Pollen reinforces learning in honey bee pollen foragers but not in nectar foragers

Abstract

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.

Correlation between octopaminergic signalling and foraging task specialisation in honeybees

“…Because the SOG is located in the ventral nerve cord, between the brain and the thoracic and abdominal ganglia, it could serve as a relay centre for information descending and ascending along the ventral nerve cord, which might be important for both the assessment of pollen with their tarsi for the control and coordination of leg movements during pollen gathering. In addition, ventral unpaired median neurons, all octopaminergic neurons, 73 innervate different parts of the SOG and the brain, and might mediate reinforcement with pollen 65 . Together, our results suggest that TYR receptor Amtyr1 in the SOG is involved in the division of labour among pollen and nectar foragers.…”

“…Because high OA levels in the brain modulate response thresholds for stimuli like odours 21 and sucrose, 20 it is plausible that OA‐treated bees were more sensitive and responsive to certain chemosensory cues of pollen, such as volatiles and tastes, 61,62 which are responsible for attracting the bees and eliciting pollen foraging behaviour 63,64 . Furthermore, because bees showing lower SRTs are less demanding regarding the reward, 61 they might also learn better with nutritional and non‐nutritional compounds available in the pollen 65 …”

Young honeybees show learned preferences after experiencing adulterated pollen

“…In the field, pollen selection might be based on the foragers’ innate preferences 27 – 30 to pollen-based cues (i.e., pollen odour, colour, and taste) and on their previous experience with neutral cues associated to pollen sources (henceforth: pollen-related cues 31 – 33 ). However, it is likely that pollen selection by foragers may be limited to the perception of pre-ingestive pollen cues (foragers do not consume fresh pollen at the source) .…”

“…Considering that nurse bees might be making decisions regarding which pollen to use to nourish the colony, we studied whether their behaviour is plastic enough to mediate the selection of pollen. We hypothesized that young bees can associate species-specific pollen-based and/or neutral pollen-related cues with nutritional or non-nutritional compounds, when pollen is used as a reinforcement 33 . We expected tasty and nutritious substances (e.g., linoleic acid, an essential fatty acid with phage-stimulating properties 42 , 43 ) to reinforce learning positively, and substances that make pollen unpalatable or harmful to bees (e.g., amygdalin or quinine that yield significant post-ingestional mortality in bees 17 , 44 ) to reinforce learning negatively.…”

Selective recruitment for pollen and nectar sources in honeybees

“…In the honeybee, an efficient collection of food sources, mainly protein and carbohydrates, is achieved by the division of labor among pollen and nectar foragers. The regulation of this division of labor is still not well understood, but there is evidence that pollen and nectar foragers differ in how they perceive rewards: pollen foragers are more sensitivity to gustatory (Page et al, 1995;1998;Pankiw and Page, 2000;Arenas and Farina, 2012;Nery et al, 2020) and olfactory stimuli (Scheiner et al, 2004;Latshaw and Smith, 2005) than nectar foragers. So far, whether and to what extent the type of resource advertised (i.e.…”