Brains, Behaviour and Intelligence in Cetaceans
(Whales, Dolphins and Porpoises)

Introduction
It is widely believed that cetaceans (the whales, dolphins and porpoises) are highly "intelligent". Probably the major historical basis for this dogma is the size and complex surface appearance of cetacean brains (Figure 1 ). The idea that brain size and surface characteristics are related to "intelligence" was widespread among neuroanatomists around the turn of the century, but received a severe blow when it was found that the brains of several distinguished people (who had bequeathed their bodies to science) showed no outstanding characteristics whatever and were, in fact, disappointingly ordinary (Kuhlenbeck,1978). This was just as well, as elements of such work were being badly misused to justify repressive racist, anti- feminist and colonial attitudes. The subject remained generally out of fashion until John Lilly, a medical doctor by training, became impressed by the absolute size of cetacean brains. His famous book "Mind in the Waters" (Lilly,1967) appears to have led to much of the modern interest in this topic.We all know in a general way what we mean by "intelligence" but unfortunately, it is so difficult to define strictly that, even when it comes to devising comparative tests for humans, all kinds of problems arise. The problems in defining "intelligence" in such a way that valid comparisons can be made across a wide of range of species have yet to be overcome, although this has not deterred a great deal of research into the subject.

Brain Quantity
If "intelligence" was simply determined by absolute brain size, there would be no difficulty in deciding which species was top (Table 1 ).

Table 1. Approximate brain weights and body weights of some mammals, 
in order of brain weight.

Species              Brain Weight   Body Weight
                     (approx.)      (approx.)
                     grams          tonnes
sperm whale (male)     7,820        37.00
African elephant       7,500        5.00
fin whale              6,930        90.00
killer whale           5,620        6.00
bottlenose dolphin     1,600        0.17
human                  1,500        0.07
cow                    500          0.6


But as the species with the biggest brains also tend to be the ones with the biggest bodies, it might be that large animals just need larger brains to control and maintain their larger bodies. Even when we talk of "intelligence" in a general way, we mean something more than the sum of body control systems. A simple way to make allowance for different body weights is to express brain weight as a percentage of body weight (Table 2).

Table 2. Approximate brain weights as a percentage of
approximate body weights of some mammals.

Species              Brain Weight as % of Body Weight
human                2.10
bottlenose dolphin   0.94
African elephant     0.15
killer whale         0.09
cow                  0.08
sperm whale (male)   0.02
fin whale            0.01

In this list humans are seen to have a great advantage over the others, and we also have a very different view of the large whales. Of course, these are only very limited lists to illustrate this type of approach to the problem.

Researchers have made far more extensive and sophisticated attempts to investigate comparative intelligence in this way. There is, however, a basic problem in compiling lists of this type, and that is deciding which weights to take as typical of a species. For example, normal humans can have brains weighing anything between 900 and 2,000 grams. The weight of an individual brain will also vary depending on whether it is fresh or preserved, and on exactly which parts are included. Body weight varies greatly between individuals, and i n some whale species the weight of individual animals can vary by about 40% over a year because of their seasonal feeding habits. The brain weight to body weight relation- ship varies with age young mammals have proportionally smaller bodies and larger heads, and brain size decreases significantly in old age. There can be marked sex differences in body size, for example adult female baleen whales in many species are much larger than males, while in sperm whales it is the adult males which are much larger than the females. Normal variations in brain and body size have only been well studied in a, few species, and usually a researcher seeking to compile extensive brain and body weight lists has no choice but to take whatever specimens are available, regardless of whether the material is really representative of the species as a whole.

Some of the most extensive modern comparative studies have been made by Jerison (e.g.1978), who has developed an index, the encephalization quotient (EQ), to express the brain weight/body weight relationship. His studies do show some cetaceans (e.g. toothed whales like the killer whale and sperm whale) with an EQ similar to humans. However, other studies conclude that relative brain size is not necessarily related to "intelligence". Pilleri, Gihr and Kraus (1985) made an exhaustive study of rodent brain size in relation to behaviour and concluded that "intelligence", whether human or animal, is not a unified brain function, but one which is too complex to be characterised with a single numerical index. They found that cerebral quotients (various ways of expressing relative brain and body size) are generally inconclusive as criteria for mammalian "intelligence".

Macphail (1982), in an extensive review of brain and behaviour in vertebrates, also found that brain size and characteristics were unsatisfactory indicators of "intelligence", because there are too many anomalies. A particular example is the spiny anteater (an egg laying mammal, related to the duck-billed platypus), with a neocortex (the so-cal led 'modern' part of the brain, which is greatly developed i n primates and humans) relatively much larger than that of a human. Despite this endowment, nobody has so far put forward any claims for superior "intelligence" in spiny anteaters.

Another problem with the search for a comparative measure of "intelligence" through brain quantity is addressed in the volume edited by Hahn, Jensen and Dudek (1979). Although a number of the papers deal with laboratory species selected and bred for increased brain size, there is extraordinary difficuIty in demonstrating any improvement in performance on a variety of tests either within or between species.

The degree of convolution or folding of the cortical brain surface has often in the past been taken as an absolute indicator of "intelligence". However, more recent work regards this as simply a mechanical reflection of an increase in neocortical volume. Jerison (1979), for example, regards degree of convolution and absolute brain size as equivalent measures, speculating that the extra volume is required to accommodate increasingly complex connections between the brain cells. Ridgway (1986) presents evidence from a variety of sources to show that bottlenose dolphins have a much higher index of folding than humans. However, as Ridgway (1986) also explains, the neocortex of the cetacean brain is relatively thin - about half that of humans - giving a total average dolphin neocortical volume about 80% of that of humans. Also, as explained in more detail below, cetacean neocortical structure is generally very much simpler than that of land mammals, and does not therefore conform to the assumptions that more convoluted neocortices are necessarily more voluminous or more complex. This is not the only anomaly, for example compare the convoluted appearances of the horse and chimpanzee brains.

Brain Quality
Another school of thought (e.g. Holloway,1979), finds the consideration of brain and body sizes alone insufficient, indeed "trivial", and emphasises the importance of the evolutionary changes in brain organisation. Holloway (1979) goes on to demonstrate that brain weight is a poor predictor of the internal structural complexity which he believes to be the most important factor in the evolution of "intelligence".

Studies of the internal structure of carefully preserved dolphin brains using a variety of techniques (e.g. Kesarev, Malofeyeva and Trykova, 1977; Morgane, Jacobs and Galaburda, 1986; Garey and Revishchin, 1990; Glazer, Morgane and Leranth, 1990) show that these animals have not developed the latest stage of brain evolution, characteristic of land mammals. It is thought that this line of evolution began about 50 million years ago in land mammals, whereas the cetacean ancestors returned to the water some 70 million years ago, well before this stage was reached. Although the cetacean brain has not followed the course of evolution of the land mammals, it does retain all the conservative characteristics seen in primitive land forms, such as hedgehogs and bats. The dolphin brain shows none of the anatomical structural heterogeneity characteristic of more evolved brains such as those of primates, but the regions of the neocortex can be differentiated by electrophysiological methods, and are arranged in very much the same order as in the hypothetical ancestor of mammals (Supin, Mukhametov, Ladygina, Popov, Mass and Poliakova, 1978).

The neocortex is the part of the brain which most clearly differentiates mammals from non-mammals, and there is a wide belief that the growth of the neocortex is responsible for the evolution of "intelligence". The anatomical characteristics of mammalian neocortex are that it has six layers and that different functional areas (e.g. that dealing with vision) have somewhat different organisation of these layers. The anatomical studies cited above demonstrate that cetaceans only have five layers in the neocortex (layer IV is missing) and that there is no anatomically different organisation of these Iayers according to function. In some views (e.g. Kesarev et al.,1977) this means that cetaceans have no true neocortex, or only a preneocortex. If a neocortex is really essential for the development of "intelligence", cetaceans are clearly disqualified. However, Macphail (1982) comprehensively demolishes the idea of a special role for the neocortex in "intelligence".

Behaviour
Yet another school of thought believes that the significance of the relative size or structural complexity of brains needs to be validated by behavioural data before any assumptions can be made about their role in the development of "intelligence". While a variety of laboratory tasks have been used, that of learning set formation (the inter-problem improvement in performance seen in subjects given a series of discriminations involving different pairs of stimuli) has been widely explored since Harlow (1949) concluded that the results reflected evolutionary relationships.

Unfortunately, subsequent work showed that closely related species may have widely divergent performances, and that some "lower" species may equal or excel "higher" species. Further , the ordering of species does not agree with that predicted from relative brain size (EQ) (Table 3).

Table 3. Learning set formation (data from various sources
cited by Macphail,1982)

Species           Score %  Encephalization  Order
                 (trial2)  Quotient (EQ)
langur               98    1.29             primate
mink                 95    ? (1-1.5)*       carnivore
ferret               90    ? (1-1.5)*       carnivore
bottlenose dolphin   87    5.31             cetacean
rhesus monkey        86    2.09             primate
cat                  70    1.71             carnivore
rat                  60    0.40             rodent
squirrel             60    1.10             rodent

* exact EQ not available, and these species have been given
the general carnivore EQ range

Macphail (1982) remarks that it is not clear that any of the differences in performance in learning set formation (or any of the other types of behavioural studies considered) observed are due to differences in intellectual capacity, and he cites a number of studies which demonstrate, as might be expected, that relative species performance is very dependent on detaiIs of experimental technique.

While all non-human animals have ways of communicating with each other, for example by body language, sounds, touch or chemicals, they have not developed anything of comparable versatility to human language. Although many attempts have been made, no non-human has yet been taught more than the rudiments of human-type language. Macphail (1982) describes the experiments and species (chimpanzee, gorilla, bottlenose dolphin, California sea lion, pigeon) concerned, and argues that such performances to date are better described as ordering responses sequentially for reward, rather than as real steps on the road to language. He also puts forward an interesting interpretation of the human capacity for problem solving, which is quite beyond the capacity of any non-human. If humans solve problems, directly or indirectly, with the aid of language, the superiority of humans in problem solving might simply reflect the possession of language, and the capacity for language, in turn might be a species-specific specialisation, independent of general "intelligence".

Discussion
Clearly, the cetacean type of mammalian brain is sufficient for the purpose, but it is anatomically simple and lacks the new structures which are conventionally associated with the development of "intelligence" among land mammals. However, as we have seen, there are good reasons for questioning these conventions.

Dolphin brains are relatively large, but again there are reasons for questioning the assumption that brain size is related to "intelligence". Crick and Mitchison's (1983) theory of the function of dream sleep may provide an alternative explanation for such anomalously large brains. They propose that rapid-eye-movement sleep (REM or dream or paradoxical sleep) acts to remove undesirable interactions in networks of cells in the cerebral cortex. They call this process, which is the opposite of learning, but different from forgetting, "reverse learning". Animals which cannot use this system need another way to avoid overloading the neural network, for example by having bigger brains. The spiny anteater and dolphins are the only mammals so far tested which do not have REM sleep (Allison, Van Twyner and Goff, 1972; Mukhametov, 1984) - and they also have disproportionally large brains. So, following this line of reasoning, dolphins and spiny anteaters would have to have big brains because they cannot dream.

The behaviour of dolphins is frequently cited as evidence for high "intelligence". The capacity of some smaller cetacean species (not all see Defran and Pryor, 1980) to learn performance tricks in captivity is often taken as "proof" of cetacean intelligence, but many other animals from elephants to fleas can achieve such feats, without this being taken as evidence for a special order of "intelligence". People who have been in close contact with dolphins and whales often speak of a feeling that they are with an "intelligent" animal , but many dog-owners, for example, have a close rapport with their pets and also speak of "intelligence" and an ability to "understand every word I say". The complexity of cetacean societies is another point frequently cited, but ants and bees, for example, have indisputably complex societies and we do not usually acknowledge these creatures as highly "intelligent". What about the cetacean's "sophisticated communication abilities"? We still know very little about the social significance of many of their sounds (excluding echo-location, which is only an aid for hunting and exploring the environment), body language and other communication systems, but in general the repertoire is far too limited to provide anything like our kind of "language". Experiments have shown that some dolphins may have the rudimentary skills necessary for understanding and use of language, but these skills seem fairly common, and have so far been found in a range of species including pigeons, pinnipeds and apes. Again, what could be more "sophisticated" than the multiple communication systems of bees? And how do we usually regard bees?

Friendliness and helpfulness towards people are often discussed, but are we flattering ourselves in believing that the animals really "intended" to help? For perhaps obvious reasons we hear less of unhelpful behaviour, but there are well- documented cases. Many species of wild animals have been tamed or habituated to humans. Sometimes such animals become a danger to themselves or to people. Even tamed wild dolphins can become a considerable nuisance (for example setting boats adrift by pulIing up anchors) and sometimes dangerous. Instancesof "friendly" dolphins attacking swimmers (apparently unprovoked) are well documented, as are instances of swimmers being pushed out to sea, "abducted" or prevented from re-entering boats and other craft (e.g. Lockyer,1990).

Gaskin (1982) has concluded that there is abundant evidence that cetaceans communicate information about "what", "where" and "who". There is no substantive evidence that they transmit information about "when", "how" or "why". So with respect to Kipling's (1902) "six honest serving men" of learning and intellect, cetaceans appear to be three servants short.

Conclusion
There is another less anthropomorphic or "speciesist" way of looking at the question of general "intelligence". All living species must be highly "intelligent" in a broad sense in order to survive. From this point of view, humans are no more and no less than one of the species living on this planet with particular adaptations (specialised "intelligence") for their own way of life. This perspective allows us to view the superb professionalism of all species with equal respect, and not in some artificial ranking order of higher or lower "intelligence" (with the hidden assumption that they are more or less worthy of conservation and consideration, and that as humans are, of course, in the first rank, their wishes have priority).

Dawkins (1980) recognises that suffering in animals may be difficult to measure and that misinterpretations of the meaning of animal behaviour can arise from projecting human feelings on to animals. Being "human-like" or "higher" or "more intelligent" is considered a poor guide to whether an animal experiences suffering. Behavioural and physiological evidence are more reliable and, taken together with information on the treatment of the animals, the situation can be evaluated. Without this basic preparation, suffering may be seen where there is none or, worse, may be overlooked because it does not wear a human face.

Thus, while it is not yet possible to make any final scientific judgements on cetacean "intelligence", there are sufficient doubts to render the unqual ified perpetuation of the dogma highly questionable - and possibly even counter- productive in the wider conservation and animal welfare context.

References:
* Allison, T., Van Twyner, H. and Goff W.H. (1972). Electrophysiological studies of the echidna, Tachyglossus aculeatus. /. Waking and sleep. Arch. ital. biol. 110: 145-184.
* Crick, F. and Mitchison, G. (1983). The function of dream sleep. Nature 304: 111-114. Dawkins, M.S.(1980). Animal Suffering. Chapman and Hall, London. 1980
* Defran, R.H. and Pryor, K. (1980). The behaviour and training of cetaceans in captivity. p. 319-362. In: L.M. Herman (Ed.) Cetacean Behaviour: Mechanisms and Functions. John Wiley and Sons, New York. 463 pp.
* Garey, L.J. and Revishchin, A. V. (1990). Structure and thalamocortical relations of the cetacean sensory cortex: histological, tracerand immun-ocyto-chemical studies. p.19-30 In: J.A. Thomas and R.A. Kastelein (Eds) Sensory Abilities of Cetaceans: Laboratory and Field Evidence. Plenum Press, New York. 710 pp.
* Gaskin, D.E. (1982). The Ecology of Whales and Dolphins. Honeymoon, London. 459 pp.
* Glazer, I.I., Morgane, P.J. and Leranth, G (1990). Immunocytochemistry of neurotransmitters in visual neocortex of several toothed whales: light and electron microscope study. p. 39-66 In: J.A. Thomas and R.A. Kastelein (Eds) Sensory Abilities of Cetaceans: Laboratory and Field Evidence. Plenum Press, New York. 710 pp.
* Hahn, M.E., Jensen, C. and Dudek, B.C. (Eds) (1979). Development and Evolution of Brain Size. Behavioral Implications. Academic Press, New York. 393pp.
* Harlow, H.F. (1949). The formation of learning sets. Psychol. Rev. 56: 51-65.
* Holloway, R.L. (1979). Brain size, allometry and reorganization: toward a synthesis. p. 59-88. In: Hahn,M.E,
* Jensen, C. and Dudek, B.C. (Eds) Development and Evolution of Brain Size. Behavioral Implications. Academic Press, New York. 393 pp. Jerison, H.J. (1978). Brain and intelligence in whales. p.159-197. In: Whales and Whaling. Australian Government Publishing Service, Canberra. Vol. 2. 219 pp.
* Jerison, H.J. (1979) The evolution of diversity in brain size. p. 29-57. In: Hahn, M.E., Jensen, C. and Dudek, B.C. (Eds) Development and Evolution of Brain Size. Behavioral Implications. Academic Press, New York. 393 pp.
* Kesarev, V.S., Malofeyeva, L.I. and Trykova, O. V. (1977). Ecological specificity of cetacean neocortex.J. Hirnforsch. 18: 447-460.
* Kipling, R. (1902). Just-So Stories Macmillan and Co. Ltd., London.
* Kuhlenbeck, H. (1978). The Central Nervous System of Vertebrates. Vol. 5: Part II. Mammalian Telencephalon: Surface Morphology and Cerebral Cortex The Vertebrate Neuroaxis as a Whole. Karger,Basle. 636 pp.
* Lilly, J.C. (1967). The Mind of the Dolphin. Doubleday, New York.
* Lockyer, C. (1990). Review of incidents involving wild, sociable dolphins, worldwide. p. 337-353 In: S. Leather-wood and R.R. Reeves (Eds) The Bottlenose Dolphin. Academic Press, San Diego. 653 pp.
* Macphail, E.M. (1982). Brain and Intelligence in Vertebrates. Clarendon Press, Oxford. 433 pp.
* Morgane, P.J., Jacobs, M.S. and Galaburda, A. (1986). Evolutionary morphology of the dolphin brain. p. 529. In: Schusterman, R.J., Thomas, J.A. and Wood, F.G. (Eds) Dolphin Cognition and Behaviour: A Comparative Approach. Lawrence Erlbaum and Associates, London. 393 pp.
* Mukhametov, L.M. (1984). Sleep in marine mammals. p. 227-237. In: A. Borbely and J-L. Valatax (Eds) Sleep Mechanisms. Experimental Brain Research. Suppl. 8. Springer-Verlag, Berlin.
* Pilleri, G., Gihr, M. and Kraus, C. (1985). Cephalization in rodents with particular reference to the Canadian beaver (Castorcanadensis). p.11-102. In: G. Pilleri (Ed.) Investigations on Beavers IV. Berne, Switzerland.
* Ridgway, S.H. (1986). Dolphin brain size. p. 59-70 In: M.M. Bryden and R.J. Harrison (Eds) Research on Dolphins. Clarendon Press, Oxford. 478 pp.
* Supin, A. Ya., Mukhametov, L.M., Ladygina, T.F., Popov, V V., Mass, A.M. and Poliakova, /.G. (1978). Electro-physiological Investigation of the Dolphin Brain. Nauka, Moscow. 213 pp.