If a fish can pass the mark test, what are the implications for consciousness and self-awareness testing in animals?

Abstract

Abstract: The ability to perceive and recognise a reflected mirror image as self (mirror self-recognition, MSR) is considered a hallmark of cognition across species. Although MSR has been reported in mammals and birds, it is not known to occur in any other major taxon. Potentially limiting our ability to test for MSR in other taxa is that the established assay, the mark test, requires that animals display contingency testing and self-directed behaviour. These behaviours may be difficult for humans to interpret in taxonomically divergent animals, especially those that lack the dexterity (or limbs) required to touch a mark. Here, we show that a fish, the cleaner wrasse Labroides dimidiatus, shows behaviour that may reasonably be interpreted as passing through all phases of the mark test: (i) social reactions towards the reflection, (ii) repeated idiosyncratic behaviours towards the mirror, and (iii) frequent observation of their reflection. When subsequently provided with a coloured tag in a modified mark test, fish attempt to remove the mark by scraping their body in the presence of a mirror but show no response towards transparent marks or to coloured marks in the absence of a mirror. This remarkable finding presents a challenge to our interpretation of the mark test—do we accept that these behavioural responses, which are taken as evidence of self-recognition in other species during the mark test, lead to the conclusion that fish are self-aware? Or do we rather decide that these behavioural patterns have a basis in a cognitive process other than self-recognition and that fish do not pass the mark test? If the former, what does this mean for our understanding of animal intelligence? If the latter, what does this mean for our application and interpretation of the mark test as a metric for animal cognitive abilities?

Editor’s note: This Short Report received both positive and negative reviews by experts. The Academic Editor has written an accompanying Primer that we are publishing alongside this article (https://doi.org/10.1371/journal.pbio.3000112). The linked Primer presents a complementary expert perspective; it discusses how the current study should be interpreted in the context of evidence for and against self-awareness in a wide range of animals.

Fig 1. Responses of cleaner wrasse to the mirror and to real fish across a clear divider.

(A) Change in social responses towards the mirror. Mean ± SE for time spent mouth fighting (red), time spent within 5 cm of the mirror without being aggressive (blue), and frequency of mirror-testing behaviours/10 min (green). Superscript labels a, b, and c denote statistical differences. Statistical results for daily changes in time spent mouth fighting, LMM, c₇² = 91.87, P < 0.0001; time spent in front of the mirror, LMM, c₇² = 64.63, P < 0.0001; and changes in the number of mirror-testing behaviours, GLMM, c₇² = 137.08, P < 0.0001. (B) Change in social responses towards the mirror for fish that failed to pass through prephases of the test. (C) Change in social responses to conspecific fish over 2 wk: statistical results for daily changes in time spent mouth fighting, LMM, df = 7, χ² = 27.36, P = 0.0003, and time spent in front of the mirror, LMM, df = 7, χ² = 9.09, P = 0.25; no idiosyncratic behaviours were observed in this condition. Underlying data for this figure can be found in S1 Data. df, degrees of freedom; GLMM, generalised linear mixed model; LMM, linear mixed model.

Fig 2. Mark locations and time spent in postures facilitating viewing of the marked site.

(A) Time spent in postures that reflect the marked location (i.e., the ‘correct’ side). Repeated-measures ANOVA, main effect of sequences: F = 12.09, P = 0.016; marked position: F = 19.06, P = 0.005; sequence × marked position: F = 0.70, P = 0.54. *P < 0.05 (n = 8). (B) Time spent in postures that reflect the unmarked locations. Repeated-measures ANOVA, sequence: F = 2.54, P = 0.12; marked position: F = 13.15, P = 0.0008; sequence × marked position: F = 0.99, P = 0.42. Underlying data for this figure can be found in S1 Data. ANOVA, analysis of variance; ns, not significant. Line colours: marked site on right side of head (orange), left side of head (blue), or throat (red). Node shapes: postures reflecting right side of head (circle), left side of head (square) or throat (triangle).

Fig 3. Frequency of throat-scraping behaviour throughout experimental phases.

(A) Frequency of throat-scraping behaviour of the four throat-marked fish during periods E2, E3, E4, and E5. (B) Schematic sequence of posturing, throat-scraping behaviour, and then posturing again in positions that reflect the throat. Underlying data for this figure can be found in S1 Data.