Neuroscience Forefront ReviewQuestioning the interpretations of behavioral observations of cetaceans: Is there really support for a special intellectual status for this mammalian order?
Introduction
Almost anywhere one looks regarding the “public face” of cognitive studies or behavioral observations relating to cetaceans (e.g. various internet sites, popular science books, ecotourism pamphlets, miracle cures for autism), they are virtually universally accepted as being indicative of high levels of intelligence. Cetaceans are commonly regarded as perhaps only second to Homo sapiens in general intellectual prowess, though some consider them far superior both intellectually and emotionally to humans (Fraser et al., 2006). This public leaning, while derived from mass media, ultimately originates from the scientific literature, in peer-reviewed journals, where assertions of undeniable intelligence appear regularly (e.g. Marino et al., 2007, Marino et al., 2008, Grimm, 2010, Herman, 2012). Three examples of this typology are: Tyack (2000), who states: “Dolphins are remarkably intelligent creatures…”; Reiss et al. (1997) who aver: “Reports of the cognitive achievements of bottlenose dolphins leave little doubt that they are intelligent animals.”; and Marino (2004) who asserts: “Like humans, dolphins are, without a doubt, brainiacs of the animal kingdom.” The word “brainiac” is the name of a super-intelligent alien character from the Superman comics – a blending of the words “brain” and “maniac”.
What these statements, published in well-respected peer-reviewed scientific journals, imply is that the species that comprise the order Cetacea hold a special place in the animal kingdom in terms of their intellectual capacity. But what is different? Is it the quantity or the quality of the intellect? Macphail (1996) has argued that it is yet to be proven that there are differences in the qualitative intellectual abilities of vertebrate species (except for human linguistic abilities), as when contextual ambiguities are removed from cognitive tests all species appear to perform equally well; but the statements made by those studying cetacean cognition clearly support the notion of a special status, both qualitatively and quantitatively, for the Cetacea (Reiss et al., 1997, Marino, 2002, Marino, 2004, Simmonds, 2006, Marino et al., 2007, Marino et al., 2008, Grimm, 2010, Herman, 2012). Perhaps the key central observation upon which the cognitive studies of cetaceans have been built is the absolute and relative size of the brain. Indeed, some cetaceans have a larger relative brain size than all other non-human animals, and some species, while having a low relative brain size, have the absolute largest brains on the planet (Pilleri and Gihr, 1970, Jerison, 1978, Marino, 1998, Manger, 2006). On the basis of Jerison’s hypothesis, that relative brain size (the encephalization quotient) is a proxy measure of biological intelligence (Jerison, 1973), the absolute and relative brain sizes of cetaceans is the most often cited basis for undertaking studies directed at revealing the potential cognitive abilities of dolphins and whales (e.g. Marino, 2002, Simmonds, 2006, Marino et al., 2007, Marino et al., 2008). But is this justified, and are the subsequent behavioral studies really supportive of the claims made? Are there perhaps simpler or alternative answers?
Previously (Manger, 2006), I outlined the anatomy of the cetacean brain, how the structure may relate to function on the basis of comparison to other mammals, and proposed a scenario for the evolution of the size of the cetacean brain related to thermogenesis as the selection pressure driving changes in both absolute and relative size, or encephalization. This hypothesis is at odds with previous concepts as the shackles of the “intelligence constraint” of cetacean brain size evolution were broken, and in fact much of the data outlined casts serious doubts over the “accepted wisdom” that cetaceans are undeniably intelligent. Despite this alternative hypothesis, several researchers are of the opinion that the observed behavior of cetaceans supports the concept of high levels of cognitive functioning (e.g. Simmonds, 2006, Connor, 2007, Marino et al., 2007, Marino et al., 2008, Herman, 2012), irrespective of what the anatomical data (which is far more difficult to misinterpret) indicate – the structure of the brain and how it works in other mammals is of no consequence, what is important is what we can infer about intelligence from cetacean behavioral studies. The present paper critically analyses the behavioral evidence that has been forwarded in support of apparent higher level cognitive abilities in cetaceans.
Section snippets
What does encephalization mean?
Encephalization is simply a measure of the size of the brain relative to the body; thus to determine how “encephalized” a particular animal is, the mass of the brain and the mass of the body is compared to the mass of the brain and body of a number of other species. Thus, a standard baseline is predetermined and the particular species is compared against that baseline. When “mammals” are used as a baseline (in this sense, mammals consists of those mammalian species not belonging to either the
When did cetacean brains become larger?
Data concerning the mass of the brain and body of cetaceans, and the timing of changes in absolute and relative size were provided by Marino et al. (2004) in a comprehensive study of fossil cetacean skulls. This database provides a strong basis from which to analyze changes in both absolute and relative brain sizes through cetacean evolutionary history (Marino et al., 2004, Manger, 2006, Manger et al., 2013). While data concerning brain and body mass of the last terrestrial and the semi-aquatic
Developing a model of cetacean encephalization – Where to start?
There are currently three proposals in the literature regarding the encephalization of cetaceans. The first that will not be discussed in detail here is the thermogenetic proposal (Manger, 2006). The second proposal indicates that the evolution of increased auditory capacities was accompanied by increased cognitive capacities, the auditory proposal (Ridgway and Au, 1999); and the third proposal is a somewhat diffuse and as yet unconsolidated proposal that I will term here the intellectual
An autocatalytic model of cetacean encephalization
Now that we have a starting point (32 m.y.a.) and the initial impetus (changing environment) for cetacean encephalization, with the intellectual proposal in mind we can develop a potential model that should provide the explanation for both the historical aspects of cetacean brain evolution and the currently observed purported “higher cognitive” behaviors. To do this I am adapting a model that has been proposed for evolution of the human brain, an autocatalytic model describing “Hominization” (
The features contributing to the autocatalytic model
In order for the autocatalytic model to be a realistic expression of what occurred during the process of cetacean encephalization, many, but not all, of the features incorporated into the model must first of all hold true under close scrutiny, i.e. are they really features that we can rely upon to construct this model? Second, in order for these features to be part of a mechanism driving the encephalization process they must also be either: (a) unique to cetaceans; or (b) be only found in
WHAT ABOUT THE ENTIRE SUITE OF BEHAVIORS?
The current review has specifically focussed on the behaviors that scientists who primarily study cetaceans claim to provide evidence of higher cognitive abilities associated with absolutely or relatively large brains (Simmonds, 2006, Connor, 2007, Marino et al., 2007, Marino et al., 2008, Herman, 2012). These behaviors are regularly cited as proof that cetaceans are more cognitively complex than other mammals, with it often being claimed that cetaceans are second only to humans in cognitive
WHAT CAN’T CETACEANS DO?
Much of this review has focussed on behaviors that cetaceans appear capable of performing; however, it is equally instructive to examine negative results when attempting to contextualize cetacean behavioral capabilities, but these are rarely reported. Here I describe two specific cases showing that cetaceans either fail, or compare badly, on specific cognitive tests when compared to apes and other species tested on the same cognitive task. The first cognitive test that shows cetaceans do not
CAN A SPECIAL INTELLECTUAL STATUS BE ASSIGNED TO CETACEANS?
In 2006 the author of this review published a manuscript that outlined a hypothesis for the evolution of relatively and absolutely large brain size in cetaceans that was not related to intellectual capacities (Manger, 2006). Unsurprisingly, given the existing view of cetaceans as intelligent beings (e.g. Reiss et al., 1997, Tyack, 2000, Marino, 2004), this review was met by vigorous and collaborative criticism (e.g. Connor, 2007, Marino et al., 2007, Marino et al., 2008, Herman, 2012). One of
Acknowledgments
P.R.M. would like to thank the National Research Foundation of South Africa for continued support of his research. I would also like to thank Muhammad Spocter for his help with the statistical aspects of the work reported in the current study and Nigel Bennett, Muhammad Spocter and Nina Patzke for reading and commenting on an earlier version of this manuscript.
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2023, Progress in Brain ResearchCitation Excerpt :It is always problematic to determine how intelligent, or behaviorally complex, an extant animal is, let alone how complex the behavior of an extinct animal may have been, but paleontologists do have some clues. Measurements of natural and artificial endocranial casts are used to calculate the encephalization quotient (Eisenberg, 1981; Jerison, 1973), which enables comparisons of relative brain size, although this is not necessarily a direct reflection of an animal's behavioral complexity (Healy and Rowe, 2007; Manger, 2006, 2013; Manger et al., 2013). More direct evidence of complex behavior can be found in exceptional cases of preservation in lagerstätten conditions, or can be proposed from the paleoneurological, functional anatomical, palaeopathological, and ichnology clues (Boucot, 1990; Boucot and Poinar, 2011).
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2018, Current BiologyCitation Excerpt :The loss of REM sleep for long periods of time in fur seals, or its complete absence in cetaceans is not incompatible with long lifespans and large brain size. Cetaceans have the largest brains and among the longest lifespans of any mammal [33] and are considered by some to rival primates in their complex cognition [34, 35]. Pathologies resulting from sleep deprivation in land mammals may be the result of stress induced by the sleep deprivation procedure, particularly the repeated awakenings, which may reach 1,000 a day, linked to the cortisol awakening response [6, 36, 37] and phasic changes in brain neuronal activity and neurochemistry, including monoamine release [2].
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2018, Seminars in Cell and Developmental BiologyCitation Excerpt :It was previously proposed that the large brain of cetaceans is a response to rapid cooling of oceanic temperatures during the evolution of the modern cetacean fauna [46], and the behavioral support for apparent cognitive sophistication in the cetaceans have been critically evaluated and found wanting [47]. The neuroanatomical [46,48] and behavioral reasons [47] most salient to rejecting the complex cognitive proposal of cetacean brain evolution were described and an alternative path to evolving a large mammalian brain was outlined Fig. 5. While all the details of the thermogenetic proposal are not fully fleshed out, the concept that a large brain can evolve in response to selection pressures other than a post-hoc interpretation of a need for greater cognitive complexity represents a novel path for understanding brain evolution across vertebrate species as it breaks the ideological shackles of large brains evolving only to enhance cognitive abilities.
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