Optic flow, a rich source of optic information for harbour seals (Phoca vitulina)

Abstract

Marine mammal vision is often considered to only provide limited information, particularly underwater in low light levels and turbidity. However, when these animals move through turbid water optic flow is elicited. A past study has documented the harbour seal's (Phoca vitulina) ability to perceive deviations from heading from optic flow simulating movement through a volume of turbid water. Here, we asked whether harbour seals are also able to perceive and analyse surface optic flow. Thus, we simulated three optic flow environments and trained three harbour seals to determine the simulated heading. The harbour seals precisely indicated their heading with a mean (±s.d.) accuracy of 4.61±0.56 deg for volume optic flow, 4.96±0.74 deg for surface optic flow mimicking movement over a surface and 3.58±1.12 deg for surface optic flow mimicking movement underneath a surface. We conclude that harbour seals have access to and can thus rely on optic (flow) information whenever there is enough light for vision, thus refuting existing opinions about poor visual guidance in harbour seals or, more generally, in marine mammals. A detailed analysis of optic flow perception in (semi-) aquatic animals is expected to enhance our understanding of optic flow perception and vision in general.

Keywords: Heading; Marine mammal; Motion vision; Movement; Vision.

Fig. 1.

Illustration of the experimental setup and stimuli used for testing aerial optic flow perception in harbour seals. (A) Experimental setup for testing optic flow perception in harbour seals in air. A 42-inch monitor was installed in the experimental chamber. The monitor was surrounded by a tunnel of black velvet (100 cm wide, 65 cm high, 120 cm long) and served to present the stimuli (here: above-surface optic flow). With the help of the tunnel and because the setup was installed in an experimental chamber, we achieved a constant ambient illumination of <0.1 lx in the experimental area in front of the monitor. The tunnel also directed the harbour seals' attention towards the monitor. In front of the monitor, a metal hoop station was installed ensuring a constant distance of the harbour seals to the monitor. Additionally, to the left and right of the hoop, two response targets (RT) were installed to which the harbour seals responded in line with a two-alternative forced-choice experiment. The behaviour of the harbour seals was observed via a camera from the back of the chamber where the experimenter was hiding behind a curtain (not shown) out of the field of view of the harbour seals to avoid secondary cueing. (B) Schematic visualization of the presented optic flow field during simulation of a translational forward movement through a volume. (C) Schematic visualization of the presented optic flow field when simulating a translational forward movement above a surface. (D) Schematic visualization of the presented optic flow field when simulating a translational forward movement underneath a surface. For a detailed description of the stimuli see Materials and Methods, ‘Stimuli’. The lines indicate the associated velocity vectors. The focus of expansion (FOE) is always on the right side of the midline of the monitor.

Fig. 2.

Performance of the three harbour seals during basic task acquisition for volume optic flow and above- and beneath-surface optic flow. The dashed line indicates the performance level of 80% correct choices the harbour seals had to reach/surpass in two consecutive sessions to fulfil the learning criterion. Areas with a grey shaded background mark sessions of overtraining. After basic task acquisition, we entered the heading accuracy threshold (HAT) determination phase. Once the HATs of one optic flow stimulus had been determined, we entered into the basic task acquisition phase for the next optic flow stimulus. (A) Learning curve of seal Luca. After Luca reached the learning criterion, we carried out seven sessions of overtraining with volume optic flow (open circles) before HAT determination. For above-surface optic flow (filled circles), we performed three sessions of overtraining and for beneath-surface optic flow (half-filled circles), we performed two sessions of overtraining after reaching the learning criterion. (B) Seal Nick was first presented with the above-surface optic flow. We carried out two sessions of overtraining for each of above-surface optic flow (filled circles), volume optic flow (open circles) and beneath-surface optic flow (half-filled circles). (C) The experimentally naive seal Miro took the longest to reach the learning criterion (sessions 36-52 with marked FOE, for details see Results, ‘Basic task acquisition’, above). After reaching the learning criterion with unmarked FOE, we performed three sessions of overtraining for above-surface optic flow (filled circles) before HAT determination. For both volume optic flow (open circles) and the subsequent beneath-surface optic flow (half-filled circles), we carried out two sessions of overtraining before HAT determination.

Fig. 3.

Determined HATs for volume, above-surface and beneath-surface optic flow for the three harbour seals and three human participants. Data are for seals Luca (filled circles), Nick (filled squares) and Miro (filled triangles) and the human participants H1 (open squares), H2 (open triangles) and H3 (open circles). Please note that we collected another HAT (marked with an asterisk) for volume optic flow with seal Luca some months after the first HAT determination (see Materials and Methods and Results ‘Harbour seals’).