Head movements and the optic flow generated during the learning flights of bumblebees

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.

Species-specific differences in the fine structure of learning walk elements inCataglyphisants

“…Learning flights of flying hymenoptera include repeated arcs, loops and turn-backs (honeybees : Becker, 1958;Capaldi and Dyer, 1999;Capaldi et al, 2000;Degen et al, 2015Degen et al, , 2016Lehrer, 1991Lehrer, , 1993Opfinger, 1931;Vollbehr, 1975;wasps: Peckham and Peckham, 1898;Stürzl et al, 2016;Tinbergen, 1932;Zeil, 1993a,b;Zeil et al, 1996;bumblebees: Collett et al, 2013;Hempel de Ibarra et al, 2009;Philippides et al, 2013;Riabinina et al, 2014;Robert et al, 2017;Wagner, 1907). Dung beetles perform rotations about their vertical axis before rolling a ball away from the dung pile (Baird et al, 2012), during which they take a snapshot of the celestial scenery (el Jundi et al, 2016).…”

“…the location of their nest. Since the first descriptions over a century ago (Peckham and Peckham, 1898;Wagner, 1907), learning flights have been investigated in great detail in wasps (Tinbergen, 1932;Zeil, 1993a,b;Zeil et al, 1996), honeybees (Becker, 1958;Capaldi and Dyer, 1999;Lehrer, 1991Lehrer, , 1993Opfinger, 1931;Vollbehr, 1975) and bumblebees Hempel de Ibarra et al, 2009;Philippides et al, 2013;Robert et al, 2017) using increasingly sophisticated techniques like harmonic radar (Capaldi et al, 2000;Degen et al, 2015Degen et al, , 2016Osborne et al, 2013) or high-speed cameras (Riabinina et al, 2014;Stürzl et al, 2016). Much less is known about learning walks of ants (Fleischmann et al, 2016;Jayatilaka, 2014;Müller and Wehner, 2010;Muser et al, 2005;Nicholson et al, 1999;Stieb et al, 2012;Wehner et al, 2004).…”

Gap perception in bumblebees

“…Here we sought to uncover the mechanisms implemented by flying insects in gap identification and perception. Bumblebees are excellent model organisms because much is known about their flight and navigational performance (Baird and Dacke, 2012; Crall et al, 2014; Mirwan and Kevan, 2013; Osborne et al, 2008; Ravi et al, 2013; Riabinina et al, 2014; Lobecke et al 2018). We presented unsuspecting bumblebees with an altered environment consisting of a wall obstructing their flight path but containing a gap that prevented direct passage to their goal and observed their behavior as they approached and traversed the gap.…”

The roles of visual parallax and edge attraction in the foraging behaviour of the butterfly Papilio xuthus

“…There is evidence that bees engage in 'active vision', structuring their flight to optimally extract motion parallax information. Flying honeybees perform lateral 'peering' manoeuvres whilst stabilising their gaze when approaching a feeder (Boeddeker and Hemmi, 2010) and, similarly, bumblebees move in such a way as to maximise 'pivoting parallax' when performing learning flights around the nest (Riabinina et al, 2014).…”