Stereopsis - 3D vision – has become widely used as a model of perception. However, all our knowledge of possible underlying mechanisms comes almost exclusively from vertebrates. While stereopsis has been demonstrated for one invertebrate, the praying mantis, a lack of techniques to probe invertebrate stereopsis has prevented any further progress for three decades. We therefore developed a stereoscopic display system for insects, using miniature 3D glasses to present separate images to each eye, and tested our ability to deliver stereoscopic illusions to praying mantises. We find that while filtering by circular polarization failed due to excessive crosstalk, “anaglyph” filtering by spectral content clearly succeeded in giving the mantis the illusion of 3D depth. We thus definitively demonstrate stereopsis in mantises and also demonstrate that the anaglyph technique can be effectively used to deliver virtual 3D stimuli to insects. This method opens up broad avenues of research into the parallel evolution of stereoscopic computations and possible new algorithms for depth perception.

Stereo or ‘3D’ vision is an important but costly process seen in several evolutionarily distinct lineages including primates, birds and insects. Many selective advantages could have led to the evolution of stereo vision, including range finding, camouflage breaking and estimation of object size. In this paper, we investigate the possibility that stereo vision enables praying mantises to estimate the size of prey by using a combination of disparity cues and angular size cues. We used a recently developed insect 3D cinema paradigm to present mantises with virtual prey having differing disparity and angular size cues. We predicted that if they were able to use these cues to gauge the absolute size of objects, we should see evidence for size constancy where they would strike preferentially at prey of a particular physical size, across a range of simulated distances. We found that mantises struck most often when disparity cues implied a prey distance of 2.5 cm; increasing the implied distance caused a significant reduction in the number of strikes. We, however, found no evidence for size constancy. There was a significant interaction effect of the simulated distance and angular size on the number of strikes made by the mantis but this was not in the direction predicted by size constancy. This indicates that mantises do not use their stereo vision to estimate object size. We conclude that other selective advantages, not size constancy, have driven the evolution of stereo vision in the praying mantis.This article is part of the themed issue ‘Vision in our three-dimensional world’.

Stereopsis is the computation of depth information from views acquired simultaneously from different points in space. For many years, stereopsis was thought to be confined to primates and other mammals with front-facing eyes. However, stereopsis has now been demonstrated in many other animals, including lateral-eyed prey mammals, birds, amphibians and invertebrates. The diversity of animals known to have stereo vision allows us to begin to investigate ideas about its evolution and the underlying selective pressures in different animals. It also further prompts the question of whether all animals have evolved essentially the same algorithms to implement stereopsis. If so, this must be the best way to do stereo vision, and should be implemented by engineers in machine stereopsis. Conversely, if animals have evolved a range of stereo algorithms in response to different pressures, that could inspire novel forms of machine stereopsis appropriate for distinct environments, tasks or constraints. As a first step towards addressing these ideas, we here review our current knowledge of stereo vision in animals, with a view towards outlining common principles about the evolution, function and mechanisms of stereo vision across the animal kingdom. We conclude by outlining avenues for future work, including research into possible new mechanisms of stereo vision, with implications for machine vision and the role of stereopsis in the evolution of camouflage.

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.

The detection of visual motion and its direction is a fundamental task faced by several visual systems. The motion detection system of insects has been widely studied with the majority of studies focussing on flies and bees. Here we characterize the contrast sensitivity of motion detection in the praying mantis Sphodromantis lineola, an ambush predator that stays stationary for long periods of time while preying on fast-moving prey. In this, its visual behaviour differs from previously studied insects and we might therefore expect its motion detection system to differ from theirs. To investigate the sensitivity of the mantis we analyzed its optomotor response in response to drifting gratings with different contrasts and spatio-temporal frequencies. We find that the contrast sensitivity of the mantis depends on the spatial and temporal frequencies present in the stimulus and is separably tuned to spatial and temporal frequency rather than specifically to object velocity. Our results also suggest that mantises are sensitive to a broad range of velocities, in which they differ from bees and are more similar to hoverflies. We discuss our results in relation to the contrast sensitivities of other insects and the visual ecology of the mantis.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-015-1008-5) contains supplementary material, which is available to authorized users.

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Vocal communication in crowded social environments is a difficult problem for both humans and nonhuman animals. Yet many important social behaviors require listeners to detect, recognize, and discriminate among signals in a complex acoustic milieu comprising the overlapping signals of multiple individuals, often of multiple species. Humans exploit a relatively small number of acoustic cues to segregate overlapping voices (as well as other mixtures of concurrent sounds, like polyphonic music). By comparison, we know little about how nonhuman animals are adapted to solve similar communication problems. One important cue enabling source segregation in human speech communication is that of frequency separation between concurrent voices: differences in frequency promote perceptual segregation of overlapping voices into separate “auditory streams” that can be followed through time. In this study, we show that frequency separation (ΔF) also enables frogs to segregate concurrent vocalizations, such as those routinely encountered in mixed-species breeding choruses. We presented female gray treefrogs (Hyla chrysoscelis) with a pulsed target signal (simulating an attractive conspecific call) in the presence of a continuous stream of distractor pulses (simulating an overlapping, unattractive heterospecific call). When the ΔF between target and distractor was small (e.g., ≤3 semitones), females exhibited low levels of responsiveness, indicating a failure to recognize the target as an attractive signal when the distractor had a similar frequency. Subjects became increasingly more responsive to the target, as indicated by shorter latencies for phonotaxis, as the ΔF between target and distractor increased (e.g., ΔF = 6–12 semitones). These results support the conclusion that gray treefrogs, like humans, can exploit frequency separation as a perceptual cue to segregate concurrent voices in noisy social environments. The ability of these frogs to segregate concurrent voices based on frequency separation may involve ancient hearing mechanisms for source segregation shared with humans and other vertebrates.

Attention is fundamentally important for sensory systems to focus on behaviourally relevant stimuli. It has therefore been an important field of study in human psychology and neuroscience. Primates, however, are not the only animals that might benefit from attention-like processes. Other animals, including insects, also have to use their senses and select one among many stimuli to forage, avoid predators and find mates. They have evolved different mechanisms to reduce the information processed by their brains to focus on only relevant stimuli. What are the mechanisms used by insects to selectively attend to visual and auditory stimuli? Do these attention-like mechanisms achieve the same functions as they do in primates? To investigate these questions, I use an established framework for investigating attention in non-human animals that proposes four fundamental components of attention: salience filters, competitive selection, top-down sensitivity control and working memory. I discuss evidence for each of these component processes in insects and compare the characteristics of these processes in insects to what we know from primates. Finally, I highlight important outstanding questions about insect attention that need to be addressed for us to understand the differences and similarities between vertebrate and insect attention.