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.

Keywords: compound eye; eye movement; saccade; stomatopod; vision.

Figure 1.

(a–c) Camera-angle view of stomatopod Odontodactylus scyllarus, in restraining tube, showing different eye positions. Arrows (red in online colour version) point approximately in the direction that the acute zone is looking in. Black areas on the eyes are pseudo-pupils and show occasional trinocular view of the eye as well as the greatly expanded acute zone pseudo-pupils when this area of the eye is directly facing the camera [10,11]. In this position, the dot (red in online colour version) in the centre of the middle pseudopupil is an end-on view of the direction indicator arrow. (d) O. scyllarus walking out of burrow (Photographs, R. L. Caldwell). (e) Eye of Lysiosquilla maculata. (f) Eye of Gonodactylus chiragra. (g) Eye of Pseudosquilla ciliata. (e–g) Show different eye shapes, (f) and (g) are rotated 90° anticlockwise relative to their normal attitude in life. (Online version in colour.)

Figure 2.

Diagram of experimental set-up. (a) Square aquarium with restrained stomatopod looking out of Perspex tube towards stimulus presentation screen. Central black circle is the hole through which camera can videotape from outside the aquarium. Small circle, on the mid-line to the left of the camera hole (red in online version), stimulus presented at 38° from the standardized stomatopod position. Small black dots, not visible to the stomatopod, mark positions of other stimulus presentation points. (b) Top-down diagrammatic view of the stimulus presentation screen showing overlapping white Perspex screens and red stimulus sticker on an arm attached to pulley-wheel, allowing stimulus to be suddenly presented at various positions in front of the stomatopod. (Online version in colour.)

Figure 3.

Example acquisitional saccades in (a) Pseudosquilla ciliata and (b) Odontodactylus scyllarus. In each graph, the y-axis has been removed but is the same as the x-axis, and each includes a representation of the positions of the stimulus screen (vertical lines at the edge of each panel and large grey circle showing position of hole for filming through) and stimulus presentation position (grey circle (red in online version) within circle) drawn in (see also figure 1). Individual data points are angular positions of the acute-zone direction, frame by frame (frame intervals 20 ms), for the right eye (filled circles) and left eye (empty circles) for seven frames during the saccade. First and last frame only are numbered on the graph for clarity and left eye numbers are italicized. Grey circles around stimulus positions show known experimental error in eye position recording using computer models [9]. (Online version in colour.)

Figure 4.

Analyses of eye movements in Pseudosquilla ciliata (right) and Odontodactylus scyllarus (left). (a) Several seconds of continuous eye movement showing both rapid saccadic movements (black bars) and scanning eye movements of around 100° s⁻¹ or less (white bars) [9]. P. ciliata exhibits a wider saccade speed range than O. scyllarus. (b) Data from individually induced saccades using sudden stimulus introduction apparatus (figure 1) showing correlation between angular distance of eye movement and angular velocity. (c) Saccadic accuracy plotted as error angle taken at the final frame of the rapid movement (e.g. as in figure 3) relative to actual stimulus position. Both species show high degree of error, averaging around 10°, not correlated with distance to target from previous direction of acute-zone gaze.