Odour Learning Bees Have Longer Foraging Careers Than Non-learners in a Natural Environment

Lisa J. Evans,Nigel E. Raine,Karen E. Smith

doi:10.3389/fevo.2021.676289

Abstract

Individual animals allowed the opportunity to learn generally outperform those prevented from learning, yet, within a species the capacity for learning varies markedly. The evolutionary processes that maintain this variation in learning ability are not yet well understood. Several studies demonstrate links between fitness traits and visual learning, but the selection pressures operating on cognitive traits are likely influenced by multiple sensory modalities. In addition to vision, most animals will use a combination of hearing, olfaction (smell), gustation (taste), and touch to gain information about their environment. Some animals demonstrate individual preference for, or enhanced learning performance using certain senses in relation to particular aspects of their behaviour (e.g., foraging), whereas conspecific individuals may show different preferences. By assessing fitness traits in relation to different sensory modalities we will strengthen our understanding of factors driving observed variation in learning ability. We assessed the relationship between the olfactory learning ability of bumble bees (Bombus terrestris) and their foraging performance in their natural environment. We found that bees which failed to learn this odour-reward association had shorter foraging careers; foraging for fewer days and thus provisioning their colonies with fewer resources. This was not due to a reduced propensity to forage, but may have been due to a reduced ability to return to their colony. When comparing among only individuals that did learn, we found that the rate at which floral resources were collected was similar, regardless of how they performed in the olfactory learning task. Our results demonstrate that an ability to learn olfactory cues can have a positive impact of the foraging performance of B. terrestris in a natural environment, but echo findings of earlier studies on visual learning, which suggest that enhanced learning is not necessarily beneficial for bee foragers provisioning their colony.

Highlights

An animal’s capacity for learning can influence essentially every aspect of its behaviour, including its ability to find food, attract mates, and avoid predators (Nowicki et al, 2002; Lönnstedt et al, 2012; Sergio et al, 2014)
The number of foraging bouts for which pollen/nectar collection was observed per bee ranged between 2 and 22, and was directly proportional to the total number of foraging bouts undertaken by each bee (Spearman’s ρ = 0.73, n = 33, p < 0.001)
To determine whether the olfactory learning abilities of B. terrestris individuals predict their foraging performance in a natural environment, proboscis extension response (PER) conditioning was used to assess olfactory learning in the laboratory before the foraging performance of the same individuals was monitored in the field

Summary

Introduction

An animal’s capacity for learning can influence essentially every aspect of its behaviour, including its ability to find food, attract mates, and avoid predators (Nowicki et al, 2002; Lönnstedt et al, 2012; Sergio et al, 2014). Learning enables individuals to respond to environmental change within their lifetime (Greenlees et al, 2010; Ward-Fear et al, 2016). Despite these apparent advantages of learning, considerable variation in learning capacity can often be observed among individuals within the same species (e.g., Chittka et al, 2003; Raine et al, 2006b; van den Berg et al, 2011; White and Brown, 2014). While it is clear that these trade-offs can affect the learning abilities of individuals, the evolutionary processes that maintain this variation in learning ability within natural populations are not yet well understood (Raine et al, 2006a; Morand-Ferron and Quinn, 2015; Morand-Ferron, 2017; Boogert et al, 2018)

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