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The targeted pollination strategy has shown positive results in directing honey bees to crop flowers offering nectar along with pollen as reward. Kiwifruit is a functionally dioecious species, which relies on bees to transport pollen from staminate to pistillate nectarless flowers. Following the targeted pollination procedures recently validated, we first developed a mimic odor (KM) based on kiwifruit floral volatiles for which bees showed the highest level of generalization to the natural floral scent, although the response towards pistillate flowers was higher than towards staminate flowers. Then, in the field, feeding colonies KM-scented sucrose solution resulted in higher amounts of kiwifruit pollen collected by honey bees compared to control colonies fed unscented sucrose solution. Our results support the hypothesis that olfactory conditioning bees biases their foraging preferences in a nectarless crop, given the higher visitation to target flowers despite having provided the mimic odor paired with a sugar reward.

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As the most abundant pollinator insect in crops, Apis mellifera is a sentinel species of the pollinator communities. In these ecosystems, honey bees of different ages and developmental stages are exposed to diverse agrochemicals. However, most toxicological studies analyse the immediate effects during exposure. Late effects during adulthood after early exposure to pollutants during larval development are poorly studied in bees. The herbicide glyphosate (GLY) is the most applied pesticide worldwide. GLY has been detected in honey and beebread from hives near treated crops. Alterations in growth, morphogenesis or organogenesis during pre-imaginal development could induce late adverse effects after the emergence. Previous studies have demonstrated that GLY alters honey bee development, immediately affecting survival, growth and metabolism, followed by late teratogenic effects. The present study aims to determine the late impact on the behaviour and physiology of adult bees after pre-imaginal exposure to GLY. For that, we reared brood in vitro or in the hive with sub-chronic exposure to the herbicide with the average detected concentration in hives. Then, all newly emerged bees were reared in an incubator until maturity and tested when they became nurse-aged bees. Three behavioural responses were assessed as markers of cognitive and physiological impairment. Our results show i) decreased sensitivity to sucrose regardless of the rearing procedure, ii) increased choice latency and locomotor alterations during chemotaxis and iii) impaired associative learning. These late toxicity signs could indicate adverse effects on task performance and colony efficiency.

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Reception of chemical information from the environment is crucial for insects' survival and reproduction. The chemosensory reception mainly occurs by the antennae and mouth parts of the insect, when the stimulus contacts the chemoreceptors located within the sensilla. Chemosensory receptor genes have been well-studied in some social hymenopterans such as ants, honeybees, and wasps. However, although stingless bees are the most representative group of eusocial bees, little is known about their odorant, gustatory, and ionotropic receptor genes. Here, we analyze the transcriptome of the proboscis and antennae of the stingless bee Tetragonisca fiebrigi. We identified and annotated 9 gustatory and 15 ionotropic receptors. Regarding the odorant receptors, we identified 204, and we were able to annotate 161 of them. In addition, we compared the chemosensory receptor genes of T. fiebrigi with those annotated for other species of Hymenoptera. We found that T. fiebrigi showed the largest number of odorant receptors compared with other bees. Genetic expansions were identified in the subfamilies 9-exon, which was also expanded in ants and paper wasps; in G02A, including receptors potentially mediating social behavior; and in GUnC, which has been related to pollen and nectar scent detection. Our study provides the first report of chemosensory receptor genes in T. fiebrigi and represents a resource for future molecular and physiological research in this and other stingless bee species.

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The areas devoted to agriculture that depend on pollinators have been sharply increased in the last decades with a concomitant growing global demand for pollination services. This forces to consider new strategies in pollinators' management to improve their efficiency. To promote a precision pollination towards a specific crop, we developed two simple synthetic odorant mixtures that honey bees generalized with their respective natural floral scents of the crop. We chose two commercial crops for fruit production that often coexist in agricultural settings, the apple (Malus domesticus) and the pear trees (Pyrus communis). Feeding colonies with sucrose solution scented with the apple mimic (AM) or the pear mimic (PM) odour enabled the establishment of olfactory memories that can bias bees towards the flowers of these trees. Encompassing different experimental approaches, our results support the offering of scented food to improve foraging and pollination activities of honey bees. The circulation of AM-scented sucrose solution inside the hive promoted higher colony activity, probably associated with greater activity of nectar foragers. The offering of PM-scented sucrose solution did not increase colony activity but led to greater pollen collection, which is consistent with pear flowers offering mainly pollen as resources for the bees. Results obtained from apple and pear crops suggest that the offering of AM- and PM-scented sucrose solution increased fruit yields. This preliminary study highlights the role of in-hive olfactory learning to bias foraging preferences within pome fruit crops.

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The increasing demand on pollination services leads food industry to consider new strategies for management of pollinators to improve their efficiency in agroecosystems. Recently, it was demonstrated that feeding beehives food scented with an odorant mixture mimicking the floral scent of a crop (sunflower mimic, SM) enhanced foraging activity and improved recruitment to the target inflorescences, which led to higher density of bees on the crop and significantly increased yields. Besides, the oral administration of nonsugar compounds (NSC) naturally found in nectars (caffeine and arginine) improved short and long-term olfactory memory retention in conditioned bees under laboratory conditions. To test the effect of offering of SM-scented food supplemented with NSC on honeybees pollinating sunflower for hybrid seed production, in a commercial plantation we fed colonies SM-scented food (control), and SM-scented food supplemented with either caffeine, arginine, or a mixture of both, in field realistic concentrations. Their foraging activity was assessed at the hive and on the crop up to 90 h after treatment, and sunflower yield was estimated prior to harvest. Our field results show that SM + Mix-treated colonies exhibited the highest incoming rates and densities on the crop. Additionally, overall seed mass was significantly higher by 20% on inflorescences close to these colonies than control colonies. Such results suggest that combined NSC potentiate olfactory learning of a mimic floral odor inside the hive, promoting faster colony-level foraging responses and increasing crop production.

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Despite Apis mellifera being the most widely managed pollinator to enhance crop production, they are not the most suitable species for highbush blueberries, which possess restrictive floral morphology and require buzz-pollination. Thus, the South American bumblebee Bombus pauloensis is increasingly managed as an alternative species in this crop alongside honeybees. Herein, we evaluated the foraging patterns of the two species, concerning the potential pollen transfer between two blueberry co-blooming cultivars grown under open high tunnels during two seasons considering different colony densities. Both managed pollinators showed different foraging patterns, influenced by the cultivar identity which varied in their floral morphology and nectar production. Our results demonstrate that both species are efficient foragers on highbush blueberry and further suggest that they contribute positively to its pollination in complementary ways: while bumblebees were more effective at the individual level (visited more flowers and carried more pollen), the greater densities of honeybee foragers overcame the difficulties imposed by the flower morphology, irrespective of the stocking rate. This study supports the addition of managed native bumblebees alongside honeybees to enhance pollination services and emphasizes the importance of examining behavioural aspects to optimize management practices in pollinator-dependent crops.

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The honeybee Apis mellifera is exposed to agricultural intensification, which leads to an improved reliance upon pesticide use and the reduction of floral diversity. In the present study, we assess the changes in the colony activity and the expression profile of genes involved in xenobiotic detoxification in larvae and adult honeybees from three apiaries located in agricultural environments that differ in their proportion of the crop/wild flora. We evaluated these variables before and after the administration of a mixture of three herbicides during the summer season. The expression of several cytochrome P450 monooxygenases decreased significantly in larvae after post-emergence weed control and showed significant differences between apiaries in the case of honeybee workers. Principal component analysis (PCA) revealed that colonies located in the plot near to a wetland area exhibited a different relative gene expression profile after herbicide application compared with the other plots. Moreover, we found significant positive correlations between pollen collection and the pesticide detoxification genes that discriminated between plots in the PCA. Our results suggest that nutrition may modify herbicide impact on honeybees and that larvae are more harmed than adults in agroecosystems, a factor that will alter the colonies' population growth at the end of the blooming period.

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The alkaloid caffeine and the amino acid arginine are present as secondary compounds in nectars of some flower species visited by pollinators. Each of these compounds affects honeybee appetitive behaviours by improving foraging activity and learning. While caffeine potentiates responses of mushroom body neurons involved in honeybee learning processes, arginine acts as precursor of nitric oxide, enhancing the protein synthesis involved in memory formation. Despite existing evidence on how these compounds affect honeybee cognitive ability individually, their combined effect on this is still unknown. We evaluated acquisition and memory retention in a classical olfactory conditioning procedure, in which the reward (sucrose solution) contained traces of caffeine, arginine or a mixture of the two. The results indicate that the presence of the single compounds and their most concentrated mixture increases bees' learning performance. However, memory retention, measured in the short and long term, increases significantly only in those treatments offering combinations of the two compounds in the reward. Additionally, the most concentrated mixture triggers a significant survival rate in the conditioned bees. Thus, some nectar compounds, when combined, show synergistic effects on cognitive ability and survival in an insect.

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Sleep plays an essential role in both neural and energetic homeostasis of animals. Honey bees (Apis mellifera) manifest the sleep state as a reduction in muscle tone and antennal movements, which is susceptible to physical or chemical disturbances. This social insect is one of the most important pollinators in agricultural ecosystems, being exposed to a great variety of agrochemicals, which might affect its sleep behaviour. The intake of glyphosate (GLY), the herbicide most widely used worldwide, impairs learning, gustatory responsiveness and navigation in honey bees. In general, these cognitive abilities are linked with the amount and quality of sleep. Furthermore, it has been reported that animals exposed to sleep disturbances show impairments in both metabolism and memory consolidation. Consequently, we assessed the sleep pattern of bees fed with a sugar solution containing GLY (0, 25, 50 and 100 ng) by quantifying their antennal activity during the scotophase. We found that the ingestion of 50 ng of GLY decreased both antennal activity and sleep bout frequency. This sleep deepening after GLY intake could be explained as a consequence of the regenerative function of sleep and the metabolic stress induced by the herbicide.

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