Motion-in-depth perception and prey capture in the praying mantis<i>Sphodromantis lineola</i>

Nityananda, Vivek; Joubier, Coline; Tan, Jerry; Tarawneh, Ghaith; Read, J.

doi:10.1242/jeb.198614

Cited by 17 publications

(21 citation statements)

References 44 publications

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“…A predatory response requires both these systems to be activated, ensuring that the mantis effectively targets attractive moving prey at the right distance. A similar 2-system account is also suggested by recent work investigating motion in depth in praying mantises (43), where the prey-detection system is sensitive to looming, while the stereo system is not. Our 2-layer model of prey detection produced strong, directional responses to all stimuli with figure motion of a target, including where this motion was purely second order.…”

Section: Discussionsupporting

confidence: 58%

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

Nityananda

O’Keeffe

Umeton

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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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.

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Section: Discussionsupporting

confidence: 58%

“…The transmittance spectra of these filters are provided in ref. 43. Tear-drop-shaped glasses were cut out of the filters with a maximum diameter of 7 cm.…”

Section: Methods Detailsmentioning

confidence: 99%

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

Nityananda

O’Keeffe

Umeton

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

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“…Among classic arthropod models for studying the neurobiology of visual avoidance behaviors are locusts (Rind et al, 2016;Dewell and Gabbiani, 2019), fruit flies (Ache et al, 2019) and crabs (Tomsic et al, 2017). In contrast, models for investigating the neural control of visually driven predatory behaviors are dragonflies (Lancer et al, 2019), praying mantis (Nityananda et al, 2019;Rosner et al, 2019) and predatory flies (Wardill et al, 2017). Except for the praying mantis (Yamawaki, 2011;Yamawaki et al, 2011), studies of visually guided escape and prey capture behaviors are performed in separate animal models.…”

Section: Introductionmentioning

confidence: 99%

Visual determinants of prey chasing behavior in a mudflat crab

Gancedo

Salido

Tomsic

2020

Journal of Experimental Biology

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The crab Neohelice inhabits mudflats where it is preyed by gulls and, conversely, preys on smaller crabs. Therefore, to the sight of moving stimuli, this crab can behave as prey or predator. The crab escape response to visual stimuli has been extensively investigated from the behavioral to the neuronal level. The predatory response (PR), however, has not yet been explored. Here, we show that this response can be reliably elicited and investigated in a laboratory arena. By using dummies of three different sizes moved on the ground at three different velocities over multiple trials, we identified important stimulation conditions that boost the occurrence of the PR and its chances of ending in successful prey capture. The PR probability was rather sustained during the first 10 trials of our experiments but then declined. The PR was elicited with high probability by the medium size dummy, less effectively by the small dummy, and hardly brought about by the large dummy, which mostly elicited avoidance responses. A GLMM analysis indicated that the dummy size and the tracking line distance were two strong determinants for eliciting the PR. The rate of successful captures, however, mainly depended on the dummy velocity. Our results suggest that crabs are capable of assessing the distance to the dummy and its absolute size. The PR characterized here, in connection with the substantial knowledge of the visual processing associated to the escape response, provides excellent opportunities for comparative analyses of the organization of two distinct visually-guided behaviors in a single animal.

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“…The stereoscopic vision of mantises has been of interest for many years (Kral & Poteser, 2009; Nityananda et al, 2019; Nityananda, Bissiana, et al, 2016; Rossel, 1980, 1983). Given the potential coevolution between depth perception and foreleg length, research aimed at sensory‐motor evolution could provide insight into the functional role of mantis foreleg length diversity.…”

Section: Discussionmentioning

confidence: 99%

“…Another component that aids the raptorial forelegs in prey capture is the evolution of the visual system, with mantises being one of the only arthropods to possess stereoscopic vision (Nityananda et al, 2016; Rossel, 1983). Research has demonstrated that mantises perceive various aspects of the photic environment including depth, and that variation in the likelihood of a feeding strike is related to aspects of the prey size, distance, contrast, and movement (Nityananda, Bissiana, Tarawneh, & Read, 2016; Nityananda, Joubier, Tan, Tarawneh, & Read, 2019; Prete, Theis, Dominguez, & Bogue, 2013). Ontogenetic analysis of body size and spatial vision in Polyspilota sp .…”

Section: Introductionmentioning

confidence: 99%

Evolutionary diversification in the raptorial forelegs of Mantodea: Relations to body size and depth perception

Oufiero

2020

Journal of Morphology

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Limb proportions have evolved among animals to meet functional demands among diverse environments. Studies from terrestrial, vertebrate locomotion have demonstrated that variation in limb proportions have adaptively evolved so animals can perform in a given environment. Most of the research on limb proportion evolution is among vertebrates and terrestrial locomotion, with little information on limb segment evolution in invertebrates or for other functional roles. For example, among invertebrates, multisegmented raptorial forelimbs have evolved multiple times independently to capture prey, but there is little information on the adaptive evolution and diversity of these limbs. Furthermore, as feeding performance is influenced by the sensory system, few studies have examined the coevolution of sensory-motor systems. Using mantises (Mantodea) I examined forelimb diversification among 97 species with a combination of methods, including ternary plots for morphospace visualization, phylogenetically informed allometric relationships, and comparison of evolutionary rates of diversification. Furthermore, using head width as a proxy for depth perception, I examined the correlated evolution of foreleg diversity with depth perception. The results show that among the three segments of the foreleg, the tibia is the smallest, most diverse, and has the highest rate of evolution after body size corrections. Furthermore, while all foreleg segments were related to head width, head width explained the most variation in tibial length compared with other foreleg segments. The results suggest a potential adaptive functional role of tibia length related to the displacement or force produced in this mechanical lever. Furthermore, results from this study support distinct ecomorphs of mantises, as several independent evolutions to grass mimicry evolve similar morphologies. Research highlightThis study demonstrates interspecific variation among segments of an invertebrate raptorial foreleg. Among Mantodea species the tibia is the most diverse and is related to a proxy for depth perception, while the other segments had strong relationships with body size. This suggests an adaptive, functional role of the tibia during prey capture. K E Y W O R D Secomorph, evolutionary morphology, praying mantis, raptorial appendage

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Motion-in-depth perception and prey capture in the praying mantisSphodromantis lineola

Cited by 17 publications

References 44 publications

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

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

Visual determinants of prey chasing behavior in a mudflat crab

Evolutionary diversification in the raptorial forelegs of Mantodea: Relations to body size and depth perception

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