Second-order cues to figure motion enable object detection during prey capture by praying mantises.

Detecting motion is essential for animals to perform a wide variety of functions. In order to do so, animals could exploit motion cues, including both first-order cues-such as luminance correlation over time-and second-order cues, by correlating higher-order visual statistics. Since first-order motion cues are typically sufficient for motion detection, it is unclear why sensitivity to second-order motion has evolved in animals, including insects. Here, we investigate the role of second-order motion in prey capture by praying mantises. We show that prey detection uses second-order motion cues to detect figure motion. We further present a model of prey detection based on second-order motion sensitivity, resulting from a layer of position detectors feeding into a second layer of elementary-motion detectors. Mantis stereopsis, in contrast, does not require figure motion and is explained by a simpler model that uses only the first layer in both eyes. Second-order motion cues thus enable prey motion to be detected, even when perfectly matching the average background luminance and independent of the elementary motion of any parts of the prey. Subsequent to prey detection, processes such as stereopsis could work to determine the distance to the prey. We thus demonstrate how second-order motion mechanisms enable ecologically relevant behavior such as detecting camouflaged targets for other visual functions including stereopsis and target tracking.

Pattern and Speed Interact to Hide Moving Prey.

Evolutionary biologists have long been fascinated by camouflage patterns that help animals reduce their chances of being detected by predators [1-4]. However, patterns that hide prey when they remain stationary, such as those that match their backgrounds [5, 6], are rendered ineffective once prey are moving [7-10]. The question remains: can a moving animal ever be patterned in a way that helps reduce detection by predators? One long-standing idea is that high-contrast patterns with repeated elements, such as stripes, which are highly visible when prey are stationary, can actually conceal prey when they move fast enough [11-14]. This is predicted by the "flicker fusion effect," which occurs when prey move with sufficient speed that their pattern appears to blur, making them appear more featureless and become less conspicuous against the background [2, 8]. However, although this idea suggests a way to camouflage moving prey, it has not been empirically tested, and it is not clear that it would work at speeds that are biologically relevant to a predator [13]. Combining psychophysics and behavioral approaches, we show that speed and pattern interact to determine the detectability of prey to the praying mantis (Sphodromantis lineola) and, crucially, that prey with high-contrast stripes become less visible than prey with background-matching patterns when moving with sufficient speed. We show that stripes can reduce the detection of moving prey by exploiting the spatiotemporal limitations of predator perception, and that the camouflaging effect of a pattern depends upon the speed of prey movement.

A Novel Form of Stereo Vision in the Praying Mantis.

Stereopsis is the ability to estimate distance based on the different views seen in the two eyes [1-5]. It is an important model perceptual system in neuroscience and a major area of machine vision. Mammalian, avian, and almost all machine stereo algorithms look for similarities between the luminance-defined images in the two eyes, using a series of computations to produce a map showing how depth varies across the scene [3, 4, 6-14]. Stereopsis has also evolved in at least one invertebrate, the praying mantis [15-17]. Mantis stereopsis is presumed to be simpler than vertebrates' [15, 18], but little is currently known about the underlying computations. Here, we show that mantis stereopsis uses a fundamentally different computational algorithm from vertebrate stereopsis-rather than comparing luminance in the two eyes' images directly, mantis stereopsis looks for regions of the images where luminance is changing. Thus, while there is no evidence that mantis stereopsis works at all with static images, it successfully reveals the distance to a moving target even in complex visual scenes with targets that are perfectly camouflaged against the background in terms of texture. Strikingly, these insects outperform human observers at judging stereoscopic distance when the pattern of luminance in the two eyes does not match. Insect stereopsis has thus evolved to be computationally efficient while being robust to poor image resolution and to discrepancies in the pattern of luminance between the two eyes. VIDEO ABSTRACT.

Unravelling the illusion of flicker fusion.

For over 150 years, researchers have investigated the anti-predator function of animal patterns. However, this work has mainly focused on when prey remain still, and has only recently started to incorporate motion into the study of defensive coloration. As motion breaks camouflage, a new challenge is to understand how prey avoid predators while moving around their environment, and if a moving prey can ever be camouflaged. We propose that there is a solution to this, in that a 'flicker fusion effect' can change the appearance of the prey in the eyes of their predators to reduce the chances of initial detection. This effect occurs when a high contrast pattern blurs at speed, changing the appearance of the prey, which may help them better match their background. Despite being widely discussed in the literature, the flicker fusion effect is poorly described, there is no clear theoretical framework for testing how it might reduce predation, and the terminology describing it is, at best, rather confusing. Our review addresses these three key issues to enable researchers to formulate precise predictions about when the flicker fusion effect occurs, and to test how it can reduce predation.