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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 honey bee Apis mellifera is a sentinel species of the pollinator community which is exposed to a wide variety of pesticides. In the last half-century, the pesticide most applied worldwide has been the herbicide glyphosate (GLY) used for weed control and with microbiocide effects. After its application in crops, the GLY residues have been detected in flowers visited by honey bees as well as in the stored food of their hives. Therefore, the honey bee brood can ingest the herbicide during larval development. Recent studies proved that GLY has detrimental effects on adult honey bees and other insects associated with the disturbance of their gut microbiota. GLY induces changes in the growth, metabolism and survival of honey bees and stingless bees reared in vitro. However, the effect of GLY on larval microbiota is unknown so far and there are few studies with an in-hive exposure to GLY. For these reasons, this study aims to determine whether GLY induces dysbiosis in honey bee larvae and affects their metamorphosis during the exposure period (pre-defecation) and the post-exposure period. Furthermore, we assessed this herbicide in vitro and in the hive to compare its effects on different rearing procedures. Finally, we tested the pigment BLUE1 as an indirect exposure marker to detect and estimate the in-hive intake concentration of GLY. Our results indicate that the intake of field-relevant concentrations of GLY induced a slowdown in growth with dysbiosis in the larval gut microbiota followed by late effects on their metamorphosis such as teratogenesis and mortality of newly emerged bees. Nevertheless, brood from the same colonies expressed different signs of toxicity depending on the rearing procedure and in a dose-dependent manner.

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Honey bees represent an iconic model animal for studying the underlying mechanisms affecting advanced sensory and cognitive abilities during communication among colony mates. After von Frisch discovered the functional value of the waggle dance, this complex motor pattern led ethologists and neuroscientists to study its neural mechanism, behavioral significance, and implications for a collective organization. Recent studies have revealed some of the mechanisms involved in this symbolic form of communication by using conventional behavioral and pharmacological assays, neurobiological studies, comprehensive molecular and connectome analyses, and computational models. This review summarizes several critical behavioral and brain processes and mechanisms involved in waggle dance communication. We focus on the role of neuromodulators in the dancer and the recruited follower, the interneurons and their related processing in the first mechano-processing, and the computational navigation centers of insect brains.

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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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Honeybees (Apis mellifera) use cues and signals to recruit nestmates to profitable food sources. Here, we investigated whether the type of resource advertised within the colony (i.e. pollen or nectar) correlates with the choices of recruits at the feeding site. We observed that pollen recruits preferred to collect pollen once arrived for the first time at the feeding site, while nectar recruits preferred to forage sucrose solutions. Bees recruited by foragers carrying both resources showed intermediate preferences. Studying the plasticity of this response, we found that nectar recruits have a low probability of switching to pollen collection, yet pollen recruits were likely to switch to sucrose solution of increasing concentrations. Our results show that cues associated with the advertised resource type correlate with the foraging tendency of recruits for pollen and sucrose solution, a feature that would guarantee an efficient resource collection.

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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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Regulation of pollen and nectar foraging in honeybees is linked to differences in the sensitivity to the reward. Octopamine (OA) participates in the processing of reward-related information in the bee brain, being a candidate to mediate and modulate the division of labour among pollen and nectar foragers. Here we tested the hypothesis that OA affects the resource preferences of foragers. We first investigated whether oral administration of OA is involved in the transition from nectar to pollen foraging. We quantified the percentage of OA-treated bees that switched from a sucrose solution to a pollen feeder when the sugar concentration was decreased experimentally. We also evaluated if feeding the colonies sucrose solution containing OA increases the rate of bees collecting pollen. Finally, we quantified OA and tyramine (TYR) receptor genes expression of pollen and nectar foragers in different parts of the brain, as a putative mechanism that affects the decision-making process regarding the resource type collected. Adding OA in the food modified the probability that foragers switch from nectar to pollen collection. The proportion of pollen foragers also increased after feeding colonies with OA-containing food. Furthermore, the expression level of the AmoctαR1 was upregulated in foragers arriving at pollen sources compared with those arriving at sugar-water feeders. Using age-matched pollen and nectar foragers that returned to the hive, we detected an upregulated expression of a TYR receptor gene in the suboesophageal ganglia. These findings support our prediction that OA signalling affects the decision in honeybee foragers to collect pollen or nectar.

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The growing global demand for pollination services leads producers to consider new strategies in pollinator management to improve its efficiency in agroecosystems [1-3]. Central place foragers, like honeybees, learn floral cues not only in the field but also inside the nest, where resource cues introduced into the hive improve foraging by guiding bees toward the learned stimuli [4]. In this regard, attempts to condition bees with crop-odor-scented food produced ambiguous results and lacked yield measurements [5-7]. To deepen our understanding of the use of odors as part of a precision pollination strategy, we developed a simple synthetic odorant mixture that bees generalized with the natural floral scent of sunflower for hybrid seed production, an economically important and highly pollinator-dependent crop [8]. Encompassing different experimental approaches, our results show that feeding colonies food scented with the sunflower mimic (SM) odor enabled the establishment of olfactory memories that biased bees to the sunflower crop. The offering of a rewarded odor mimicking the sunflower floral fragrance promoted higher foraging activity, increased the proportion of dances advertising the target inflorescences and reduced delays in dance onset, positively affected the density of bees on the crop, and increased yields from 29% to 57% in different sunflower hybrids. This study highlights the role of olfactory learning within the social context of the hive to bias foraging preferences in a novel agricultural environment and suggest that improvements in the tested parameters were due to bees anticipated response to the sunflower scent.

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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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In stingless bees, unlike honey bees, the relationship between chemosensory abilities and colony labor division has been poorly studied. Here we examined odor reception and gustatory responsiveness of the stingless bee Tetragonisca angustula focusing on workers, whose are involved in different tasks. Using the proboscis extension response, we studied sucrose response thresholds (SRTs) of foragers and guards. Peripheral responses to odors at the antennae were recorded by electroantennography (EAG). Additionally, we quantified and described the number and type of sensilla present on the antennae using scanning electron microscopy. Foragers' SRTs changed according to the resource collected: nonpollen foragers showed higher SRTs than pollen foragers and guards, that showed similar sucrose responsiveness. EAG signal strength of both foragers and guards increased with increasing odor concentration. Interestingly, guard bees showed the highest response to citral, an odor that triggers defensive behavior in T. angustula. Type and number of sensilla present in the antennae of guards and foragers were similar. Our results suggest that differences found in chemosensory responses among worker subcastes are task dependent.

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The honey bee Apis mellifera is the most abundant managed pollinator in diverse crops worldwide. Consequently, it is exposed to a plethora of environmental stressors, among which are the agrochemicals. In agroecosystems, the herbicide glyphosate (GLY) is one of the most applied. In laboratory assessments, GLY affects the honey bee larval development by delaying its moulting, among other negative effects. However, it is still unknown how GLY affects larval physiology when there are no observable signs of toxicity. We carried out a longitudinal experimental design using the in vitro rearing procedure. Larvae were fed with food containing or not a sub-lethal dose of GLY in chronic exposure (120 h). Individuals without observable signs of toxicity were sampled and their gene expression profile was analyzed with a transcriptomic approach to compare between treatments. Even though 29% of larvae were asymptomatic in the exposed group, they showed transcriptional changes in several genes after the GLY chronic intake. A total of 19 transcripts were found to be differentially expressed in the RNA-Seq experiment, mainly linked with defensive response and intermediary metabolism processes. Furthermore, the enriched functional categories in the transcriptome of the exposed asymptomatic larvae were linked with enzymes with catalytic and redox activity. Our results suggest an enhanced catabolism and oxidative metabolism in honey bee larvae as a consequence of the sub-lethal exposure to GLY, even in the absence of observable symptoms.

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Insect pollination is issential for hybrid seed production systems, among which, introduced and native bees are the primary pollinating agents transferring pollen from male fertile (MF) to male sterile (MS) lines. On a highly dimorphic sunflower (Helianthus annuus) crop, we assessed the foraging behavior of solitary Melissodes bees and honey bees Apis mellifera. We found that Melissodes spp. were dominant in and showed fidelity to MF plants, gathering sunflower pollen efficiently throughout the day. In contrast, honey bees dominated on MS lines, mostly gathered nectar and exhibited high floral constancy, even after interacting with a second visitor. Also, honey bees carried sunflower pollen on their bodies while visiting MS inflorescences. This study highlights the need for a thorough understanding of the factors involved in a pollinator-dependent agroecosystem crop to assess the contribution of native bees on pollination of crops which offer resources spatially separated in two highly dimorphic parental lines.

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The honeybee Apis mellifera is an important pollinator in both undisturbed and agricultural ecosystems. Its great versatility as an experimental model makes it an excellent proxy to evaluate the environmental impact of agrochemicals using current methodologies and procedures in environmental toxicology. The increase in agrochemical use, including those that do not target insects directly, can have deleterious effects if carried out indiscriminately. This seems to be the case of the herbicide glyphosate (GLY), the most widely used agrochemical worldwide. Its presence in honey has been reported in samples obtained from different environments. Hence, to understand its current and potential risks for this pollinator it has become essential to not only study the effects on honeybee colonies located in agricultural settings, but also its effects under laboratory conditions. Subtle deleterious effects can be detected using experimental approaches. GLY negatively affects associative learning processes of foragers, cognitive and sensory abilities of young hive bees and promotes delays in brood development. An integrated approach that considers behavior, physiology, and development allows not only to determine the effects of this agrochemical on this eusocial insect from an experimental perspective, but also to infer putative effects in disturbed environments where it is omnipresent.

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The honey bee is the most frequently used species in pollination services for diverse crops. In onion crops (Allium cepa), however, bees avoid visiting certain varieties, being attracted differently to male sterile (MS) and fertile (OP) lines. These differences might be based on the phenolic profiles of the cultivars' nectars. To understand the relationship between nectar composition and pollinator attraction to different onion lines, we tested sensory and cognitive abilities and palatability in honey bees exposed to MS and OP onion nectars and sugar solutions mimicking them. We evaluated the proboscis extension response (PER) after antennal contact (unconditioned response) to MS or OP onion nectars, finding no statistical differences, which indicates similar gustatory perception for the two nectars. We also performed food uptake assays to test palatability of different artificial nectars, considering their flavonoids and potassium content. The presence of potassium decreased the palatability of the artificial nectars. Finally, we evaluated the bees' cognitive abilities when the reward (unconditioned stimulus) offered during conditioning PER assays presents differences in composition. We found that potassium by itself impaired learning; however, such impairment was even higher when naringenin and quercetin were added in the unconditioned stimulus (MS nectar mimic). Interestingly, potassium together with luteolin (OP nectar mimic) improved learning. Our study demonstrates that the differences in the nectars' flavonoid profiles combined with their high potassium content could explain the previously reported differences in attractiveness between onion lines, suggesting an important role of nectar compounds other than sugars for the attractiveness of flowers to pollinators.

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