Survival of the stillest: predator avoidance in shark embryos

Abstract

Sharks use highly sensitive electroreceptors to detect the electric fields emitted by potential prey. However, it is not known whether prey animals are able to modulate their own bioelectrical signals to reduce predation risk. Here, we show that some shark (Chiloscyllium punctatum) embryos can detect predator-mimicking electric fields and respond by ceasing their respiratory gill movements. Despite being confined to the small space within the egg case, where they are vulnerable to predators, embryonic sharks are able to recognise dangerous stimuli and react with an innate avoidance response. Knowledge of such behaviours, may inform the development of effective shark repellents.

Figure 1. A–C.

Photographs depicting three major life stages of the bamboo shark (Chiloscyllium punctatum). A: Embryo encapsulated within an egg case. B: Early juvenile (post hatching) showing its high contrast banding pattern. C. Sexually mature individual that has lost its banding leaving a more typical counter-shading pattern, which it uses to camouflage itself on the substrate. Scale bars = 10 mm.

Figure 2. Average freeze response duration (±2×Standard Error) of bamboo shark embryos (stage 32–34) to a range of sinusoidal frequencies (0–20 Hz) and stimulus intensities (0.4–2.1 µV/cm).

Shaded bar corresponds to natural respiratory signals produced by potential predators (1.0–2.0 Hz) and low frequency modulations of D.C. fields produced by approaching predators as they move relative to an object (0.1–1.0 Hz) . Peak response frequency: 0.5 Hz; duration: mean 18.9 secs.

Figure 3. A–I.

Freeze response duration (±2×Standard Error) of bamboo shark embryos (stages 32–34) to a range of sinusoidal frequencies (0–20 Hz) and stimulus intensities (0.4–2.1 µV/cm). Embryos are categorised into nine groups according to their relative stage in development and intensity of the electric field strength exposure. A: Stage 32 embryos exposed to 1.9–2.1 µV/cm (peak response frequency: 0.5 Hz; duration: mean 16.7 secs). B: Stage 32 embryos exposed to 0.9–1.1 µV/cm (peak response frequency: 0.5 Hz; duration: mean 14.9 secs). C: Stage 32 embryos exposed to 0.4–0.6 µV/cm (peak response frequency: 0.5 Hz; duration: mean 0.3 secs). D: Stage 33 embryos exposed to 1.9–2.1 µV/cm (peak response frequency: 0.75 Hz; duration: mean 27.7 secs). E: Stage 33 embryos exposed to 0.9–1.1 µV/cm (peak response frequency: 1.0 Hz; duration: mean 13.8 secs). F: Stage 33 embryos exposed to 0.4–0.6 µV/cm (peak response frequency: 0.5 Hz; duration: mean 3.7 secs). G: Stage 34 embryos exposed to 1.9–2.1 µV/cm (peak response frequency: 0.5 Hz; duration: mean 59.4 secs). H: Stage 34 embryos exposed to 0.9–1.1 µV/cm (peak response frequency: 0.5 Hz; duration: mean 38.4 secs). I: Stage 34 embryos exposed to 0.4–0.6 µV/cm (peak response frequency: 0.5 Hz; duration: mean 15.8 secs).

Figure 4. Relative freeze response duration when embryos (stage 34) are repeatedly exposed to the same stimulus at set time intervals after the first (initial) response.

Embryos were individually exposed to the same stimulus to get an average initial response time. Embryos were then exposed to the same stimulus 60 minutes after initial response, and re-exposed at decreasing time intervals. Response duration is expressed as a percentage of the initial response.

Figure 5. Experimental apparatus used to study the response of bamboo shark embryos to predator simulating dipole electric fields.

A function generator and stimulus controller were used to deliver a dipole electric field of specific intensity and frequency to electrodes positioned along the same longitudinal axis as the embryo. Embryo responses were recorded with a video camera positioned directly in front of the experimental tank.