Shrimps that pay attention: saccadic eye movements in stomatopod crustaceans

Abstract

Discovering that a shrimp can flick its eyes over to a fish and follow up by tracking it or flicking back to observe something else implies a 'primate-like' awareness of the immediate environment that we do not normally associate with crustaceans. For several reasons, stomatopods (mantis shrimp) do not fit the general mould of their subphylum, and here we add saccadic, acquisitional eye movements to their repertoire of unusual visual capabilities. Optically, their apposition compound eyes contain an area of heightened acuity, in some ways similar to the fovea of vertebrate eyes. Using rapid eye movements of up to several hundred degrees per second, objects of interest are placed under the scrutiny of this area. While other arthropod species, including insects and spiders, are known to possess and use acute zones in similar saccadic gaze relocations, stomatopods are the only crustacean known with such abilities. Differences among species exist, generally reflecting both the eye size and lifestyle of the animal, with the larger-eyed more sedentary species producing slower saccades than the smaller-eyed, more active species. Possessing the ability to rapidly look at and assess objects is ecologically important for mantis shrimps, as their lifestyle is, by any standards, fast, furious and deadly.

Null point of discrimination in crustacean polarisation vision

“…Rather than a locomotion-based behavioural change, the animals responded by making saccadic gaze shifts with one or both eyestalks towards the looming stimuli. These could be distinguished from the majority of general eye movements by their high speed and directionalitymovements that are commonly observed in target tracking stomatopods (Cronin et al, 1988;Marshall et al, 2014a). Secondly, there was no statistical difference in the stomatopods' response probability between the two stimulus types (0 and −45 deg) (ANCOVA,F=0.208,P=0.66; Fig.…”

“…There are several proposed explanations for the extreme mobility of stomatopod eyes, including their use for target acquisition and tracking, and for scan movements associated with the colour and polarisation sensitivity in the mid-band region (Cronin et al, 1988;Land et al, 1990;Thoen et al, 2014;Marshall et al, 2014a). Such movements have strong implications for their polarisation vision system, which, as a result, does not appear to suffer from the null points experienced by stabilised twochannel receptor arrangements.…”

Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems

“…In the case of eyestalks these are signaled by eyestalk statocysts and leg proprioceptors, thereby maintaining constant orientation of the eyes to the visual horizon (Scapini et al, 1978). Stalked eyes can also track visual stimuli (Neil et al, 1983), and in stomatopod crustaceans stalked eyes scan potential prey by saccadic movements, thus enabling active (acquisitive) vision (Marshall et al, 2014). These actions are comparable to visually driven leg movements during prey tracking in mantispid Neuroptera (Kral et al, 2000).…”

Neural organization of afferent pathways from the stomatopod compound eye

“…Another unusual feature of the stomatopod eye is that subsets of photoreceptors from upper and lower eye halves and the midband sample the same zone in space, that is each eye has trinocular vision, the result of considerable skew in the optic axis of ommatidia within the eye (Manning, Schiff, & Abbott, ; Marshall & Land, ). This, coupled with the fact that each eye moves independently using scanning eye movements (Land, Marshall, Brownless, & Cronin, ; Marshall, Land, & Cronin, ), likely allows the midband receptors to simultaneously sample visual information regarding color and circular polarization, which is then presumably combined with achromatic and linearly polarized information from upper and lower eye halves to assemble a reconstruction of the visual scene that has within it 20 channels of information (12 color, 6 polarization directions, intensity, and stereopsis). How and where this information is integrated in the optic lobes is not yet known.…”