Felicity Muth

Colour learning when foraging for nectar and pollen: bees learn two colours at once

Bees are model organisms for the study of learning and memory, yet nearly all such research to date has used a single reward, nectar. Many bees collect both nectar (carbohydrates) and pollen (protein) on a single foraging bout, sometimes from different plant species. We tested whether individual bumblebees could learn colour associations with nectar and pollen rewards simultaneously in a foraging scenario where one floral type offered only nectar and the other only pollen. We found that bees readily learned multiple reward–colour associations, and when presented with novel floral targets generalized to colours similar to those trained for each reward type. These results expand the ecological significance of work on bee learning and raise new questions regarding the cognitive ecology of pollination.

Treating hummingbirds as feathered bees: a case of ethological cross-pollination

Hummingbirds feed from hundreds of flowers every day. The properties of these flowers provide these birds with a wealth of information about colour, space and time to guide how they forage. To understand how hummingbirds might use this information, researchers have adapted established laboratory paradigms for use in the field. In recent years, however, experimental inspiration has come less from other birds, and more from looking at other nectar-feeders, particularly honeybees and bumblebees, which have been models for foraging behaviour and cognition for over a century. In a world in which the cognitive abilities of bees regularly make the news, research on the influence of ecology and sensory systems on bee behaviour is leading to novel insights in hummingbird cognition. As methods designed to study insects in the laboratory are being applied to hummingbirds in the field, converging methods can help us identify and understand convergence in cognition, behaviour and ecology.

A novel protocol for studying bee cognition in the wild

Summary 1.Understanding how animals perceive, learn and remember stimuli is critical for understanding both how cognition is shaped by natural selection, and how ecological factors impact behaviour. However, the majority of studies on cognition involve captive animals in laboratory settings. While controlled settings are required to accurately measure aspects of cognition, they may not yield realistic estimates of learning performance in natural environments. Wild bees offer a useful system in which to study cognitive ecology as well as comparative cognition more broadly: they encompass around 20,000 species globally, varying in characteristics such as life history strategy, degree of sociality, and dietary specialization. Yet the limited number of protocols currently available for studying insect cognition has restricted research to a few commercially available bee species, in almost exclusively lab settings. 2.We present a protocol (Free-Moving Proboscis Extension Response [FMPER]) to measure wild bees’ colour preferences, learning performance, and memory. 3.We first used lab-reared bumblebees Bombus impatiens to establish that FMPER yielded results consistent with learning theory. We then successfully tested wild honeybees Apis mellifera in the lab, and Bombus vosnesenskii at field sites. 4.FMPER is straightforward to implement, low-cost, and may be readily adapted to other flower-visiting insects. We believe it will be useful to a broad range of evolutionary biologists, behavioural ecologists, and pollination ecologists interested in measuring cognitive performance in the wild and across a broader range of species. This article is protected by copyright. All rights reserved.

Learning about larceny: experience can bias bumble bees to rob nectar

How do nectar-feeding animals choose among alternative flower-handling tactics? Such decisions have consequences not only for animal fitness (via food intake) but for plant fitness as well: many animals can choose to “rob” nectar through holes chewed in the base of a flower instead of “legitimately” collecting it through the flower’s opening, thus failing to contact pollen. Although variation within a species in these nectar-foraging tactics is well documented, it is largely unknown why some individuals specialize (at least in the short term) on robbing, others on legitimate visitation, and others switch between these behaviors. We investigated whether the tendency to rob nectar through previously-made holes (secondary robbing) is influenced by prior foraging experience. In a laboratory experiment, we trained groups of bumble bees (Bombus impatiens) either to visit artificial flowers legitimately or to secondary-rob; a third group received no training. On subsequent visits to flowers, all bees had the opportunity to use either foraging tactic. We found that experience did affect bees’ tendency to secondary-rob: trained bees were more likely to adopt the tactic they had previously experienced. Untrained bees initially sampled both tactics, but over time preferred to secondary-rob. Experience also increased bees’ success at gaining nectar from flowers, but only when visiting flowers legitimately (the less preferred tactic). Overall, these findings highlight the importance of experience in animals’ choices of alternative handling tactics while foraging and help explain long-standing observations of variation in nectar-robbing behavior among individuals of the same population.Significance statementAnimals that can adopt alternative behaviors frequently use only one of them. A widespread but little understood example of this is nectar feeding, in which foragers can choose between “legitimately” collecting nectar through a flower’s opening or “robbing” nectar via holes chewed through a flower’s base. We showed in a laboratory experiment that prior foraging experience can bias bumble bees’ choices to rob nectar from pre-existing holes (i.e., to “secondary”-rob). Initial exposure to flowers that could only be robbed or only be legitimately visited increased bees’ tendency to subsequently adopt that behavior at the expense of sampling the alternative behavior, even when other bees seemed to prefer the alternative. These results help explain field observations that bees often specialize on a single nectar-collecting behavior and that there is individual variation in which behavior is adopted, contributing to our understanding of nectar robbing from the animals’ perspective.

A pollen fatty acid enhances learning and survival in bumblebees

Learning associations between food-related stimuli and nutrients allows foragers to collect resources efficiently. In turn, the nutrients that foragers consume can themselves affect learning performance, through innate preferences for pre-ingestive stimuli, as well as post-ingestive reinforcement. Bees are insect models of learning and memory, yet the vast majority of this research concerns nectar (carbohydrate) rather than pollen (protein/lipid) rewards, despite the fact that many bees collect both simultaneously. We asked how one component of pollen surface chemistry, a free fatty acid (oleic acid), affected bees’ performance in a nectar-learning task. We found that ingestion of oleic acid enhanced visual learning, likely through positive post-ingestive reinforcement. This was supported by our finding that although bees did not prefer to consume the oleic acid solution, its ingestion both decreased motor activity and increased survival. These results are a step towards understanding how nutritionally complex floral rewards may affect cognitive processes that underlie pollination mutualisms.