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. 2021 Jun 1;224(11):jeb236653.
doi: 10.1242/jeb.236653. Epub 2021 Jun 8.

Run and hide: visual performance in a brittle star

Lauren Sumner-Rooney  1 , John D Kirwan  2 , Carsten Lüter  3 , Esther Ullrich-Lüter  3
Affiliations

Run and hide: visual performance in a brittle star

Lauren Sumner-Rooney et al. J Exp Biol. .

Abstract

Spatial vision was recently reported in a brittle star, Ophiomastix wendtii, which lacks discrete eyes, but little is known about its visual ecology. Our aim was to better characterize the vision and visual ecology of this unusual visual system. We tested animal orientation relative to vertical bar stimuli at a range of angular widths and contrasts, to identify limits of angular and contrast detection. We also presented dynamic shadow stimuli, either looming towards or passing the animal overhead, to test for potential defensive responses. Finally, we presented animals lacking a single arm with a vertical bar stimulus known to elicit a response in intact animals. We found that O. wendtii orients to large (≥50 deg), high-contrast vertical bar stimuli, consistent with a shelter-seeking role and with photoreceptor acceptance angles estimated from morphology. We calculate poor optical sensitivity for individual photoreceptors, and predict dramatic oversampling for photoreceptor arrays. We also report responses to dark stimuli moving against a bright background - this is the first report of responses to moving stimuli in brittle stars and suggests additional defensive uses for vision in echinoderms. Finally, we found that animals missing a single arm orient less well to static stimuli, which requires further investigation.

Keywords: Echinoderms; Extraocular vision; Ophiuroids; Vision.

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Conflict of interest statement

Competing interests The authors declare no competing or financial interests.

Figures

Fig. 1.
Fig. 1.
Orientation experiments in Ophiomastix wendtii. (A) Animals were placed at the centre of a circular arena with a vertical bar stimulus presented at one side and their movements were filmed from above. (B) Stimuli varied in angular width (i,ii) or in Michelson contrast (iii,iv). (C) Intensity profiles of the four example stimuli i–iv, demonstrating variation in width and amplitude.
Fig. 2.
Fig. 2.
Ophiomastix wendtii reacts to shadows looming and passing overhead. Animals were placed within a small tank with an overhead screen that presented a loom stimulus (a growing black circle) or an overhead pass (OHP) stimulus (a circle of the same maximum width passing across the screen). Observers were blind to the presence or absence of stimuli, and reported presence or absence of a response from filmed experiments. Curves represent modelled responses to loom and OHP stimuli, accounting for animal and observer identity. The vertical line at log κ=0 represents responses to a control stimulus. The proportion of the area under each curve that exceeds the control can be interpreted as the probability that animals responded to the stimulus.
Fig. 3.
Fig. 3.
Ophiomastix wendtii responds to vertical bar stimuli of angular width 50 deg and above. The total angular width of the stimulus was increased from 20 to 70 deg, in 10 deg increments. Michelson contrast was 0.95. (A) Terminal bearings were disoriented relative to stimuli of 20–40 deg angular width, but clustered around the centre of the stimuli 50 deg and above. Pink dots represent one individual, presented with the stimulus once. Arrows indicate the direction and length of the mean vector; curved blue lines indicate maximum likelihood-based confidence intervals. (B) Marginal effects at the mean of orientation towards the stimulus with respect to stimulus angular width. The thin blue lines represent individual predictions. The dashed curved lines represent credible intervals (CI) for 50, 80 and 95% probability; 20 deg, N=40; 30 deg, N=43; 40 deg, N=41; 50 deg, N=52; 60 deg, N=42; 70 deg, N=40.
Fig. 4.
Fig. 4.
Effects of stimulus width on speed and tortuosity. (A) Stimulus size affected the duration of the experiments, with animals presented with a control stimulus (angular width=0 deg; N=37) taking significantly longer to complete trials than animals presented with 30–70 deg visual stimuli (Mann–Whitney U-test with Bonferroni correction for pairwise comparisons). (B) Full tracked paths of animals presented with control (left), 20 deg (centre) and 70 deg (right) stimuli. Note that not all experiments were available on video for tracking. (C) Straightness of animal paths (the length of the mean vector of turning angles, used to measure the efficiency of a directed walk) was consistently above 0.95 for all experiments, but was significantly higher in experiments using a visual stimulus than a control stimulus (Mann–Whitney U-test with Bonferroni correction for pairwise comparisons). (D) Sinuosity (a function of the mean cosine of turning angles, used to measure tortuosity in random walks) was significantly lower in experiments using a 70 deg than a control stimulus (Tukey's test with Bonferroni correction for pairwise comparisons). *Statistically significant differences (Padj<0.05).
Fig. 5.
Fig. 5.
Ophiomastix wendtii does not respond to low-contrast vertical bar stimuli. A vertical bar stimulus of 60 deg angular width was also presented with Michelson contrasts (MC) of 0.05 (N=39) and 0.1 (N=42). (A) Terminal bearings were disoriented relative to the centre of the stimulus. Arrows indicate the direction and length of the mean vector; curved blue lines indicate maximum likelihood-based confidence intervals. (B) Marginal effects at the mean of MC as a categorical variable on rates of successful orientation for a control stimulus (MC=0, N=37) and three experimental stimuli (MC of 0.05, 0.1 and 0.95). A circle represents a point estimate of the mean for each contrast level and a vertical line encloses the range of success proportions wherein the mean has 0.95 probability of falling.
Fig. 6.
Fig. 6.
Orientation to a vertical bar stimulus is impaired in Ophiomastix wendtii missing a single arm. (A) Terminal bearings relative to the initial orientation of the missing arm demonstrate that animals tend to move directly away from their missing arm. (B) Individuals missing one arm did not orient to the centre of a stimulus of 60 deg angular width and Michelson contrast of 0.95 when placed in the arena at a random orientation. (C) When individuals that began these experiments with the missing arm facing the stimulus were removed (open circles), the remaining individuals clustered around the stimulus. (D) Comparisons of initial and terminal body orientation showed that the position of the missing arm relative to the arena did not change during experiments, i.e. animals did not turn. Arrows indicate the direction and length of the mean vector; curved blue lines indicate confidence intervals around these; N=29 animals.
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