Searching for reward motivates and drives behaviour. In honey bees, Apis mellifera, specialized pollen foragers are attracted to and learn odours with pollen. However, pollen's role as a reward remains poorly understood. Unlike nectar, pollen is not ingested during collection. We hypothesized that pollen (but not nectar) foragers could learn pollen by the sole antennal or tarsal stimulation. Then, we tested how pairing of pollen (either hand- or bee-collected) and a neutral odour during a pre-conditioning affects performance of both pollen and nectar foragers during the classical conditioning of the proboscis extension response. Secondly, we tested whether nectar and pollen foragers perceive the simultaneous presentation of pollen (on the tarsi) and sugar (on the antennae) as a better reinforcement than sucrose alone. Finally, we searched for differences in learning of the pollen and nectar foragers when they were prevented from ingesting the reward during the conditioning. Differences in pollen reinforced learning correlate with division of labour between pollen and nectar foragers. Results show that pollen foragers performed better than nectar foragers during the conditioning phase after being pre-conditioned with pollen. Pollen foragers also performed better than nectar foragers in both the acquisition and extinction phases of the conditioning, when reinforced with the dual reward. Consistently, pollen foragers showed improved abilities to learn cues reinforced without sugar ingestion. We discussed that differences in how pollen and nectar foragers respond to a cue associated with pollen greatly contribute to the physiological mechanism that underlies foraging specialization in the honeybee.

Division of labor is central to the ecological success of social insects. Among foragers of the honey bee, specialization for collecting nectar or pollen correlates with their sensitivity to sucrose. So far, differences in gustatory perception have been mostly studied in bees returning to the hive, but not during foraging. Here, we showed that the phase of the foraging visit (i.e. beginning or end) interacts with foraging specialization (i.e. predisposition to collect pollen or nectar) to modulate sucrose and pollen sensitivity in foragers. In concordance with previous studies, pollen foragers presented higher sucrose responsiveness than nectar foragers at the end of the foraging visit. On the contrary, pollen foragers were less responsive than nectar foragers at the beginning of the visit. Consistently, free-flying foragers accepted less concentrated sucrose solution during pollen gathering than immediately after entering the hive. Pollen perception also changes throughout foraging, as pollen foragers captured at the beginning of the visit learned and retained memories better when they were conditioned with pollen + sucrose as reward than when we used sucrose alone. Altogether, our results support the idea that changes in foragers' perception throughout the foraging visit contributes to task specialization.

Division of labor is central to the ecological success of social insects. Among foragers of the honeybee specialization for collecting nectar or pollen correlates with their sensitivity to sucrose. So far, differences in gustatory perception have been mostly studied in bees returning to the hive, but not during foraging. Here, we showed that the phase of the foraging visit (i.e. beginning or end) interacts with foraging specialization (i.e. predisposition to collect pollen or nectar) to modulate sucrose and pollen sensitivity in foragers. In concordance with previous studies, pollen foragers presented higher sucrose responsiveness than nectar foragers at the end of the foraging visit. On the contrary, pollen foragers were less responsive than nectar foragers at the beginning of the visit. Consistently, free-flying foragers accepted less concentrated sucrose solution during pollen gathering than immediately after entering the hive. Pollen perception also changes throughout foraging, as pollen foragers captured at the beginning of the visit learned and retained memories better when they were conditioned with pollen + sucrose as reward than when we used sucrose alone. Altogether, our results support the idea that changes in foragers' perception throughout the foraging visit contributes to task specialization.

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Pollen selection affects honeybee colony development and productivity. Considering that pollen is consumed by young in-hive bees, and not by foragers, we hypothesized that young bees learn pollen cues and adjust their preferences to the most suitable pollens. To assess whether young bees show preferences based on learning for highly or poorly suitable pollens, we measured consumption preferences for two pure monofloral pollens after the bees had experienced one of them adulterated with a deterrent (amygdalin or quinine) or a phagostimulant (linoleic acid). Preferences were obtained from nurse-aged bees confined in cages and from nurse bees in open colonies. Furthermore, we tested the bees’ orientation in a Y-maze using a neutral odour (Linalool or Nonanal) that had been previously associated with an amygdalin-adulterated pollen. Consumption preferences of bees, both in cages and in colonies, were reduced for pollens that had been adulterated with deterrents and increased for pollens that had been supplemented with linoleic acid. In the Y-maze, individuals consistently avoided the odours that they had previously experienced paired with the deterrent-adulterated pollen. Results show that nurse-aged bees associate pollen-based or pollen-related cues with either a distasteful/malaise experience or a tasty/nutritious event, leading to memories that bias their pollen-mediated response.

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