Predatory behavior under monocular and binocular conditions in the semiterrestrial crab Neohelice granulata

Abstract

Introduction: Neohelice granulata crabs live in mudflats where they prey upon smaller crabs. Predatory behavior can be elicited in the laboratory by a dummy moving at ground level in an artificial arena. Previous research found that crabs do not use apparent dummy size nor its retinal speed as a criterion to initiate attacks, relying instead on actual size and distance to the target. To estimate the distance to an object on the ground, Neohelice could rely on angular declination below the horizon or, since they are broad-fronted with eye stalks far apart, on stereopsis. Unlike other animals, binocular vision does not widen the visual field of crabs since they already cover 360° monocularly. There exist nonetheless areas of the eye with increased resolution.

Methods: We tested how predatory responses towards the dummy changed when animals' vision was monocular (one eye occluded by opaque black paint) compared to binocular.

Results: Even though monocular crabs could still perform predatory behaviors, we found a steep reduction in the number of attacks. Predatory performance defined by the probability of completing the attacks and the success rate (the probability of making contact with the dummy once the attack was initiated) was impaired too. Monocular crabs tended to use frontal, ballistic jumps (lunge behavior) less, and the accuracy of those attacks was reduced. Monocular crabs used prey interception (moving toward the dummy while it approached the crab) more frequently, favoring attacks when the dummy was ipsilateral to the viewing eye. Instead, binocular crabs' responses were balanced in the right and left hemifields. Both groups mainly approached the dummy using the lateral field of view, securing speed of response.

Conclusion: Although two eyes are not strictly necessary for eliciting predatory responses, binocularity is associated with more frequent and precise attacks.

Keywords: binocular integration; crustacean; eye occlusion; predatory strategy; stereopsis.

FIGURE 1

Experimental arena and measurement criteria. Scheme (A) and photograph (B) of the experimental arena (top view from where the video camera was located). A tracking line located at the center of the arena allowed an attached dummy (1.5 cm diameter) to be pulled, using a manual steering wheel, at ground level between the two sides of the arena. Relative azimuthal position criteria used for the dummy in binocular (C) and monocular crabs: left vision (D) and right vision (E). Two arcs of 180° were defined. The frontal part (midline between the eyes) was considered 0°. Positive values (0 to 180°) were considered for the right hemifield in binocular crabs (C) and for the side of the viewing eye in monocular crabs (D,E). Negative angles (0 to – 180°) were used for the left side for the binocular condition (C) and for the side corresponding to the blind eye in monocular conditions (D,E). (F) We measured dummy-crab distance (d) and relative position of the dummy (θ) at the beginning of the attack. (G) For lunging attacks, the accuracy of the strike (AS) was worked out by projecting a line from the middle of the two outstretched claws and measuring the distance from this line (when it intersected the tracking line) to the middle of the dummy.

FIGURE 2

Response differences in binocular and monocular crabs. (A) Percentage of responses evoked by the dummy in crabs (purple: binocular; green: monocular) categorized into four mutually exclusive responses: freezing response (FR; if crabs were moving and stopped upon the movement of the dummy), no response (NR; if no change in behavior was evoked by the dummy), avoidance response (AR; if crabs moved away from the dummy) and predatory response (PR; if crabs moved toward the dummy). (B) Observed predatory responses were split into incomplete attacks (IA) and, for complete attacks: successful attacks (SA; if the crab caught or touched the dummy) and unsuccessful attacks (UA; if it did not). (C) Proportion of the 3 attack strategies used for the complete predatory responses. Interception represents an attack triggered while the dummy was approaching the crab (red). Lunge behavior, if the crab jumped forward very quickly (blue) and pursuit if the crab attacked while the dummy was moving away (gray).

FIGURE 3

Relative azimuthal position of the dummy respective to the frontal midline of the crab at the start of the attack for all complete attacks in binocular (A) and monocular (B) crabs. The midline between the eyes is set at 0°, positive values represent the right hemifield in binocular crabs and the side ipsilateral to the viewing eye in monocular crabs, negative angles represent the left side and the side corresponding to the blind eye. Relative azimuthal position is plotted against dummy-crab distance. The strategies used are represented by the different symbols: squares for interception, circles for lunge and triangles for pursuit attacks. The outcome of each attack is denoted by the color: orange for successful and blue for unsuccessful attacks.

FIGURE 4

(A) Orientation of the crabs in the arena at the beginning of the complete attack trials (when the dummy first began to move). The x-axis categories display the side of the crab (Front, Back, Left, and Right) closest to the tracking line. Purple bars: binocular crabs; Green bars: monocular crabs split in right vision (light green) and left vision (dark green). (B) Attack strategies used depended on the orientation of the crabs in the arena at the beginning of the trial. Percentage of use of the different strategies of predatory responses (PRs; Interception: red; Lunge: blue; Pursuit: gray) in relation to the side of the crab (Front, Back, Left, and Right) closest to the tracking line and the viewing condition: binocular, right and left vision.

FIGURE 5

Parameters of interception attacks in binocular [(A,C): purple] and monocular [(B,D): green] crabs. (A,B) Bar plots showing the number of trials where the crabs had the dummy positioned in the different relative azimuthal positions (Bin size 45°; | 0–45°| = front; | 45–135°| = lateral; | 180–135°| = back) when the decision to attack was expected to be made (170 ms before the first approach movement). (C,D) Bar plots showing the number of trials where the crabs oriented at different angles respective to the dummy at the end of the attack (Bin size 45°; | 0–45°| = front; | 45–135°| = lateral; | 180–135°| = back). In (B,D) a marked side bias in monocular crabs toward the seeing eye side is noticeable. The black line marks the frontal midline that separate the two hemifields.

FIGURE 6

Parameters of lunge attacks in binocular [(A,C): purple] and monocular [(B,D): green] crabs. (A,B) Bar plots showing the number of trials where the crabs had the dummy positioned in different relative azimuthal positions (Bin size 45°; | 0–45°| = front; | 45–135°| = lateral; | 180–135°| = back) when the decision to attack was expected to be made. (C,D) Bar plots showing the number of trials where the crabs oriented at different angles respect to the dummy at the end of the attack (Bin size 45°; | 0–45°| = front; | 45–135°| = lateral; | 180–135°| = back). The distribution of binocular and monocular data is very similar. The black line marks the frontal midline that separate the two hemifields.