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

Abstract

Several examples of insects using visual motion to measure distance have been documented, from locusts peering to gauge the proximity of prey, to honeybees performing visual odometry en route between the hive and a flower patch. However, whether the use of parallax information is confined to specialised behaviours like these or represents a more general purpose sensory capability, is an open question. We investigate this issue in the foraging swallowtail butterfly Papilio xuthus, which we trained to associate a target presented on a monitor with a food reward. We then tracked the animal's flight in realtime, allowing us to manipulate the size and/or position of the target in a closed-loop manner to create the illusion that it is situated either above or below the monitor surface. Butterflies are less attracted to (i.e. slower to approach) targets that appear, based on motion parallax, to be more distant. Furthermore, we found that the number of abortive descent manoeuvres performed prior to the first successful target approach varies according to the depth of the virtual target, with expansion and parallax cues having effects of opposing polarity. However, we found no evidence that Papilio modulate the kinematic parameters of their descents according to the apparent distance of the target. Thus, we argue that motion parallax is used to identify a proximal target object, but that the subsequent process of approaching it is based on stabilising its edge in the 2D space of the retina, without estimating its distance.

The Dominant Role of Visual Motion Cues in Bumblebee Flight Control Revealed Through Virtual Reality

“…Even when the bees could unrealistically see the target through the obstacles (as though they possessed “X-ray vision”), they nevertheless avoided them. Our results confirm previous findings that motion cues are innate and dominant in the insect's flight control mechanisms (locusts and mantis: e.g., Kral and Poteser, 1997 ; honeybees: e.g., Srinivasan et al, 1989 ; fruit flies, e.g., Fry et al, 2009 ; van Breugel and Dickinson, 2012 ; butterflies: Stewart et al, 2015 ).…”

“…The real-time tracking procedure was similar to that described in Stewart et al ( 2015 ), controlled by a custom-written Java program utilizing the ImageJ API. Prior to running experiments, the projection matrices of the two tracking cameras were calculated by manually identifying the positions of the arena vertices in the camera image, and then performing a least-squares fit.…”

“…In this way, we created virtual objects that appeared to be situated in 3D space outside the monitor surface. Similar approaches have been previously used to study visually-guided behavior in other insects such as locusts (Wallace, 1959 ), fruit flies (Schuster et al, 2002 ), and butterflies (Stewart et al, 2015 ), as well as rodents and fish (Stowers et al, 2017 ). This study is (to our knowledge) the first to employ VR techniques to investigate bees, animals noted within the neuroethology community for their agile flight and impressive capacity for “cognitive” tasks such as learning and navigation.…”

Dynamic Corridor Illusion in Pigeons: Humanlike Pictorial Cue Precedence Over Motion Parallax Cue in Size Perception

“…Therefore, pigeons might use motion parallax cues for something other than size constancy. Some animals use motion parallax cues for bodily motor control (Stewart et al., 2015; Wallace, 1959; for review, see Kral, 2003). Given that pigeon’s pretectal neurons in the accessory optic system, which processes visual motion caused by self-motion, are sensitive to the visual depth defined by motion parallax (Xiao & Frost, 2013), pigeons might use motion parallax for visuomotor control during flying and landing.…”

Multisensory integration in Lepidoptera: Insights into flower‐visitor interactions

“…Lepidoptera innately prefer brighter targets , and have difficulty learning to visit darker targets. Edge detection based on intensity contrast plays an important role in landing behaviour in P. xuthus . Interestingly, swallowtail butterflies ( P. xuthus and P. aegeus ) respond to light polarisation, apparently perceiving it as false brightness and colour in foraging and oviposition contexts, respectively .…”