Research ArticleNEUROSCIENCE

Cuttlefish use stereopsis to strike at prey

See allHide authors and affiliations

Science Advances  08 Jan 2020:
Vol. 6, no. 2, eaay6036
DOI: 10.1126/sciadv.aay6036
  • Fig. 1 Anaglyph glasses combined with 3D disparate stimuli demonstrate perception of stereopsis in cuttlefish.

    (A) Experimental setup for tracking cuttlefish hunting behavior when presented with a prey stimulus. (B) Cuttlefish fitted with experimental anaglyph 3D colored glasses (see movies S1 and S2). Photo credit: Rachael Feord, University of Cambridge. (C) Stereoscopic stimulus geometry for the three disparity conditions. (D) Methodology used to calculate the illusory prey location using (i) the distance between the images at the screen (disparity), (ii) the interocular distance (measured for each animal), and (iii) the eyes to screen distance. (E) Distance from the animal’s eyes to the screen at the beginning of the ballistic part of the strike for a range of stimulus disparities. The stimulus image disparity range was −1 to +3 cm, with 4, 39, 9, 29, and 10 trials, respectively (n = 5). Significant differences are noted with star values, with the P values from left to right: *P = 0.0123, ***P = 0.0041, *P = 0.0161, and ***P < 0.0001 [one-way analysis of variance (ANOVA)]. Black line: mean; inner gray box: SEM; outer gray box: SD. (F) For each stimulus disparity and trial, the expected cuttlefish position when stereopsis is used [calculation method is shown in (D)] was subtracted from the measured position (P = 0.2490, 0.8897, 0.7498, and 0.4008; bootstrap test). (G) Length of tentacle extension for each stimulus disparity (P values from left to right: 0.0041, <0.0000, and <0.0000, one-way ANOVA). (H) For each stimulus disparity and trial, the difference between the measure and the expected length of tentacle extension was calculated (values are taken from 0 disparity; P < 0.0001, P = 0.2236, P = 0.0356, and P < 0.0001; bootstrap test). For (E) to (H), n = 2, 5, 2, 5, and 2 for −1-, 0-, 1-, 2-, and 3-cm disparities, respectively.

  • Fig. 2 Binocular vision improves hunting behavior.

    (A) Cuttlefish fitted with anaglyph 3D colored glasses enabled presentations of quasi-monocular and binocular visual stimuli (see movie S3). (B) Quantification of lapsed time, distance traveled, and distance from the animal’s eyes to the screen from quasi-monocularly (n = 3) and binocularly stimulated (n = 5) animals for four stages of the hunt: (i) detection = from stimulus appearance to first reaction, (ii) positioning = from first reaction to tentacles showing, (iii) strike start = from tentacles showing to beginning of ballistic strike, and (iv) prey seizure = from the ballistic start of the strike to animal contact. From one-way ANOVA, ***P < 0.0001 (top), ***P < 0.0001 (middle), and **P = 0.0018 (bottom). Black line: mean; inner gray box: SEM; outer gray box: SD. (C) Relationship between the time lapsed (i) until stimulus detection and (ii) between detection and positioning, combined quasi-monocular and binocular data: r2 = 0.0114; quasi-monocular alone (n = 3): r2 = 0.1331; binocular alone (n = 5): r2 = 0.0162. (D) Total lapsed time from stimulus presentation until “strike start” for quasi-monocular and binocular experiments. To test for the effect of target reversal, trials were categorized into those where the animal struck at prey before (left) or after (right) the direction of travel of the stimulus reversed (at 10.3 s). Quasi-monocular and binocular groups did not differ significantly [P = 0.3518 (left group) and 0.1040 (right group), one-way ANOVA].

  • Fig. 3 Cuttlefish perceive 3D locations correctly when stimuli are anticorrelated between the two eyes, but not uncorrelated.

    (A) The stimulus contrast was correlated between the right and left eyes (e.g., at 0-cm disparity, left green + right blue = cyan stimulus). Using this principle, we generated stimuli where a shrimp silhouette was filled with a random pattern of dark and bright dots against a background of random dark and bright dots, i.e., the shrimp was indistinguishable from the background in any one monocular frame (shrimp outline was added here only for display purpose). Middle: Distance from the animal’s eyes to the screen at the beginning of the ballistic part of the strike for no disparity and for 2-cm disparity tests (middle: ***P < 0.0001, one-way ANOVA). Bottom: Distance of each group from the expected value (0 cm used as control; P = 0.730, bootstrap test; see movie S3). (B) Top: Test as in (A), but with the stimulus contrast anticorrelated between the left and right eyes. Middle: As in (A), ***P < 0.0001, one-way ANOVA. Bottom: P = 0.499, Bootstrap test. Black line: mean; inner gray box: SEM; outer gray box: SD. n = 6 and 3 for 0- and 2-cm correlated disparities, and n = 5 and 4 for 0- and 2-cm anticorrelated disparities.

  • Fig. 4 Cuttlefish have independent eye movements, and their eyes are not equally converged before the strike.

    (A) Eye vergence angle at three time points during predatory behavior for 0- and 2-cm disparity stimuli where 0° is the eye looking laterally. T1: immediately before shrimp presentation; T2: after animal has rotated its body to view the screen and is moving forward; *P < 0.05; T3: during ballistic tentacle shoot; P = 0.15, 0.04, and 0.30, respectively, one-way ANOVA with time points. (B) Four randomly chosen examples of the eye angle of the two eyes at the three time points in the trial (see figs. S6 and S7 for data from all trials). (C) For each 0- and 2-cm disparity stimulus trial, the difference between the angular positions of the two eyes at the three time points was calculated, here shown as the cumulative percentage of animals (left) and its derivative (right). For (A) and (C), n = 5 and 5 for 0- and 2-cm disparities, respectively.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/6/2/eaay6036/DC1

    Fig. S1. Spectral content of screen and stimuli.

    Fig. S2. Stimulus spectra, filter properties, and spectral content cross-talk measurements—red/blue glasses.

    Fig. S3. Stimulus spectra, filter properties, and spectral content cross-talk measurements—blue/green glasses.

    Fig. S4. Speed of stimuli and polarity or background contrast do not alter the perceived location of the 3D prey.

    Fig. S5. Control analyses for different hunting behavior parameters.

    Fig. S6. Cuttlefish eye angles vary greatly during the hunt.

    Fig. S7. Diversity in cuttlefish eye vergence during the hunt.

    Fig. S8. Positioning does not differ between stimuli and glasses types.

    Movie S1. Method and animal behavior.

    Movie S2. Example responses to control and disparate stimuli (relates to Fig. 1).

    Movie S3. Example responses to quasi-monocular and binocular stimuli (relates to Fig. 2).

    Movie S4. Example responses to correlated, anticorrelated, and uncorrelated random dot stimuli (relates to Fig. 3).

  • Supplementary Materials

    The PDFset includes:

    • Fig. S1. Spectral content of screen and stimuli.
    • Fig. S2. Stimulus spectra, filter properties, and spectral content cross-talk measurements—red/blue glasses.
    • Fig. S3. Stimulus spectra, filter properties, and spectral content cross-talk measurements—blue/green glasses.
    • Fig. S4. Speed of stimuli and polarity or background contrast do not alter the perceived location of the 3D prey.
    • Fig. S5. Control analyses for different hunting behavior parameters.
    • Fig. S6. Cuttlefish eye angles vary greatly during the hunt.
    • Fig. S7. Diversity in cuttlefish eye vergence during the hunt.
    • Fig. S8. Positioning does not differ between stimuli and glasses types.
    • Legends for movies S1 to S4

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mp4 format). Method and animal behavior.
    • Movie S2 (.mp4 format). Example responses to control and disparate stimuli (relates to Fig. 1).
    • Movie S3 (.mp4 format). Example responses to quasi-monocular and binocular stimuli (relates to Fig. 2).
    • Movie S4 (.mp4 format). Example responses to correlated, anticorrelated, and uncorrelated random dot stimuli (relates to Fig. 3).

    Files in this Data Supplement:

Stay Connected to Science Advances

Navigate This Article