fibras Musculares Esqueléticas/fisiología , Neuronas/fisiología , Fosfatidilinositol 3-Quinasas/farmacología , Inhibidores de las Quinasa Fosfoinosítidos-3 , Fosforilación , Inhibidores de Proteínas Quinasas/farmacología , Estructura Terciaria de Proteína , Subunidades de Proteína/química , Subunidades de Proteína/genética , Subunidades de Proteína/metabolismo , XenopusRESUMEN
BACKGROUND: Exclusion from a social group is an effective way to avoid parasite transmission. This type of social removal has also been proposed as a form of collective defense, or social immunity, in eusocial insect groups. If parasitic modification of host behavior is widespread in social insects, the underlying physiological and neuronal mechanisms remain to be investigated. We studied this phenomenon in honey bees parasitized by the mite Varroa destructor or microsporidia Nosema ceranae, which make bees leave the hive precociously. We characterized the chemical, behavioral and neurogenomic changes in parasitized bees, and compared the effects of both parasites. RESULTS: Analysis of cuticular hydrocarbon (CHC) profiles by gas chromatography coupled with mass spectrophotometry (GC-MS) showed changes in honey bees parasitized by either Nosema ceranae or Varroa destructor after 5 days of infestation. Levels of 10-HDA, an antiseptic important for social immunity, did not change in response to parasitism. Behavioral analysis of N. ceranae- or V. destructor- parasitized bees revealed no significant differences in their behavioral acts or social interactions with nestmates. Digital gene expression (DGE) analysis of parasitized honey bee brains demonstrated that, despite the difference in developmental stage at which the bee is parasitized, Nosema and Varroa-infested bees shared more gene changes with each other than with honey bee brain expression gene sets for forager or nurse castes. CONCLUSIONS: Parasitism by Nosema or Varroa induces changes to both the CHC profiles on the surface of the bee and transcriptomic profiles in the brain, but within the social context of the hive, does not result in observable effects on her behavior or behavior towards her. While parasitized bees are reported to leave the hive as foragers, their brain transcription profiles suggest that their behavior is not driven by the same molecular pathways that induce foraging behavior.
Asunto(s)
Abejas/parasitología , Encéfalo/metabolismo , Ácaros , Nosema , Conducta Social , Animales , Abejas/fisiología , Interacciones Huésped-Parásitos , Hidrocarburos/química , TranscriptomaRESUMEN
Parasites are known to cause the loss of individuals in social insects. In honey bee colonies the disappearance of foragers is a common factor of the wide extended colony losses. The emergent parasite of the European honey bee Nosema ceranae has been found to reduce homing and orientation skills and alter metabolism of forager bees. N. ceranae-infected bees also show changes in Ethyl Oleate (EO) levels, which is so far the only primer pheromone identified in workers that is involved in foraging behavior. Thus, we hypothesized that N. ceranae (i) modifies flight activity of honey bees and (ii) induces EO changes that can alter foraging behavior of nestmates. We compared flight activity of infected bees and non-infected bees in small colonies using an electronic optic bee counter during 28 days. We measured EO levels by gas chromatography-mass spectrometry and spore-counts. Bee mortality was estimated at the end of the experiment. Infected bees showed precocious and a higher flight activity than healthy bees, which agreed with the more elevated EO titers of infected bees and reduced lifespan. Our results suggest that the higher EO levels of infected bees might delay the behavioral maturation of same age healthy bees, which might explain their lower level of activity. We propose that delayed behavioral maturation of healthy bees might be a protective response to infection, as healthy bees would be performing less risky tasks inside the hive, thus extending their lifespan. We also discuss the potential of increased flight activity of infected bees to reduce pathogen transmission inside the hive. Further research is needed to understand the consequences of host behavioral changes on pathogen transmission. This knowledge may contribute to enhance natural colony defense behaviors through beekeeping practices to reduce probability of colony losses.
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Abejas/microbiología , Conducta Animal , Fenómenos de Retorno al Lugar Habitual , Nosema/fisiología , Feromonas/metabolismo , Animales , Abejas/metabolismo , Abejas/fisiología , Colapso de Colonias , Vuelo Animal , Interacciones Huésped-Parásitos , Conducta SocialRESUMEN
Chemical communication is a widely used mode of communication for social insects and has been demonstrated to be involved in many behaviours and physiological processes such as reproduction, nutrition or the fight against parasites and pathogens. In the honey bee, Apis mellifera, the release of chemical compounds by the brood plays a role in worker behaviour, physiology, and foraging activities and colony health as a whole. Several compounds have already been described as brood pheromones, such as components of the brood ester pheromone and (E)-ß-ocimene. Several other compounds originating from diseased or varroa-infested brood cells have been described as triggering the hygienic behaviour of workers. So far, studies of brood emissions have focused on specific stages of development and little is known about the emission of volatile organic compounds by the brood. In this study, we investigate the semiochemical profile of worker honey bee brood during its whole developmental cycle, from egg to emergence, with a specific focus on volatile organic compounds. We describe variation in emissions of thirty-two volatile organic compounds between brood stages. We highlight candidate compounds that are particularly abundant in specific stages and discuss their potential biological significance.
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Varroidae , Compuestos Orgánicos Volátiles , Abejas , Animales , Larva/fisiología , Feromonas , Conducta Animal , Varroidae/fisiologíaRESUMEN
Information on honeybee foraging performance and especially bee loss rates at the colony level are crucial for evaluating the magnitude of effects due to pesticide exposure, thereby ensuring that protection goals for honeybee colonies are met (i.e. threshold of acceptable effects). However, current methods for monitoring honeybee foraging activity and mortality are very approximate (visual records) or are time-limited and mostly based on single cohort analysis. We therefore assess the potential of bee counters, that enable a colony-level and continuous monitoring of bee flight activity and mortality, in pesticide risk assessment. After assessing the background activity and bee loss rates, we exposed colonies to two concentrations of sulfoxaflor (a neurotoxic insecticide) in sugar syrup: a concentration that was considered to be field realistic (0.59 µg/ml) and a higher concentration (2.36 µg/ml) representing a worst-case exposure scenario. We did not find any effect of the field-realistic concentration on flight activity and bee loss rates. However, a two-fold decrease in daily flight activity and a 10-fold increase in daily bee losses were detected in colonies exposed to the highest sulfoxaflor concentration as compared to before exposure. When compared to the theoretical trigger values associated with the specific protection goal of 7 % colony-size reduction, the observed fold changes in daily bee losses were often found to be at risk for colonies. In conclusion, the real-time and colony-level monitoring of bee loss rates, combined with threshold values indicating at which levels bee loss rates threaten the colony, have great potential for improving regulatory pesticide risk assessments for honeybees under field conditions.