Cleaner fish recognize self in a mirror via self-face recognition like humans

Abstract

Some animals have the remarkable capacity for mirror self-recognition (MSR), yet any implications for self-awareness remain uncertain and controversial. This is largely because explicit tests of the two potential mechanisms underlying MSR are still lacking: mental image of the self and kinesthetic visual matching. Here, we test the hypothesis that MSR ability in cleaner fish, Labroides dimidiatus, is associated with a mental image of the self, in particular the self-face, like in humans. Mirror-naive fish initially attacked photograph models of both themselves and unfamiliar strangers. In contrast, after all fish had passed the mirror mark test, fish did not attack their own (motionless) images, but still frequently attacked those of unfamiliar individuals. When fish were exposed to composite photographs, the self-face/unfamiliar body were not attacked, but photographs of unfamiliar face/self-body were attacked, demonstrating that cleaner fish with MSR capacity recognize their own facial characteristics in photographs. Additionally, when presented with self-photographs with a mark placed on the throat, unmarked mirror-experienced cleaner fish demonstrated throat-scraping behaviors. When combined, our results provide clear evidence that cleaner fish recognize themselves in photographs and that the likely mechanism for MSR is associated with a mental image of the self-face, not a kinesthetic visual-matching model. Humans are also capable of having a mental image of the self-face, which is considered an example of private self-awareness. We demonstrate that combining mirror test experiments with photographs has enormous potential to further our understanding of the evolution of cognitive processes and private self-awareness across nonhuman animals.

Keywords: mental image; mirror self-recognition; photograph mark-test; self-awareness; self-face recognition.

Fig. 1.

Results of mirror mark test. The number of throat-scraping behaviors by cleaner fish in E1: period before treatment, E2: fish marked and mirror not visible, and E3: fish marked and mirror visible. ×3 = 3 individuals. Friedman test, χ₅2 = 20.00, P < 0.0001, and Kendall W (effect size) = 1.000. A and B show statistically significant differences by exact Wilcoxon signed-rank tests with sequential Bonferroni adjustment.

Fig. 2.

Cleaner fish photograph models used in experiment 1. (Cleaner fish photograph models used in experiment 1. (A) Faces of focal fish, and (B) an example of the photographic models used in the experiment. SS, self; UU, unknown fish; self-face/unknown body, SU; and unknown face/self-body, US.

Fig. 3.

Frequency of aggressive behavior directed toward photographic models in experiment 3. Self (SS) and unfamiliar fish (UU) models and composite self-face/unfamiliar body (SU) and unfamiliar face/self-body (US) models. Before MSR = before mirror presentation, after MSR = after passing the mark test. Means and SEM. (A) Total aggression. Friedman test, χ₅2 = 36.51, n = 10, P < 0.0001, and Kendall W (effect size) = 0.730. a and b show statistically significant differences by exact Wilcoxon signed-rank tests with sequential Bonferroni adjustments. (B) Aggressive behaviors: rushing (white), bumping (light gray), and biting (dark gray). Friedman test, χ₅2 = 3.75, n = 10, P = 0.59, and Kendall W (effect size) = 0.075; χ₅2 = 27.59, n = 10, P < 0.0001, and Kendall W (effect size) = 0.552; and χ₅2 = 35.05, n = 10, P < 0.0001, and Kendall W (effect size) = 0.701, respectively. (C) Changes in aggression toward photograph models over the 5 min experimental period.

Fig. 4.

Frequency of aggressive behavior toward three composite photographs of self-face, familiar neighbor face, and unfamiliar stranger face, all placed on the body of another unfamiliar individual. Aggression toward self and neighbor photograph models after a 1 d absence from the focal fish’s territory. Means and SEM. (A) Total aggressions. Friedman test, χ₂2 = 16.00, n = 8, P < 0.001, and Kendall W (effect size) = 1.000. A–C show statistically significant differences by exact Wilcoxon signed-rank tests with sequential Bonferroni adjustments. (B) Aggressive behaviors: rushing (white), bumping (light gray), and biting (dark gray). Friedman test, χ₅2 = 3.90, n = 8, P = 0.14, and Kendall W (effect size) = 0.244; χ₅2 = 13.04, n = 8, P < 0.01, and Kendall W (effect size) = 0.815; and χ₅2 = 14.21, n = 8, P < 0.001, and Kendall W (effect size) = 0.888, respectively. (C) Changes in aggression toward photograph models over the 5 min experimental period.