Feed-forward and visual feed-back control of head roll orientation in wasps (Polistes humilis, Vespidae, Hymenoptera)

Abstract

SUMMARYFlying insects keep their visual system horizontally aligned, suggesting that gaze stabilization is a crucial first step in flight control. Unlike flies, hymenopteran insects such as bees and wasps do not have halteres that provide fast, feed-forward angular rate information to stabilize head orientation in the presence of body rotations. We tested whether hymenopteran insects use inertial (mechanosensory) information to control head orientation from other sources, such as the wings, by applying periodic roll perturbations to male Polistes humilis wasps flying in tether under different visual conditions indoors and in natural outdoor conditions. We oscillated the thorax of the insects with frequency-modulated sinusoids (chirps) with frequencies increasing from 0.2 to 2Hz at a maximal amplitude of 50deg peak-to-peak and maximal angular velocity of ±245degs -1 . We found that head roll stabilization is best outdoors, but completely absent in uniform visual conditions and in darkness.Step responses confirm that compensatory head roll movements are purely visually driven. Modelling step responses indicates that head roll stabilization is achieved by merging information on head angular velocity, presumably provided by motion-sensitive neurons and information on head orientation, presumably provided by light level integration across the compound eyes and/or ocelli (dorsal light response). Body roll in free flight reaches amplitudes of ±40deg and angular velocities greater than 1000degs -1 , while head orientation remains horizontal for most of the time to within ±10deg. In free flight, we did not find a delay between spontaneous body roll and compensatory head movements, and suggest that this is evidence for the contribution of a feed-forward control to head stabilization. Supplementary material available online at

Head roll stabilisation in the nocturnal bull ant Myrmecia pyriformis: Implications for visual navigation

“…We note in this context that to the best of our knowledge, there are no studies characterising the optomotor control systems in ants. The observation that delays are longer in response to the horizon pattern compared with the striped pattern has also been described for head roll compensation in wasps (Viollet and Zeil, 2013), and is most probably due to differences in pattern size (Warzecha and Egelhaaf, 2000). With regard to the low gain of the visual control loop, it is important to note that the ants in our optomotor experiments were not walking.…”

“…Viollet and Zeil, 2013;Goulard et al, 2015): firstly, we did not detect delays at least at a temporal resolution of 8 ms (Fig. 4C,D); secondly, ants are able to compensate to some degree even in total darkness (Fig.…”

“…Goulard et al, 2015) or an efference copy (e.g. Viollet and Zeil, 2013), that mediate this response.…”

“…Flying insects are able to keep the roll and pitch orientation of the head constant despite large, but predictable, changes of orientation of the thorax associated with flight control (Beatus et al, 2015;Boeddeker et al, 2010;Goulard et al, 2015;Land, 1973;Schilstra and van Hateren, 1998;Viollet and Zeil, 2013). Walking insects, however, face not only the predictable stride-cycle-dependent body oscillations but also unpredictable ground topography-dependent body rotations Egelhaaf, 2012, 2014).…”

A quadriocellar scoliid wasp (Hymenoptera, Scoliidae) from Mallorca, with a brief account of supernumerary ocelli in insects

“…This suggests that for some cases there might be a genetic component, although the general rarity of supernumerary ocelli in other groups tends to suggest that such apparent heritability is far from the norm. What is remarkable is that these aberrant individuals are often captured while carrying on otherwise seemingly normal lives, a particularly remarkable fact given that ocelli are implicated in light responses and orientation (e.g., Taylor 1981a, 1981b, Schuppe and Hengstenberg 1993, Warrant 2006, Berry et al 2006, Viollet and Zeil 2013. The scoliid wasp reported herein was perfectly developed in all other respects, and it does not seem that it had to deal with negative effects caused by the supernumerary ocellus.…”