The Journal of Experimental Biology © 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 2633-2642 doi:10.1242/jeb.102897 2633 ABSTRACT Insects inform themselves about the 3D structure of their surroundings through motion parallax. During flight, they often simplify this task by minimising rotational image movement. Coordinated head and body movements generate rapid shifts of gaze separated by periods of almost zero rotational movement, during which the distance of objects from the insect can be estimated through pure translational optic flow. This saccadic strategy is less appropriate for assessing the distance between objects. Bees and wasps face this problem when learning the position of their nest-hole relative to objects close to it. They acquire the necessary information during specialised flights performed on leaving the nest. Here, we show that the bumblebee’s saccadic strategy differs from other reported cases. In the fixations between saccades, a bumblebee’s head continues to turn slowly, generating rotational flow. At specific points in learning flights these imperfect fixations generate a form of ‘pivoting parallax’, which is centred on the nest and enhances the visibility of features near the nest. Bumblebees may thus utilize an alternative form of motion parallax to that delivered by the standard ‘saccade and fixate’ strategy in which residual rotational flow plays a role in assessing the distances of objects from a focal point of interest. KEY WORDS: Insect navigation, Pivoting parallax, Visual learning, Saccades, Active vision, Motion parallax INTRODUCTION Bees and wasps leaving their nest for the first time are able to relocate it on their return (Capaldi and Dyer, 1999; Tinbergen, 1932). They acquire the necessary visual information during elaborate flight manoeuvres that are known as learning flights, which these insects perform on their first few departures from the nest (Lehrer, 1993; Opfinger, 1931; Vollbehr, 1975; Wagner, 1907; Zeil, 1993a). The wasp Cerceris (Zeil, 1993b), honeybees (Cheng et al., 1987; Dittmar et al., 2011; Lehrer and Collett, 1994) and ground-nesting bees (Brünnert et al., 1994) seem to learn the distance of visual features from the nest or a feeding site through motion parallax. We have made high-speed video recordings of the head and body movements of the bumblebee, Bombus terrestris L., during phases of its learning flights when the bees are close to the nest. Analysis of the videos reveals the movement strategies through RESEARCH ARTICLE 1 Centre for Computational Neuroscience and Robotics, Department of Informatics, University of Sussex, Brighton BN1 9QJ, UK. 2 Psychology, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4QG, UK. 3 School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK. *Present address: Solomon H. Snyder Department of Neuroscience, Center for Sensory Biology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. ‡ Author for correspondence (t.s.collett@sussex.ac.uk) Received 21 January 2014; Accepted 8 May 2014 which these bees can acquire information about the distances between the nest-hole and small, nearby visual features. Bombus terrestris nests in holes in the ground and the entrance to the nest may be obscured by vegetation, so that the exact position of the nest is only known through the arrangement of nearby visual landmarks. To learn the position of the nest in relation to such cues, bumblebees spend many seconds looping close to the ground in flight manoeuvres that are centred on the position of the nest-hole and extend only tens of centimetres from it (Philippides et al., 2013). The loops (e.g. Fig. 1A) are a major structural component of bumblebee learning flights and it is likely that cues to the position of the nest are learnt during these loops (Collett et al., 2013; Philippides et al., 2013). The bees then gradually fly higher and their loops expand until they cover many metres (Osborne et al., 2013). During this expansion, bumblebees may learn the larger, more distant visual features, which can guide the bees’ return to the neighbourhood of the nest, as shown in honeybees (Becker, 1958; Capaldi and Dyer, 1999). In addition to generating body movements appropriate for acquiring visual information, many insects refine the visual feedback generated during their locomotion by moving their head, and thus eyes, relative to the body. Several insects are known to employ a ‘saccade and fixate’ strategy during flight or walking (Bender and Dickinson, 2006; Blaj and van Hateren, 2004; Boeddeker et al., 2010; Land, 1973; Ribak et al., 2009; Schilstra and van Hateren, 1998; Schilstra and van Hateren, 1999; van Hateren and Schilstra, 1999), in which high speed turns in the yaw plane (saccades) are separated by periods of low rotational speed (fixations). The coordinated head and body movements that underlie this strategy have been analysed most fully in blowflies (Schilstra and van Hateren, 1998; Schilstra and van Hateren, 1999; van Hateren and Schilstra, 1999). The angular speed of the fly’s head in space follows an almost rectangular profile with close to zero rotational speed between saccades and a high rotational speed during saccades. Minimising rotational flow in fixations both reduces blur (Land, 1997), so enhancing object detection, and may simplify the estimation of the distance of objects from the insect through translational parallax (Collett, 1978; Sobel, 1990; Wallace, 1959). Saccadic turns with coordinated head and body movements also occur during learning flights in Cerceris (Zeil et al., 2007) and in honeybees (Boeddeker et al., 2010). Insects may extract information about the position and distance of visual features relative to the insect during these fixations, when retinal image motion is mostly a consequence of the insect’s translation. Translational parallax gives information about distance relative to the observer – the faster the image of a feature moves, the closer the feature is. If an insect monitors distance through translational parallax, it can best assess the distances of objects from the nest by acquiring parallax information at the nest entrance. An alternative form of motion parallax termed ‘pivoting parallax’ (Voss and Zeil, 1998) can give information about the distance between the nest and Head movements and the optic flow generated during the learning flights of bumblebees Olena Riabinina 1, *, Natalie Hempel de Ibarra 2 , Andrew Philippides 1 and Thomas S. Collett 3,‡