Dolphin experiment

Participants

Three adult male bottlenose dolphins (Tursiops truncates) (Peace, Tino and Eagle) participated in the study (see Fig. 4a). They were all wild-born and had lived in the Port of Nagoya Public Aquarium (PNPA) in Nagoya City, Aichi, Japan, for approximately 6 years at the time of the study. Their estimated ages ranged from 9 to 12 years and they lived as a group in a pool (elliptical shape, 16 m × 11 m and 6.5 m in depth). They usually received four 15-minute sessions of husbandry, performance and cognitive training–including matching-to-sample tasks–per day13. However, they did not participate in public performances during the study period. The participants were fed approximately 9 kg of fish during the training sessions, which were conducted by several trainers. The experimental procedure for the dolphins was approved by a PNPA committee and adhered to the Ethical Guidelines for the Conduct of Research on Animals by Zoos and Aquariums issued by the World Association of Zoos and Aquariums (WAZA), the Code of Ethics issued by the Japanese Association of Zoos and Aquariums (JAZA) and the Japanese Act on Welfare and Management of Animals.

Stimuli

Stimuli used in the dolphin experiment are shown in Figure 2. Each stimulus was 20 cm × 20 cm, made of PVC (polyvinyl chloride) tubing (2.5 cm in diameter) and covered with yellow waterproof vinyl tape. When the dolphins viewed the stimuli from the water (approximately 1 m from the stimulus), they had approximately 10 degrees of visual angle. These stimuli were made of three-dimensional materials, but the third dimension was not manipulated; thus, we regarded these as two-dimensional stimuli. As shown in Figure 2, these stimuli were composed of several simple features. Based on previous studies, we chose seven features to distinguish these forms from one another. The features included vertical/horizontal lines, curvature, diagonal lines, closure, open endedness, right angles and acute angles. There were other critical features related to form perception, but features that appeared in fewer than three stimuli were omitted from analyses (such as X or T junctions).

Procedure

We tested perceptual similarity using a face-to-face matching-to-sample task (Fig. 1a). Experiments were conducted in the air at poolside. Two experimenters controlled all experimental events. One of the experimenters (E1) sat behind a light blue plastic board (60 cm wide × 60 cm high). After a 10-second intertrial interval in which the dolphin remained in front of the board, E1 presented the sample stimulus by hand. The dolphin was required to touch the sample with his rostrum (“rostrum-touch”). After the rostrum-touch, E1 retracted the sample and then presented the two choice stimuli with both hands. This task is known as delayed matching. If the dolphin touched the stimulus that was identical to the sample, E1 blew a whistle, retracted both stimuli and gave pieces of fish as a reward. If the dolphin chose the other stimulus, E1 immediately retracted the stimuli without any feedback. The other experimenter (E2) stood near the apparatus, instructed E1 about the stimulus arrangement for each trial and recorded the dolphin's choice. Each session consisted of 10 trials and sessions were inserted in the routine husbandry training schedules. Each dolphin participated in 1–4 sessions per day. Initially, all dolphins were trained on the matching task with three-dimensional objects, such as plastic bottles and flying discs. Using step-by-step criteria, all three dolphins engaged in this acquisition training until they showed at least 75% accuracy over 3,000 trials (3,140 trials averaged across dolphins). In this study, each dolphin showed 79% accuracy across the last 80 trials. After successfully completing acquisition training, they participated in data-collection sessions.

By combining nine stimuli into pairs, we included 36 pairings in the study. However, only one pair appeared in each 10-trial session. This procedure differed from that for chimpanzees (described later) because the accuracy of the dolphins often decreased when various kinds of stimulus sets randomly appeared in one session. Dolphins Peace and Eagle received five sessions (50 trials) for each pair, receiving a total 180 sessions (1,800 trials). Due to time constraints at the Aquarium, Tino received a total of only 360 trials and was not presented with nine pairs of the 36 pairs in the study (indicated with arrows in Fig. 3a). Although Tino completed fewer trials, his performance was quite similar to that of the other two dolphins, as shown in the high intraclass correlation coefficient (ICC(2,3) = 0.634). Correlation coefficients comparing the accuracy of Tino with that of the two other dolphins were 0.40 for Tino and Peace (P = 0.041) and 0.52 for Tino and Eagle (P = 0.015), which is comparable to that for Peace and Eagle (r = 0.41, P = 0.028, using Holm's corrections). Note that response-time data, although recorded during the study, were not used for data analyses because of considerable variance.

Chimpanzee experiment

Participants

Seven chimpanzees (Pan troglodytes) (Ai, 33-year-old female; Ayumu, 10-year-old male; Chloe, 29-year-old female; Cleo, 10-year-old female; Pan, 26-year-old female; Pal, 10-year-old female; and Pendesa, 33-year-old female) participated in the study (see Fig. 4b). All participants lived in a social group of 14 individuals in an indoor and environmentally enriched outdoor compound (770 m2) at the Primate Research Institute, Kyoto University (KUPRI), Japan38. They were not food-deprived and were fed fruits, vegetables and primate chow three times each day during the study. They had previously engaged in various kinds of computer-controlled perceptual and cognitive tasks, including those involving matching to sample19,21,22,39,40,41,42,43,44. As a result, all chimpanzee participants were already familiar with generalised identity-matching tasks at the beginning of the present experiments; thus, we did not need to conduct any acquisition training for this group. The mean accuracy of all participants was 87.3% ± 6.6 (SD) in the first session. The care and use of the chimpanzees adhered to the 3rd edition of the Guide for the Care and Use of Laboratory Primates issued by KUPRI in 2010, which is compatible with the guidelines issued by the National Institute of Health in the United States of America. The research design was approved by the Animal Welfare and Animal Care Committee of KUPRI and by the Animal Research Committee of Kyoto University. All procedures adhered to the Japanese Act on Welfare and Management of Animals.

Apparatus and stimuli

Experimental sessions were conducted in a booth (1.8 × 2.15 × 1.75 m) in the experimental room adjacent to the chimpanzee facility. Each chimpanzee came to the booth via an overhead walkway connecting the facility and the booth. A 17-inch LCD monitor (1280 × 1024 pixels, pixel size: 0.264 mm × 0.264 mm) with a touch panel was installed on the wall of the booth (see Fig. 1b). Viewing distance was approximately 40 cm. The food reward was delivered via a universal feeder. All equipment and experimental events were controlled by computer. Stimuli used for the chimpanzees were colour photographs of the stimuli used for the dolphins. Each stimulus was 210 pixels × 210 pixels (55 mm × 55 mm, approximately 8 deg of visual angle) and was presented in yellow against a light blue background (see Fig. 1b).

Procedure

We used a delayed matching task with the chimpanzee participants (Fig. 1b). Each trial began with the presentation of a blue square (26 mm × 26 mm) at the bottom centre of the monitor. When the chimpanzee touched this square twice, a sample stimulus appeared at one of six (three columns × two rows) predetermined locations. When the chimpanzee touched the sample, it immediately disappeared, followed by the presentation of the two choice stimuli. The configuration of the stimuli was randomly changed from trial to trial. If the chimpanzee touched the choice stimulus identical to the sample, all stimuli disappeared, followed by the sound of a chime and the presentation of a food reward (a small piece of apple or raisin). If the chimpanzee touched the other stimulus, a buzzer sound was presented as error feedback. Following an error trial, a modified version of a correction procedure was used in which only the correct choice stimulus was presented (for correction only; not used in data analyses). This procedure was used to prevent inappropriate runs of error trials. The intertrial interval was 2 seconds. In contrast to the sessions with dolphins, sessions with the chimpanzees consisted of 36 trials, during which all 36 pairs appeared once. Each chimpanzee received 20 sessions; therefore, we collected data from 20 trials for each pair. As in the dolphin trials, response-time data were not used for analyses although they were recorded at the time.

Human experiments

Participants

Twenty PNPA volunteers participated as a group in the rating experiment. All participants had normal or corrected-to-normal vision. The purpose of and procedure for rating were explained orally by the experimenter and informed consent was obtained from all participants. All protocols were approved by the Human Research Ethics Committee of KUPRI.

Procedure

We used visual analog scaling (VAS) in the experiment with humans22. Participants sat in a visitor room and received a sheet on which pictures of the 36 stimuli pairs were printed. Each stimulus was 7 mm × 7 mm (approximately 3 deg of visual angle). Participants were instructed to judge the similarity of the stimulus pair and make a mark on an adjacent horizontal line. The rating for “most dissimilar” was placed on the left end of the line and the mark for “most similar” was placed on the right end of the line. The sheets were scanned and converted to digital image files. Using customised application software, dissimilarity was calculated based on the spatial location of the check mark.

Data analysis

Dissimilarity index

For dolphins and chimpanzees, the dissimilarity index for each pair was defined as the absolute value of the percent of correct choices subtracted by 50% (chance level). This index ranged from 0 (most similar) to 50 (most dissimilar). For humans, the relative distance of the mark from the right was used as the dissimilarity index, which also ranged from 0 to 1.

Inter-observer variability

To evaluate similarities in the performances of participants, we calculated the ICC using random-effects models (i.e., ICC(2, n); n designates the number of participants). These values were calculated using SPSS 19.0 J and statistically tested with a null hypothesis of ICC = 0. Furthermore, using dissimilarity data averaged across participants, we also calculated the ICC (using a mixed effects model) for evaluating inter-species variability.

Multidimensional scaling analysis

To understand the spatial configuration of perceptual similarities among stimuli, we conducted multidimensional scaling analyses for each species using INDSCAL. This method yielded spatial representations for the stimuli as well as weights for each dimension of this representation for each observer. We adopted a two-dimensional solution for the present analyses using SPSS 19.0J. Obtained representations ranged from −2.0 to 2.0 for each dimension. To evaluate goodness of fit, we presented stress values and coefficients of determination (RSQ).

Relative contribution of features

To evaluate the relative contribution of each individual feature to the perceptual grouping, we calculated the mean percent of correct choices for pairs in which both stimuli had the same individual features. These values were standardised using means and standard deviations (referred to as standardised dissimilarity); they were then analysed with a two-way (species × features) repeated-measures ANOVA.