ArticlePDF Available

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

Authors:

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.
... A final way sufficient mirror exposure can be confirmed is through the emergence of contingent body movements, which includes repetitive or unusual body movements only witnessed when the animal is in front of a mirror. These movements are believed to reflect animals testing the contingency between their body movements and their mirror reflection, suggesting an understanding of how a mirror works (Delfour & Marten, 2001, Cammaerts & Cammaerts, 2015, Ari & D'Agostino, 2016, Morrison & Reiss, 2018. Prior et al. (2008) gave European magpies 150 min of mirror exposure. ...
... 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. ...
... In our review we have outlined alternatives to the mark test, such as peculiar behaviour that an animal may exhibit in front of the mirror. An elephant using a mirror to monitor its body and correct its position (Povinelli, 1989), a whale using a mirror to look inside its mouth (Delfour & Marten, 2001), a monkey using a mirror to inspect a strange device implanted on its head (Rajala et al., 2010), or the numerous other instances of contingency checking such as inspection of their anal-genital region (Chang et al., 2015;Gallup, 1970;Hauser et al., 1995;Rajala et al., 2010), are no less indicators of self-recognition than the mark test. ...
... A final way sufficient mirror exposure can be confirmed is through the emergence of contingent body movements, which includes repetitive or unusual body movements only witnessed when the animal is in front of a mirror. These movements are believed to reflect animals testing the contingency between their body movements and their mirror reflection, suggesting an understanding of how a mirror works (Delfour & Marten, 2001, Cammaerts & Cammaerts, 2015, Ari & D'Agostino, 2016, Morrison & Reiss, 2018. Prior et al. (2008) gave European magpies 150 min of mirror exposure. ...
... 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. ...
... In our review we have outlined alternatives to the mark test, such as peculiar behaviour that an animal may exhibit in front of the mirror. An elephant using a mirror to monitor its body and correct its position (Povinelli, 1989), a whale using a mirror to look inside its mouth (Delfour & Marten, 2001), a monkey using a mirror to inspect a strange device implanted on its head (Rajala et al., 2010), or the numerous other instances of contingency checking such as inspection of their anal-genital region (Chang et al., 2015;Gallup, 1970;Hauser et al., 1995;Rajala et al., 2010), are no less indicators of self-recognition than the mark test. ...
Article
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.
... Still, species that do not pass the MSR test per se, may show different behaviors in front of a mirror, such as contingency checking (moving body parts to check if the same movement is also happening in the mirror), frequent observation of the reflection, and others. This was shown in killer whales, false killer whales (Delfour and Marten, 2001), manta-rays (Ari and D'Agostino, 2016), and rats (Yakura et al., 2018). Additionally, a pilot study with horses showed that some animals could at least recognize that the mirror image was not real (Baragli et al., 2017). ...
... 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. ...
Article
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 selfaware, but that the complexity of this process differs among species. We discuss this topic by addressing several different questions regarding self-awareness: what is selfawareness, 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.
... The mark test has been broadly used to study the phylogenetic distribution of mirror self-recognition and selfawareness in mammals (i.e., elephants (Plotnik et al. 2006), horses (Baragli et al. 2017), pandas (Ma et al. 2015), marine mammals (Delfour and Marten 2001;Reiss and Marino 2001), primates (Paukner et al. 2004;Roma et al. 2007;Suddendorf and Collier-Baker 2009;Chang et al. 2015)), fish (cichlids: Hotta et al. 2017, mantas: Ari and D'Agostino 2016, cleaner wrasses: Kohda et al. 2019Kohda et al. , 2022, birds (see Brecht et al. (2020) for review), and invertebrates (squids: Ikeda andMatsumoto 2007, ants: Cammaerts andCammaerts 2015). Despite being debated (Anderson and Gallup 2015;Anderson 2018, 2020), these studies show that this ability evolved independently in great apes (humans (Amsterdam 1972), chimpanzees (Gallup 1970;Povinelli et al. 1997), bonobos (Westergaard and Hyatt 1994;Walraven et al. 1995), orangutans (Lethmate and Dücker 1973;Suarez and Gallup 1981;Miles 1994), gorillas (Patterson and Cohn 1981;Parker et al. 1994;Posada and Colell 2007)), dolphins (Reiss and Marino 2001;Morrison and Reiss 2018), elephants (Plotnik et al. 2006), cleaner wrasses (Kohda et al. 2019(Kohda et al. , 2022, two corvid species (i.e., Eurasian magpies (Prior et al. 2008), and Indian house crows (Buniyaadi et al. 2020)). ...
Article
Full-text available
Mirror self-recognition (MSR) assessed by the Mark Test has been the staple test for the study of animal self-awareness. When tested in this paradigm, corvid species return discrepant results, with only the Eurasian magpies and the Indian house crow successfully passing the test so far, whereas multiple other corvid species fail. The lack of replicability of these positive results and the large divergence in applied methodologies calls into question whether the observed differences are in fact phylogenetic or methodological, and, if so, which factors facilitate the expression of MSR in some corvids. In this study, we (1) present new results on the self-recognition abilities of common ravens, (2) replicate results of azure-winged magpies, and (3) compare the mirror responses and performances in the mark test of these two corvid species with a third corvid species: carrion crows, previously tested following the same experimental procedure. Our results show interspecies differences in the approach of and the response to the mirror during the mirror exposure phase of the experiment as well as in the subsequent mark test. However, the performances of these species in the Mark Test do not provide any evidence for their ability of self-recognition. Our results add to the ongoing discussion about the convergent evolution of MSR and we advocate for consistent methodologies and procedures in comparing this ability across species to advance this discussion.
... The mirror test is the most representative test of social cognition. Only a few animals passed the test, including chimpanzees [138], orangutans [139], bonobos [140], gorillas [141], [142], Asiatic elephant [143], dolphins [144], orcas [145], macaque monkeys [146], etc. Based on the mirror test, we proposed the Multi-Robots Mirror Self-Recognition Test [34], in which three robots with identical appearance move their arms randomly in front of the mirror at the same time, and each robot needs to determine which mirror image belongs to it. ...
Preprint
Full-text available
Spiking neural networks (SNNs) have attracted extensive attentions in Brain-inspired Artificial Intelligence and computational neuroscience. They can be used to simulate biological information processing in the brain at multiple scales. More importantly, SNNs serve as an appropriate level of abstraction to bring inspirations from brain and cognition to Artificial Intelligence. In this paper, we present the Brain-inspired Cognitive Intelligence Engine (BrainCog) for creating brain-inspired AI and brain simulation models. BrainCog incorporates different types of spiking neuron models, learning rules, brain areas, etc., as essential modules provided by the platform. Based on these easy-to-use modules, BrainCog supports various brain-inspired cognitive functions, including Perception and Learning, Decision Making, Knowledge Representation and Reasoning, Motor Control, and Social Cognition. These brain-inspired AI models have been effectively validated on various supervised, unsupervised, and reinforcement learning tasks, and they can be used to enable AI models to be with multiple brain-inspired cognitive functions. For brain simulation, BrainCog realizes the function simulation of decision-making, working memory, the structure simulation of the Neural Circuit, and whole brain structure simulation of Mouse brain, Macaque brain, and Human brain. An AI engine named BORN is developed based on BrainCog, and it demonstrates how the components of BrainCog can be integrated and used to build AI models and applications. To enable the scientific quest to decode the nature of biological intelligence and create AI, BrainCog aims to provide essential and easy-to-use building blocks, and infrastructural support to develop brain-inspired spiking neural network based AI, and to simulate the cognitive brains at multiple scales. The online repository of BrainCog can be found at https://github.com/braincog-x.
... The fact that cetacean relative brain sizes approach those of humans has sparked both scientific and public interest in understanding the cetacean brain, with much attention being given to the selection pressures that lead to, and the implications of, the high EQ values observed in the toothed whales (Odontoceti). The high EQs of cetaceans have been attributed to the need of cetaceans for expanded cognitive abilities [10,[13][14][15]; their complex social structure [16,17]; their sophisticated echolocation system [7,[18][19][20][21]; their diet [22], and even their thermoregulatory needs [23,24]. Intriguingly, living cetaceans include not only species with high EQ values, particularly the delphinoid odontocetes, but also include species with some of the lowest mammalian EQs such as the balaenid mysticetes [11]. ...
Article
Full-text available
Most authors have identified two rapid increases in relative brain size (encephalization quotient, EQ) in cetacean evolution: first at the origin of the modern suborders (odontocetes and mysticetes) around the Eocene-Oligocene transition, and a second at the origin of the delphinoid odontocetes during the middle Miocene. We explore how methods used to estimate brain and body mass alter this perceived timing and rate of cetacean EQ evolution. We provide new data on modern mammals (mysticetes, odontocetes, and terrestrial artiodactyls) and show that brain mass and endocranial volume scale allometrically, and that endocranial volume is not a direct proxy for brain mass. We demonstrate that inconsistencies in the methods used to estimate body size across the Eocene-Oligocene boundary have caused a spurious pattern in earlier relative brain size studies. Instead, we employ a single method, using occipital condyle width as a skeletal proxy for body mass using a new dataset of extant cetaceans, to clarify this pattern. We suggest that cetacean relative brain size is most accurately portrayed using EQs based on the scaling coefficients as observed in the closely related terrestrial artiodactyls. Finally, we include additional data for an Eocene whale, raising the sample size of Eocene archaeocetes to seven. Our analysis of fossil cetacean EQ is different from previous works which had shown that a sudden increase in EQ coincided with the origin of odontocetes at the Eocene-Oligocene boundary. Instead, our data show that brain size increased at the origin of basilosaurids, 5 million years before the Eocene-Oligocene transition, and we do not observe a significant increase in relative brain size at the origin of odontocetes.
Book
What is a self? What does it mean to have selfhood? What is the relationship between selfhood and identity? These are puzzling questions that philosophers, psychologists, social scientists, and many other researchers often grapple with. Self and Identity is a book that explores and brings together relevant ideas on selfhood and identity, while also helping to clarify some important and long standing scientific and philosophical debates. It will enable readers to understand the difference between selves in humans and other animals, and the different selves that we come to possess from when we are born to when we become old. It also explains how and why the self might break down due to mental illness, thereby providing insight into how we might treat illnesses such as dementia and depression, both of which are conditions that fundamentally affect our selfhood. Taking an important step towards clarifying our understanding of human selfhood and applying it to mental illness, this book will be of great interest to researchers and postgraduate students exploring philosophical questions of selfhood, as well as those examining the connection to clinical disorders.
Chapter
CetaceanCetacea/cetaceans minds have been the topic of intense scientific interest for decades, and our continued study of them takes us on a complicated journey that requires us to regard cetacean brainsBrain and behavior as simultaneously very different and very familiar to us. Cetacean brains have undergone one of the most dramatic transformations during their evolutionEvolution from terrestrial animals to the highly acoustic and socially sophisticated animals we know today. Their brains are a challenging combination of highly conserved mammalian characteristics along with a unique neocortical organization that suggests that it processes information through alternative neural strategies to those of the primate brain. Their sensorium and perceptual capacities, especially in the realm of communicationCommunication, are unusual even for a fully aquatic mammal. Their cognitive and social capacities make it clear that there are striking convergences in psychology between cetaceansCetacea/cetaceans and many terrestrial carnivores as well as primates such as we are, including the reliance on strong social bondsSocial bonds and, in many cases, culturalCultural traditions.
Thesis
Whales have become an important topic in marine science. One of the best solutions for their protection is a better understanding of their social structure and the way they communicate with each other. To this end, Underwater Passive Acoustics (UPA) offers a unique solution to simultaneously capture both source-specific and more contextual information, thus providing a better understanding of both the behavior of whales and their relationships with the ecosystem around them. As the volume of APSM data to be processed has become very large, the development of automated artificial intelligence (AI) methods to analyze this data is now of prime importance in marine bioacoustics. These rely heavily on the quantity and quality of the annotated data, which is the main limitation in their use. This work explores two approaches in a weakly supervised context, by acting or on the context itself, through the question of where and how one can better extract useful information to supervise AI methods; or by acting on AI methods in this context, through the question of how to develop AI methods to better respond to weak supervision. Our contribution has enabled the development of new tools to aid in the recognition of cetacean sounds through open science with the OsmOSE project, a collaborative and interdisciplinary project following the principles of Findable, Accessible, Interoperable and Reusable data.
Article
Full-text available
After prolonged exposure to their reflected images in mirrors, chimpanzees marked with red dye showed evidence of being able to recognize their own reflections. Monkeys did not appear to have this capacity.
Article
Full-text available
Evaluates the theories outlined by R. W. Mitchell (see record 1994-16947-001) to account for mirror self-recognition and corrects some misleading information in Mitchell's paper. Issues discussed include the need for controls, mirror correspondence, Mitchell's inductive and deductive models, mature vs immature self-recognition, self-awareness, and self-recognition and evidence of mental state attribution. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
Full-text available
To date humans, chimpanzees, and orangutans are the only species which have been shown capable of recognizing themselves in mirrors. Several species of macaques have now been provided with years of continuous exposure to mirrors, but they still persist in reacting to their reflection as if they were seeing other monkeys. Even gibbons (apes) and gorillas (great apes) seem incapable of learning that their behavior is the source of the behavior depicted in the image. Most primates, therefore, appear to lack a cognitive category for processing mirrored information about themselves. The implications of these data for traditional views of consciousness are considered briefly, and a recent attempt to develop an operant analog to self-recognition is critically evaluated. Finally, an attempt is made to show that self-awareness, consciousness, and mind are not mutually exclusive cognitive categories and that the emergence of self-awareness may be equivalent to the emergence of mind. Several indices of “mind” which can be applied to nonhuman species are discussed in the context of an attempt to develop a comparative psychology of mind.
Article
Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
Article
reports on the results of a series of studies utilizing a mirror to assess whether dolphins recognize contingent representations of themselves or use the mirror to examine an area of the body not otherwise visible that has been marked with a highly salient substance / devised and conducted several new tests for self-recognition, tailored for dolphins rather than primates [Ss were 5 dolphins, 6–14 yrs old, living at Sea Life Park] address the central question of whether the dolphins' mirror-directed behavior is social or self-examination / discuss the role of environmental, social, and individual influences on the test results (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
Describes a technique in which organisms are provided with extended exposure to mirrors and then given an explicit test of self-recognition (through the unobtrusive application of marks to facial features visually inaccessible without a mirror). Use of this procedure with chimpanzees and orangutans in a series of studies by the present author provided evidence of self-recognition, with patterns of self-directed behavior emerging after only 2–3 days. In support of the widely held view that the self-concept may develop out of social interaction with others, the capacity for self-recognition in chimpanzees appears to be influenced by early social experience. To date, however, attempts to demonstrate self-recognition in all other species except man have failed. The phyletic limits of this capacity may have important implications for claims concerning the evolutionary continuity of mental experience. (64 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
to date, the only species to show compelling evidence of self-recognition are humans, chimpanzees, and orangutans / an important question is whether self-awareness is a uniquely primate (great ape-human) ability or a potential outcome of any sufficiently intelligent system / in order to address this question . . . compare tests of self-awareness in primates with another taxonomic group that has diverged extensively from them yet displays a comparable level of neurobehavioral complexity, namely, the Cetacea describe the responses of 2 captive bottlenose dolphins with whom [the authors] attempted to replicate the mirror self-recognition paradigm originally applied to chimpanzees (Gallup, 1970) / [variables assessed are viewing time, specific responses to the mirror, and specific responses to the mark during the mark test] (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
New Zealand fur seals, Arctocephalus forsteri, breed in densely packed colonies where males hold exclusive territories. Both sexes overheat while on land and use shade and pools of water for cooling. In addition, females are aggressive towards one another and rarely tolerate neighbours closer than 1 m away. At a New Zealand colony of this species, agonistic interactions among females occurred most often in areas used for thermoregulation: shaded rock substrate and pools of water. Fewest interactions occurred in sunny, dry areas. These findings suggest that females are competing for a limited resource, which could limit harem size.