Braininess in primates and other mammals, relevant to cognitive empathy and play behaviour

@botswanabugs @tonyrebelo @jeremygilmore @paradoxornithidae

In recent Posts, I have pointed out that baboons (Papio spp., https://en.wikipedia.org/wiki/Baboon) and other primates have surprisingly little cognitive empathy for animals with such large brains.

So, it may be worth quantifying just how large the brains of baboons really are. The same applies to other relevant animals that are capable of play behaviour during adulthood.

Encephalisation Quotient (EQ, https://en.wikipedia.org/wiki/Encephalization_quotient) is a quantitative expression of brain mass/volume relative to body mass, corrected allometrically. It provides the most basic parameter of braininess.

EQ can only really be compared within lineages. This is because the brains of e.g. birds vs mammals are too different to make their EQ values comparable.

The concept of EQ is mathematically simple. However, it is inevitable that various authors vary in how they calculate it, leading to considerable differences in the actual values among studies. Making comparisons within a given study mitigates this problem.

The following are some of the salient facts:

Gibbons (https://en.wikipedia.org/wiki/Gibbon) are much brainier than baboons, despite being incomparably less social.

Capuchin monkeys (https://en.wikipedia.org/wiki/Capuchin_monkey), which live in South America, are brainier than any ape. This is often overlooked, partly owing to the small body size of capuchins.

Baboons are by no means the brainiest of the Old World monkeys (https://en.wikipedia.org/wiki/Old_World_monkey). Their EQ is inferior to those of less gregarious relatives such as mangabeys (https://en.wikipedia.org/wiki/Mangabey) and the patas monkey (https://en.wikipedia.org/wiki/Common_patas_monkey).

Patas monkeys, in particular, show noteworthy braininess. This is consistent with their exceptional ability to survive, much as humans do, by their wits out in the open, in an environment replete with predators (https://en.wikipedia.org/wiki/Southern_patas_monkey).

The contrast in braininess between the patas monkey and e.g. the proboscis monkey (https://en.wikipedia.org/wiki/Proboscis_monkey) of Borneo (https://en.wikipedia.org/wiki/Borneo) is particular food for thought.

The following values for EQ are given by one study:

human (Homo sapiens) 7.4-7.8.

chimpanzee (Pan) 2.2-2.5

rhesus macaque (Macaca mulatta, https://en.wikipedia.org/wiki/Rhesus_macaque) 2.1

elephants (Loxodonta and Elephas) 1.13-2.36

horse (Equus caballus) 0.9
(also see https://www.researchgate.net/profile/Michele-Povinelli/publication/259319958_The_Brain_of_the_Horse_Weight_and_Cephalization_Quotients/links/59d48ef34585150177fc4da4/The-Brain-of-the-Horse-Weight-and-Cephalization-Quotients.pdf)

domestic sheep (Ovis aries) 0.8

My commentary:
Old World monkeys (here exemplified by the rhesus macaque) are less brainy than chimpanzees. However, the difference is not as great as many naturalists might suppose.

Ungulates (as represented by the horse and the domestic sheep) are far inferior to Old World monkeys, having EQ of <1, compared to the value of >2 for the rhesus macaque.

However, elephants are brainier than ungulates, having EQ of 1.1-2.4.

I do not know why the values for elephants show such a wide range. However, please note that the maximum value (2.36) is similar to that of chimpanzees. If we take the middle of the range for elephants (i.e. about 1.74), it is double the value for the domestic sheep and closer to the value for the rhesus macaque than to the values for the ungulates.

This shows that elephants are indeed brainy for non-primates.

According to a different study (check Schoenemann P T (2004) Brain size scaling and body composition in mammals. Brain Behavior Evolution 63, 47-60, https://pubmed.ncbi.nlm.nih.gov/14673198/ and https://brainevo.sitehost.iu.edu/publications/schoenemann.BBE.04.pdf and https://www.researchgate.net/publication/8961836_Brain_Size_Scaling_and_Body_Composition_in_Mammals):

human (Homo sapiens) 5.07

proboscis monkey (Nasalis larvatus) 1.11

olive colobus (Procolobus verus, https://en.wikipedia.org/wiki/Olive_colobus) 1.50

patas monkey (Erythrocebus patas) 1.93

gracile capuchin monkey (Cebus sp., https://en.wikipedia.org/wiki/Gracile_capuchin_monkey) 2.52

lemurs (Lemuroidea, https://en.wikipedia.org/wiki/Lemur) 1.0 or <1.0

langurs (Semnopithecus, https://en.wikipedia.org/wiki/Semnopithecus) relatively small values for monkeys

caribou/reindeer (Rangifer tarandus in wild, not domestic, form) 0.78

wildebeest (Connochaetes sp.) 0.68

warthog (Phacochoerus sp.) 0.40

hippopotamus (Hippopotamus sp.) 0.27

African bush elephant (Loxodonta africana) 0.63

bottlenose dolphin (Tursiops truncatus) 3.60

various dolphins (Delphinidae) 2.43-4.45

My commentary:

Elephants are clearly far brainier than hippos (0.6 cf 0.3).

Warthogs are less brainy (0.4) than ruminants (0.7-0.8), which I find rather surprising. However, note the similarity in EQ between warthog and hippo, which makes sense in view of a multifacetted similarity in morphology, ecology, and life history strategy between pigs and hippos.

The above data-set

does not show elephants to be brainier than ruminants; however, other data-sets (published by other authors) do so; and
shows capuchin monkeys of South America (which are the brainiest of all non-human primates) to have EQ 2.5, compared with the human value of 5; there are no apes in this list, but note that the EQ value for capuchin monkeys (2.52) exceeds even that for the patas monkey (1.93), which is among the brainiest of Old World monkeys, and apparently (see below) brainier than baboons.

It is unsurprising that the patas monkey - which is exceptional among monkeys in living a quasi-cursorial existence in predator-rich African savannas without the benefit of cliffs or trees to take refuge in/on - is almost twice as brainy as the proboscis monkey. The latter

lives on a large island (Borneo), and
eats leaves, which swell its body mass with bulky fibre.

Different values again were calculated by Martin (1984, https://link.springer.com/chapter/10.1007/978-1-4757-5244-1_3) and Jerison (1973, https://www.science.org/doi/10.1126/science.184.4137.677 and http://hjerison.bol.ucla.edu/).

In the list below I present them in the same order, i.e. Martin’s and then Jerison’s, separated by the word ‘or’.

human (Homo sapiens) 6.28 (according to Martin 1984) or 8.07 (according to Jerison 1973)

gibbon sp. 2.40 or 2.60

chimpanzee (Pan troglodytes) 2.38 or 3.01

bonobo (Pan paniscus) 1.80 or 2.36

macaque (Macaca sp.) 1.78 or 1.95

mangabey (Cercocebus sp.) 2.09 or 2.29

?vervet monkey (?Chlorocebus sp., https://en.wikipedia.org/wiki/Chlorocebus) 1.96 or 2.05

proboscis monkey (Nasalis larvatus) 1.07 or 1.24

olive colobus (Procolobus verus) 1.27 or 1.41

baboon (Papio sp.) 1.74 or 2.05

patas monkey (Erythrocebus patas) 1.99 or 2.19

capuchin (Cebus sp.) 3.25 or 3.25

My commentary:

Note that South American capuchin monkeys (which use tools and share food) have EQ (3.25) far greater than that of baboons (1.74-2), which makes sense. Capuchin monkeys actually exceed apes in EQ (the latter in this data-set having values of <3). Baboons have similar values to macaques and guenons.

Mangabeys and the patas monkey seem superior to baboons in EQ despite being less gregarious. I find this puzzling.

Colobines (https://en.wikipedia.org/wiki/Colobinae) such as the proboscis monkey are clearly inferior to cercopithecids in EQ, which may be partly owing to their gut-fill with bulky leaves.

Everyone agrees that chimpanzees (genus Pan) are brainy. However, it is not true that the EQ values of chimpanzees and cercopithecids have non-overlapping ranges. Instead, there is considerable overlap. This means that the most familiar genera of apes are not categorically brainier than Old World monkeys.

For example the EQ for the bonobo is 1.8-2.4 according to these authors, compared to similar values for mangabeys (and the patas monkey not much inferior).

It is true that a gibbon (2.4-2.6) is categorically brainier than any Old World monkey (for which all values fall <2.3). However, this cannot be said for chimpanzees (Jerison’s value for a baboon exceeds Martin’s value for the bonobo).

And, as I have already mentioned, capuchins clearly exceed chimpanzees in EQ.

It is interesting that the brainiest of apes seems to be a gibbon, despite the lack of gregariousness in gibbons. I.e. gibbons (2.4-2.6) far exceed baboons (1.7-2.1) in EQ, despite the gibbons being incomparably less socially complex than the baboons.

This indicates the difference between apes and cercopithecids. However, chimpanzees do not exemplify this as clearly.

As in a study cited earlier in this Post, it is remarkable how much less brainy the proboscis monkey of Borneo is than the patas monkey of African savannas (<1.25 cf >2). This is partly explained by the greater gut-fill (leaves) of the colobine. However, it also reflects the far more hectic environment of the African cercopithecid, which is extreme among non-human primates in living out in the open by its wits, in a predator-rich environment with short sparse vegetation and no cliffs for refuge.

Publicado el 30 de junio de 2022 a las 04:56 AM por

milewski

Comentarios

In the book ‘Wild Justice’ by Marc Bekoff and Jessica Pierce (2009), there is a chapter (ch. 5, pp. 110ff) on play behaviour. Here are my notes.

Although these authors do not put it this way, they imply that part of the function of play behaviour is ‘the practising/rehearsal of justice’, i.e. that via play animals can learn how to apply the principles of justice to their social lives during adulthood. I accept this implication as a valid one although this has not been spelled out in this book. My inference is that part of the reason why baboons cease to play once they reach puberty is that there is no point ‘practising justice’ in their society; their society has no use for justice. On page 121, Bekoff and Pierce implicitly extend this, by pointing out that one of the features of play behaviour is that it temporarily suspends, or even inverts, the dominance hierarchy, e.g. by means of ‘self-handicapping’. This can be interpreted as a kind of ‘practise of hypothetical fairness’, not so?

A surprising fact is that, in Homo sapiens, an ability assess another individual’s intentions emerges already in infancy, at the age of just six months. This is before a human infant can sit or walk. The researcher who has shown this is Kiley Hamlin (Yale), who has published in Nature. My inference is that a human infant can already distinguish self from conspecific other before it learns to sit, let alone walk or talk, whereas baboons never learn to do this even in full maturity.

One expert on play behaviour is Gordon Burghardt (Uni of Tennessee). Apparently play behaviour has been recorded even in certain spp. of crustaceans! Another expert is Sergio Pellis (Uni of Lethbridge). Pellis, confirming that Rattus norvegicus plays during adulthood, has studied how this relates to social dominance: ‘even in rats, fairness and trust are important in the dynamics of playful interactions’.

Does Kerrie Lewis Graham (Texas State Uni), who has researched play in primates particularly, realise that baboons are odd among monkeys in not playing as adults?

On page 120, Bekoff and Pierce mention that laughter has been recorded in Rattus and Canis (as well as apes), with an implication that this continues into adulthood. I do not know whether laughter has been studied in dolphins. However, I would not be surprised if laughing ‘vocalisations’ are used also by certain cetaceans during adult play.

The play behaviour of capuchin monkeys (Cebus spp.) has been studied by Sarah Brosnan and Frans de Waal. Capuchins differ from baboons in using tools and sharing food. These authors conclude that capuchin monkeys carefully monitor equity and fair treatment among peers; social monitoring for equity is especially evident among females. Chimpanzees are also known to show a sense of aversion for inequity.

As Bekoff and Pierce imply, cognitive empathy is associated with ‘indignity’ and ‘gratitude’. As I see it, animals lacking cognitive empathy, such as baboons, are incapable of indignity and gratitude, which is entangled with their incapability of play in adulthood.

On page 131, Bekoff and Pierce (2009) write: “Trust is essential for maintaining group cohesion.” I doubt this: there is strong gregariousness in baboons but I don’t see trust as playing a part in this in any meaningful sense. With a system of apology whereby transgressions and offences can be excused, trust is not really necessary according to my interpretation.

https://books.google.com.au/books?id=cCUMzvEvdM4C&pg=PA200&lpg=PA200&dq=wild+justice+bekoff+and+pierce+an+additional+area+of+research+sheds+light+on+animals'+sense&source=bl&ots=UeM0Fb17YL&sig=BgqaAYPWFb_yF9L_tVn-SOw2tas&hl=en&sa=X&ved=0ahUKEwi8iPummM7MAhUlrqYKHZ5ZAd0Q6AEIGzAA#v=onepage&q=wild%20justice%20bekoff%20and%20pierce%20an%20additional%20area%20of%20research%20sheds%20light%20on%20animals'%20sense&f=false

Anotado por milewski hace casi 2 años

It strikes me that there is a certain difference between ‘apology’ and ‘forgiveness’ that is worth clarifying w.r.t. the lack of cognitive empathy in baboons. The difference lies in trust, a concept alien to the mentality of baboons.

An apology can be made without any concept of trust or forgiveness. This is because, in its most basic form, an apology acts as a simple signal of submission. What it basically says is: I accept inferiority in this dispute.

So the acceptance of an apology does not require trust to have been established; it merely requires the offended partly to accept the ‘submission’, so that the relationship can proceed.

Forgiveness is beyond apology, in the sense that forgiveness requires trust. I hypothesise that, because trust is a non-concept to baboons, they are incapable of forgiving. It is not that they have a capacity to forgive but choose not to: it is that to baboons forgiveness is meaningless.

Play in adulthood is intimately entangled with apology and forgiveness. When adults of the domestic dog play, one can often see gestures of apology. These allow play to resume. I do not know whether the domestic dog has a capacity to forgive in the same sense as we humans do. The main reason to suspect that the domestic dog does have this capacity is the very fact that it plays at all, in adulthood. It should be obvious that a capacity for forgiveness is in turn entangled with a sense of humour.

However, baboons differ from the domestic dog as follows.

During their adult interactions, baboons certainly do have certain gestures of apology. These are essentially either ‘submissive’ or ‘reassuring’, and they lubricate the uneasy coexistence among adult males in particular. However, there is no need to invoke forgiveness, trust, humour or play in interpreting these ‘apologies’, because an apology is a much simpler act than an act of play. When a human apologises, this may or may not mean, in addition to ‘excuse me’, the following: ‘forgive me’, and ‘trust me’, as well as ‘please continue to play with me’. In baboons, as I see them, it always means only one simple thing: excuse me. Forgiveness, trust, and adult play all depend on cognitive empathy, which baboons seem to lack.

Anotado por milewski hace casi 2 años

It seems clear that even the laboratory rat/brown rat (Rattus norvegicus) has cognitive empathy. In order to put this into useful context w.r.t. baboons, here is a brief preamble.

The laboratory rat is derived from a species that evolved partly in adaptation to opportunities created by humans. Owing to its peculiar niche, it is reasonable to characterise R. norvegicus as combining extreme fecundity with above-average intelligence for a mammal. The brown rat can breed fast enough to keep up with our efforts to exterminate it as a pest, and it uses not just its fecundity but also its intelligence to compete with us for the food we grow and store. It is, in many ways, our match even though it is a ‘dumb rodent’. It is both more fecund and more intelligent than one would expect for a wild rodent.

I suspect that this species should be split into two separate species, the commensal form and the domesticated form. However, regardless of the taxonomy, it seems that the genus Rattus is capable of play during its adult stage. In this way it seems to differ from baboons. Baboons are far more brainy than Rattus, and yet they do not – as far as I know – continue to play during adulthood.

This difference is even more surprising that it may seem at first glance. This is because rats are not as socially complex or versatile as baboons are, at least in any sense easily comprehensible to us humans. Furthermore, R. norvegicus is a short-lived species, with a life history strategy based mainly on extremely rapid reproduction and growth – the opposite approach to that characterising primates. That even a rodent such as Rattus – with its short life, rapid growth, extremely brief juvenile period, and premium on reproductive activity once adult, and with a societal structure presumably designed around this agenda – should retain play behaviour during adulthood seems almost ‘too good to be true’ from the anthropocentric viewpoint that would love to recognise cognitive empathy in non-human mammals.

We humans despise rats as, in many ways, our antithesis, our enemies, our competitors, and our ‘spiritual nemesis’. The surprise in all of this is that, when one compares Rattus with the baboons that are so closely related to us with such an ostensibly similar society, it turns out to be Rattus that more resembles us in play behaviour specifically, and cognitive empathy more generally.

A clear-enough picture seems to be emerging. This is that cognitive empathy (and the correlated play behaviour continuing into adulthood) is actually unremarkable for mammals. Even mammals as primitive as wallabies retain a capacity to play into adulthood (studied by Duncan Watson and David Croft). What is odd is not that non-human mammals play as adults and show cognitive empathy, but that baboons do not.

http://www.ratbehavior.org/RatPlay.htm

Anotado por milewski hace casi 2 años

This paper (https://www.researchgate.net/publication/270620894_African_Elephant_Play_Competence_and_Social_Complexity and https://www.semanticscholar.org/paper/African-Elephant-Play%2C-Competence-and-Social-Lee-Moss/aa2a9f6b9eb65d84ab3c7aedb7925920d21c5686) shows that the African bush elephant plays not just as a juvenile but also as an adult.

This confirms that the African bush elephant differs from baboons in this way. Both elephants and baboons, of course, play as juveniles.

However, it seems that elephants have greater playfulness than baboons at the adult stage of life. Elephants retain playful behaviour as adults, whereas according to my readings baboons lose play behaviour as adults.

This supports the view that elephants show greater cognitive empathy than that shown by baboons.

So, now we know that elephants are different from baboons in at least three ways w.r.t. cognitive empathy: they show consideration for conspecific individuals in terms of consolation and comforting an individual victimised by a bully, they pass the visual mirror test, and they continue to play as adults. All these behaviours seem ‘par for the course’ from the human viewpoint, for an intelligent and socially complex mammal.

So, the surprise is not so much that elephants show these behaviours, but rather that baboons do not show them. Since elephants also show tool-use, and baboons do not, a syndrome is emerging.

I suspect that, in due course, it will be shown that another of the behaviour repertoires of which elephants is TEACHING (e.g. a mother teaching a juvenile how to make/use a tool), something which I regard as absent in baboons at any age.

As I have mentioned in several recent Posts, elephants show more cognitive empathy than baboons do, despite being unrelated to humans and, in the scheme of things, probably less brainy than baboons (although precise comparisons are difficult).

And I have speculated that elephants, which have small eyes but extremely well-developed olfaction and hearing, can probably pass an olfactory or audial version of the ‘mirror test’, which signifies a cognitive ability to distinguish between self and other within the species. This ability is of course basic to cognitive empathy. Apes pass the visual mirror test, but baboons do not.

The references below show that the Asian elephant (Elephas maximus) has, to my surprise, been shown to pass the visual mirror test. Despite its small eyes and its reliance on other senses, even by visual means this species of elephant is empathetic enough to be able to tell self apart from other. This is a clear hint that elephants are more empathetic than baboons, not so?

http://www.worldanimalprotection.org.au/news/understanding-emotional-lives-elephants?utm_source=Google&utm_medium=Google-grant&utm_campaign=news&gclid=CjwKEAjw6sC5BRCogcaY_dKZ2nESJABsZihxb_4_hGBWF3S4y0jpnBuHsLCWDBky8-WbI4YwjWHFFRoCh_bw_wcB

http://www.natureworldnews.com/articles/12269/20150127/understanding-an-elephants-playful-side.htm

Anotado por milewski hace casi 2 años

I quote from an article that appeared in PNAS.

“Female chimpanzees like to help others spontaneously rather than act selfishly, suggesting altruism...Yerkes Primate Research Centre...tested seven female chimps to see if observations of the species’ generous behaviour in the field matched their decisions in a lab. Given a choice of two coloured tokens, one which guaranteed a banana treat for two and the other which gave a reward for the chooser only, the chimps tended to pick the social option...Previous studies have suggested that chimps tended to act selfishly. The researchers also found that chimps most often acted generously when the waiting partner reminded the chooser gently of her presence but did not act up or bully her into picking the treat for two. ‘It was far more productive for partners to be calm and remind the choosers they were there from time to time’, researchers said.”

I do not know whether a similar experiment has ever been done on baboons, but everything I have read about baboons leads me to expect that they would differ from chimpanzees in failing this test.

Anotado por milewski hace casi 2 años