Mirror image processing in three marine mammal species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus)

doi:10.1016/S0376-6357(01)00134-6

Behavioural Processes

Volume 53, Issue 3, 26 April 2001, Pages 181-190

https://doi.org/10.1016/S0376-6357(01)00134-6 Get rights and content

Abstract

Dolphins (Tursiops truncatus) and their relatives might be expected to show mirror-induced contingency checking, a prerequisite to self-recognition, because of their high brain development, their complex social life and their demonstrated abilities in bodily imitation. A study of killer whales’(Orcinus orca) behaviour in front of a mirror is presented, including a mark test. Shorter investigations of mirror behaviour are also described in false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus). Contingency checking was present in killer whales and possibly also in false killer whales, but no clear contingency checking was observed in sea lions. The mark test on killer whales suggested that the marked animal anticipated that its image would look different. This study shows that killer whales and false killer whales, like bottlenose dolphins, appear to possess the cognitive abilities required for self-recognition.

Introduction

The mirror self-recognition paradigm has been used with many species of primates to assess the existence of a cognitive ability allowing individuals to understand mirrored information about the self (Gallup, 1982). To recognize its own mirror image, an individual may need a representation of itself; it may be aware of its own existence and possess the ability to monitor its own mental states (Anderson, 1984a, Anderson, 1984b): it may experience perceptual and reflective consciousness (Griffin, 1991).

Dolphins and their relatives might be expected to recognize themselves in mirrors because they possess a highly developed neural system, a complex social life and they show bodily imitation (Mitchell, 1993a, Mitchell, 1993b, Parker, 1991). Evidence for self-recognition in bottlenose dolphins (Tursiops truncatus) has already been found: looking in the mirror at parts of the body otherwise unobservable (Marten and Psarakos, 1994, Marten and Psarakos, 1995a, Marten and Psarakos, 1995b), and looking at themselves in a mirror after a zinc oxide mark is wiped off (Marino et al., 1994). The purpose of the present study is to extend the mirror behaviour paradigm to three additional species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens), and sea lions (Zalophus californianus), and to compare the results across all four species. Killer whales, false killer whales, and bottlenose dolphins are in the same family: delphinidae; sea lions are in another order, being pinnipeds. The cetaceans tested here are closely related, and we would expect killer whales and false killer whales to have similar mental characteristics to bottlenose dolphins and therefore behave similarly in front of a mirror.

Contingency checking consists of moving body parts, often rhythmically, and simultaneously looking at the mirror reflection to see if the same movement is occurring in the mirror. We focused our search on the presence or absence of contingency checking, which may be an indicator of self-recognition (Marten and Psarakos, 1994, Marten and Psarakos, 1995a, Marten and Psarakos, 1995b). We conducted a detailed study of the behaviour of killer whales in front of a mirror, including a mark test. Two smaller investigations on false killer whales and sea lions, using some of the same methods for observation and data collection, are included for comparative perspective.

Section snippets

Mirror experiment on killer whales (Orcinus orca)

The killer whales were studied for 24 days during September 1995. The study took place at Marineland in Antibes (France). At that time, five killer whales (Orcinus orca) were displayed: three females and two males. Because of an injury to his dorsal fin, one of the two males was isolated. Sharkan (14 years old), her daughter Shouka (2–7 years old) and a second female, Freya (20 years old), shared two tanks (35×70×15 m and 25×25×15 m) with the father of Shouka: Kim (20 years old). At the time of

Killer whale behaviour

(a) Time in front of mirror versus time in front of window

For one female, the mean amount of time spent in front of the mirror was significantly greater than mean time spent in front of the window (Fig. 1): Sharkan spent most of her time close to the mirror. Freya and Shouka also came often when the window was transformed as mirror.

(b) Differences in behaviour in front of the mirror and the no-mirror control

Discussion

The killer whales and false killer whales both responded to the mirror by displaying contingency checking behaviours. According to Crook (1983), to do this the subject must be conscious of the correspondence between its body position and a particular environmental state concomitant with each locomotor act; the subject must have at least an implicit knowledge of its position. False killer whales’ behaviour in front of the mirror was different from that in the live social condition. One possible

Conclusion

How does the individual perceive itself? It might consciously think about an object or an event and make rational choices (Griffin, 1991); it might perceive invariants between the image of the object (here, its reflection) and the real object (here, its own appearance) (Loveland, 1995); it might become the object of its own attention (Gallup, 1982); it might make a connection between its own image and the kinaesthetic and proprioceptive representation of its body. The interspecific comparison

Acknowledgements

We would like to thank Marineland Antibes for allowing us to carry out these experiments in their facility. The Earthtrust dolphin behaviour research laboratory is a cooperative effort between Earthtrust and Sea Life Park Hawaii. We would like to express our appreciation for support from the following: BHP Hawaii, the Sarah Stewart Foundation, and the Fondation Singer-Polignac in France. We would like to thank three anonymous referees for their helpful comments and suggestions.

References (26)

G.G Gallup et al.
Mirror, mirror on the wall which is the most heuristic theory of them all? A response to Mitchell
New Ideas Psychol.
(1993)
K.A Loveland
Self-recognition in the bottlenose dolphin: ecological considerations
Conscious. Cogn.
(1995)
K Marten et al.
Using self-view television to distinguish between self-examination and social behavior in the bottlenose dolphin (Tursiops truncatus)
Conscious. Cogn.
(1995)
K Marten et al.
Marten and Psarakos commentary response
Conscious. Cogn.
(1995)
R.W Mitchell
Mental models of mirror-self-recognition: two theories
New Ideas Psychol.
(1993)
R.W Mitchell
Recognizing one's self in a mirror? A reply to Gallup and Povinelli, De Lannoy, Anderson, and Byrne
New Ideas Psychol.
(1993)
R.W Mitchell
Evidence of dolphin self-recognition and the difficulties of interpretation
Conscious. Cogn.
(1995)
J Altmann
Observational study of behavior: sampling methods
Behaviour
(1974)
J.R Anderson
The development of self-recognition: a review
Dev. Psychol.
(1984)
J.R Anderson
Monkeys with mirrors: some questions for primate psychology
Int. J. Primatol.
(1984)

J.R Anderson

Self-recognition in dolphins: credible cetaceans; compromised criteria, controls and conclusions

Conscious. Cogn.

(1995)

L.T Ballance

Habitat use patterns and ranges of the Bottlenose dolphin in the Gulf of California, Mexico

Mar. Mammal Sci.

(1992)

Brodie, P.F., 1985. The acoustic alarctic aquabat. BBC Wildlife, pp....

Cited by (95)

Mirror mirror on the wall, it's not the mark I care about at all
2022, Learning and Motivation
Citation Excerpt :
In the presence of a mirror, the amount of self-exploratory and contingent behaviour increased, which the authors argued was evidence of mirror self-recognition. Similarly, Delfour and Marten (2001) observed whales displaying self-exploratory and unusual behaviour in the mirror. For example, the whales were observed exploring the inside of their mouth, and shaking their tongue in the mirror, behaviour that, again, independent of the mark test, invites interpretation as self-recognition.
The extent to which different species display self-recognition is a controversial topic in comparative cognition. Self-recognition is widely validated through the mark test in which a dye or paint mark is applied surreptitiously to the subject. Mark-directed responses in the presence of a mirror are taken as evidence of self-recognition. Over the past 50 years many different species have been administered the mark test, but only a handful have passed it. Some have suggested that species that pass the mark test are those that have a complex social structure. In this review, we propose, rather, that the reason why an animal fails the mark test is because the study has failed to adequately account for one or more of three crucial elements: mirror understanding, self-exploration, and mark saliency. Alternative methods of validating mirror self-recognition also are discussed.
An evolutionary view of self-awareness
2022, Behavioural Processes
Citation Excerpt :
Just as there is evidence suggesting that some species pass the MSR test, there is also evidence showing that other species, in addition to not passing the test, also do not display other forms of mirror-directed behavior, e.g. contingency checking. Remarkably, some of these animals can be regarded as being cognitively complex, including gibbons (Hyatt, 1998; Suddendorf and Collier-Baker, 2009), giant pandas (Ma et al., 2015), and California sea lions (Delfour and Marten, 2001). Moreover, as opposed to their pigeon and crow counterparts, great tits (Kraft et al., 2017), jungle crows (Kusayama et al., 2000), New Caledonian crows (Medina et al., 2011), Carrion crows (Brecht et al., 2020), Azure-winged magpies (Wang et al., 2020), keas, and Goffin’s cockatoos (van Buuren et al., 2019) also present with a lack of mirror-directed behaviors.
The capacity to be self-aware is regarded as a fundamental difference between humans and other species. However, growing evidence challenges this notion, indicating that many animals show complex signs and behaviors that are consonant with self-awareness. In this review, we suggest that many animals are indeed self-aware, but that the complexity of this process differs among species. We discuss this topic by addressing several different questions regarding self-awareness: what is self-awareness, how has self-awareness been studied experimentally, which species may be self-aware, what are its potential adaptive advantages. We conclude by proposing alternative models for the emergence of self-awareness in relation to species evolutionary paths, indicating future research questions to advance this field further.
Mirror responses in the common hill myna (Gracula religiosa) and the African grey parrot (Psittacus erithacus)
2021, Zoology
Scientists have spent great efforts exploring self-recognition in non-human animals using the mirror test. In avian species, some of the passerines have passed the test, although the findings are still under debate. The present study aimed at investigating mirror self-recognition ability and making a comparative study of mirror responses in two avian species, the common hill myna from the Passeriformes and the African grey parrot from the Psittaciformes. The subjects underwent four stages of experiment: habituation, baseline, mirror exposure and mark test. Our subjects spent significantly longer time in gazing into the mirror than the plexiglass as control. We also found they significantly increased the durations of grooming behaviour when presented with the mirror. No species difference was detected in the above two behaviours. However, the African grey parrots were more likely to approach the mirror than the common hill mynas, indicating their different ways of mirror exploration. All subjects failed to pass the mark test. In this study, we found no evidence of mirror self-recognition in the common hill myna and the African grey parrot.
The harmful effects of captivity and chronic stress on the well-being of orcas (Orcinus orca)
2020, Journal of Veterinary Behavior
Citation Excerpt :
Another is mirror self-recognition, that is, the ability to use a mirror to investigate one's own body. In a study of their responses to mirrors, orcas show contingency checking behavior—a correlate of self-directed responses exhibited by most individuals who demonstrate mirror self-recognition (Delfour and Marten, 2001). Observations of orcas reveal that they experience deep emotions and strong social attachments.
Orcas are large, deep-diving cetaceans who are known for their global distribution, wide-ranging behavior, intelligence, and social complexity. They possess one of the largest and most complex brains in the mammalian kingdom. However, they are the third most common species of cetaceans kept in aquariums and marine theme parks. Most spend many years, and sometimes decades, in captivity. At the time of writing, 60 individuals are held in concrete tanks globally. The scientific data on how both wild-caught and captive-born orcas fare in captivity are increasingly robust in demonstrating that they cannot thrive under artificial circumstances in concrete tanks. In captivity, orcas exhibit a wide range of abnormal behaviors and often die at an early age from infections and other health conditions that are uncommon in a wild setting. Though numerous papers and reports describe these adverse effects, they do not offer a clear and systematic explanation for why captive orcas suffer chronic stress and how it affects their well-being. We describe likely mechanisms for the high levels of morbidity and mortality in captive orcas, including the impact of chronic stress on physiology and illness. We conclude that orcas are poor candidates for maintenance in captivity and suggest that a radical shift is required in their treatment, to meet their complex needs.
What’s at Play: Humpback Whale Interaction with Seaweed Is a Global Phenomenon
2023, Journal of Marine Science and Engineering
Sociality and self-awareness in animals
2023, Frontiers in Psychology

View all citing articles on Scopus

View full text

Mirror image processing in three marine mammal species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus)

Abstract

Introduction

Section snippets

Mirror experiment on killer whales (Orcinus orca)

Killer whale behaviour

Discussion

Conclusion

Acknowledgements

New Ideas Psychol.

Conscious. Cogn.

Conscious. Cogn.

Conscious. Cogn.

New Ideas Psychol.

New Ideas Psychol.

Conscious. Cogn.

Observational study of behavior: sampling methods

Behaviour

The development of self-recognition: a review

Dev. Psychol.

Monkeys with mirrors: some questions for primate psychology

Int. J. Primatol.

Self-recognition in dolphins: credible cetaceans; compromised criteria, controls and conclusions

Conscious. Cogn.

Habitat use patterns and ranges of the Bottlenose dolphin in the Gulf of California, Mexico

Mar. Mammal Sci.