Serial visual reversal learning in harbor seals (Phoca vitulina)

Abstract

Progressively improving performance in a serial reversal learning (SRL) test has been associated with higher cognitive abilities and has served as a measure for cognitive/behavioral flexibility. Although the cognitive and sensory abilities of marine mammals have been subject of extensive investigation, and numerous vertebrate and invertebrate species were tested, SRL studies in aquatic mammals are sparse. Particularly in pinnipeds, a high degree of behavioral flexibility seems probable as they face a highly variable environment in air and underwater. Thus, we tested four harbor seals in a visual two-alternative forced-choice discrimination task and its subsequent reversals. We found significant individual differences in performance. One individual was able to solve 37 reversals showing progressive improvement of performance with a minimum of 6 errors in reversal 33. Two seals mastered two reversals, while one animal had difficulties in learning the discrimination task and failed to complete a single reversal. In conclusion, harbor seals can master an SRL experiment; however, the performance is inferior to results obtained in other vertebrates in comparable tasks. Future experiments will need to assess whether factors such as the modality addressed in the experiment have an influence on reversal learning performance or whether indeed, during evolution, behavioral flexibility has not specifically been favored in harbor seals.

Keywords: Behavioral flexibility; Cognition; Pinniped; Progressive improvement; Visual discrimination.

Fig. 1

Experimental setup. The stimuli, a horizontal versus a vertical black bar (6 × 20 cm) on a white PVC board (B, 2 × 1.8 m) 15 cm above the water surface were presented to the animal stationing in a hoop station (HS) at 1.8 m distance with its head above the water surface. Between trials, stimuli were covered by a guillotine slide shutter (GS). The start of a trial was signaled by lifting the shutter upon which the animal left the station, swam towards the stimuli, and indicated its decision by touching the response target (RT) below the stimulus of its choice with the snout. Upon touching a response target, the response was recorded, and the shutter was closed. The experimenter observed the animal from behind the board through an observation slit (OS) and by means of three mirrors, M2, M3 and one mirror mounted behind the animal (not shown in the figure) to view the animal in the hoop station. Three stimuli (S_x, S_y, S_x) were mounted on the sliding board (SB, shown enlarged in the inset, not drawn to scale). During the intertrial interval (ITI), the stimulus pair in the stimulus window (SW) was changed (S_x, S_y or S_y, S_x) by moving the board to the left or right behind the closed shutter

Fig. 2

Performance of the four tested harbor seals displaying the number of errors per reversal. Please note that for seal Nick, only the first four of the 37 Rs are displayed. Dashed lines indicate that training continued after the acquisition phase in seal Moe and after R2 in seal Sam without the seals completing the respective reversal until the experiment was terminated

Fig. 3

Seal Nick’s performance in number of errors per reversal. This seal successfully completed 37 reversals. His performance progressively improved to a minimum of 6 errors in R33 albeit the presence of strong fluctuations in performance

Fig. 4

Seal Nick’s performance in % correct choices per session for A R0-R14, and B R15-R37. The solid line indicates the learning criterion of 80% correct choices to be met in one session, the dashed lines mark the upper and lower significance level of 70% and 30% correct choices, and the central dotted line at a performance of 50% corresponds to chance performance

Fig. 5

Performance in % correct choices per session for R0-R2 for all seals. For Nick, only the results of the first 2 Rs of altogether 37 Rs are displayed. Note that Moe did not complete R1, and sessions 48 to 120 of the unresolved R are not shown. The solid line indicates the learning criterion of 80% correct choices to be met in one session, the dashed lines mark the upper and lower significance level of 70% and 30% correct choices, and the central dotted line at a performance of 50% corresponds to chance performance

Fig. 6

Side preference of seal Nick displayed in (A) % responses on the left side per R, regardless of correctness. Significant difference between % responses per side is marked with * for P ≤ 0.05 and ** for P ≤ 0.001. There is no indication for a decline in Nick's side preference before R29. B Absolute number of sessions per R stacked by percentage of correct responses on the left side; 100% (15 out of 15 possible correct responses, black bar), 93% (14 out of 15 possible correct responses, dark gray), 87% (13 out of 15 possible correct responses, light gray), 80% (12 out of 15 possible correct responses, shaded bar), and < 80% (less than 12 out of 15 possible correct responses, white). In 77.4% of all sessions, Nick responded correctly on the left side with performances between 80 and 100%, indicating that his success in mastering an R was determined by his correct responses when the S+ was on the right