Honeybees can recognise images of complex natural scenes for use as potential landmarks

Abstract

SUMMARYThe ability to navigate long distances to find rewarding flowers and return home is a key factor in the survival of honeybees (Apis mellifera). To reliably perform this task, bees combine both odometric and landmark cues, which potentially creates a dilemma since environments rich in odometric cues might be poor in salient landmark cues, and vice versa. In the present study, honeybees were provided with differential conditioning to images of complex natural scenes, in order to determine if they could reliably learn to discriminate between very similar scenes, and to recognise a learnt scene from a novel distractor scene. Choices made by individual bees were modelled with signal detection theory, and bees demonstrated an ability to discriminate between perceptually similar target and distractor views despite similar spatiotemporal content of the images. In a non-rewarded transfer test bees were also able to recognise target stimuli from novel distractors. These findings indicate that visual processing in bees is sufficiently accurate for recognising views of complex scenery as potential landmarks, which would enable bees flying in a forest to use trees both as landmark and/or odometric cues.

Flowers help bees cope with uncertainty: signal detection and the function of floral complexity

“…Signal detection theory (Green and Swets, 1966) provides a framework for understanding decision making in situations where perceptual or environmental noise makes discrimination between two signals difficult (Dyer et al, 2008;Wiley, 2006). For example, Fig.1 illustrates a hypothetical signal detection problem faced by bees: flower types that differ in reward value on average differ along some perceptual dimension (such as color), but individual flowers vary in their traits.…”

Conceptual learning by miniature brains

“…Using this protocol, it has been shown that bees are capable of higher-order forms of visual learning [12,14,21]: they categorize both artificial patterns [31][32][33][34][35] and pictures of natural scenes [36] (see reference [37] for a review), they navigate complex mazes [38,39], exhibit top-down modulation of their visual perception [40], or use spatial configuration to recognize complex pictures [31,[41][42][43].…”

Seeing near and seeing far; behavioural evidence for dual mechanisms of pattern vision in the honeybee (Apis mellifera)

“…For example, a foraging honeybee may leave a hive and (i) fly several hundred metres through a treed landscape using odometric and landscape cues to judge the distance to a patch containing rewarding flowers (Dyer et al, 2008a;Srinivasan et al, 2000;Vladusich et al, 2005), (ii) at the flower patch detect potential target flowers at a distance and recognise rewarding flowers at 'close' range against background noise using spatial (Dafni et al, 1997), achromatic (Hempel de Ibarra and Vorobyev, 2009) and colour cues (Chittka and Wells, 2004;Dyer et al, 2008b;Giurfa et al, 1996;Hempel de Ibarra and Vorobyev, 2009), and (iii) finally, fly back to the hive and recognise the precise location using a variety of orientation and landmark cues (Dyer et al, 2008a;Srinivasan, 2011;Vladusich et al, 2005). These different tasks are likely to place very different demands upon a visual system.…”

“…For example, the capacity for humans to read (Ahissar et al, 2009), recognise faces (Collishaw and Hole, 2000;Maurer et al, 2002) or even identify fingerprints (Busey and Vanderkolk, 2005) and abstract 'Greeble' figures (Gauthier and Tarr, 1997) is dependent upon the level of experience with a particular class of stimuli. Whilst it has been assumed that comparatively simple insect brains only allow for vision that is mediated by 'hard-wired' physiological mechanisms (Backhaus et al, 1987;Horridge, 2000;Horridge, 2009a;Horridge, 2009b), several recent studies have shown that what a honeybee perceives is very dependent upon the type of visual experience that an individual animal receives (Avarguès-Weber et al, 2011;Dyer et al, 2008a;Giurfa et al, 1999;Stach et al, 2004;Stach and Giurfa, 2005), and comparative studies of cognitive capacity are of high value . For example, considering pattern vision, the level of discrimination by an individual animal is very dependent upon whether a target stimulus is learned in isolation, which is termed absolute conditioning, or whether a target stimulus is learned in relation to a perceptually similar distractor, which is termed differential conditioning (Giurfa et al, 1999).…”

“…Fine levels of discrimination capability for honeybee vision following differential conditioning (Avarguès-Weber et al, 2010b;Dyer et al, 2008a;Dyer and Vuong, 2008; are not consistent with other studies, which reveal that, in many cases, honeybee spatial vision is simple and based on lowlevel feature detectors that combine to create elemental cues (Horridge, 1996;Horridge, 2000;Horridge, 2003a;Horridge, 2003b;Horridge, 2009a;Horridge, 2009b), and the coincidence of these elemental cues are remembered as a retinotopic label for a target image such that bees generalise between stimuli containing similar cues (Horridge, 2009a). For example, when training honeybees in a Y-maze apparatus to a 4-bar asymmetric target and distractor pair, it has been claimed that honeybees can learn to discriminate these stimuli if presented at a large visual angle of 100deg but bees fail to learn this discrimination task if the stimuli are presented at a relatively small visual angle of 50deg (Horridge, 2009a;Horridge, 2009b;Horridge, 1996).…”