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Patterns in relative size

differences in some major brain

structures among haplorrhine

primates.

Brigitte Norman

INTRODUCTION

The relative size of the brain in human and non-human

primates has been under much scrutiny in recent

decades. Apart from its obvious research interest (why

do humans have such large brains?), the allometric

relationship between brain and body size is a

fascinating field of study that has led to many different

avenues of enquiry. It has revealed a number of

consistent patterns, linked regularities and inter-

connected factors with far reaching consequences.

The greatest brain differences within the primate order

have been found between the Prosimians and

Anthropoids, but this survey will focus specifically on

the haplorrhine primates (all anthropoid primates and

Tarsius). Patterns in size variations within this group

are considered in relation to the whole brain, the main

structural areas (neocortex, cerebellum, midbrain), and

some specialised structures (visual cortex and main

olfactory bulbs).

METHODS

The size of the brain is highly dependent on that of the

body (large animals have proportionately large brains),

but the scaling of the brain relative to the body is not a

linear relationship. For example, it has been

consistently observed that across the mammalian order,

brain size increases by a factor of 0.75 to the size of

the body. That is to say, the brain to body ratio gets

increasingly smaller as the animals get larger. In

primates, the exponent is even smaller, between 0.66

and 0.80 depending on the species (Harvey & Krebbs

1990; Deacon 1995; 1997). This is a serious problem

when straight ratios of brain to body size -

encephalization quotients (EQ) - are used as a basis for

inference (Passingham 1981).

Regression analyses. Because of the non-linear

relationship between the size of the brain to that of the

body, statistical 'regression analyses', which can take

into account the effect of absolute body size, are now

generally used. The size of the brain for each species is

plotted against each body weight along the Y and X

axes respectively - the axes scale are generally

logarithmically transformed to adjust the data at the

large end of the spectrum. A line, describing the

average derived from all the values on both axes, is

fitted to give the trend for that particular group. Each

point on this trendline represents the predicted Y value

(brain) given a particular X value (body size). Thus,

each species has either a. the same amount, b. more, or

c. less brain tissue than would be expected for their

body size. The amount by which they deviate from the

trend (the differential) provides the basis for

comparative analyses of variations in a selected group.

A major problem in regression analyses is determining

the best way to describe the trend, or the 'best line of

fit', since different equations result in different trends.

(Clutton-Brock & Harvey 1980; Martin & Barbour

1989; Harvey & Krebbs 1990). A coefficient of

determination (r2) is therefore included to indicate how

closely the line fits the data. It compares the estimated

value and actual values and ranges from 1 (perfect

correlation) to 0 (no correlation).

There are other problems. In the most commonly used

regression method, Least-Squares, there is the

assumption that Y (e.g. brain size) is dependent on X

(e.g. body size), and that X was measured without

error. But, Martin & Barbour (1989:67) observe, "in

any biological context, it is usually difficult to argue

for a direct dependence of Y upon X, especially when

interspecific allometric relationships are involved".

The size of animal bodies is not necessarily an absolute

value since it is subject to a number of factors, all of

which can differ from individual to individual within a

given species. Furthermore, differential values ought to

reflect potential measurement errors such as can occur

in both variables (Clutton-Brock & Harvey 1980;

Martin & Barbour 1989; Harvey & Krebbs 1990; Ebert

& Russel 1994; Steele 1996).

There are statistical methods which take into

consideration basic relationships between variables and

potential errors in both axes. The best and most

commonly used are the Reduced Major Axis, and

Major Axis approaches(Clutton-Brock & Harvey 1980;

Martin & Barbour 1989; Harvey & Krebbs 1990; Ebert

& Russel 1994; Steele 1996). However, these are not

as easily derived as the Least-Squares regression. So,

for the purpose of this preliminary analysis, because of

its greater ease of calculation the Least-Squares

method has been used instead.

Source data. All the data used in these analyses are

derived from Stephan et al. (1981), additional data

have not been incorporated. There are two reasons for

this. Firstly, this is the most complete data set in the

primate literature, having 41 variables (not including

body and total brain measures). These data have been

measured for a total number of 76 species, including

48 primates species, including Homo (although some

structures have not been measured for all the species).

Secondly, the data were measured by the researchers

themselves. They explain how, and under what

conditions the measurements were made. Information

from other sources would not have been derived in

comparable circumstances, thereby introducing an

unnecessary bias. Although no biological measures can

be taken as absolute, the use of this single data set has,

at least, the advantage of consistency.

Because, phylogenetic patterns are looked for, the data

has been adapted from species to genus. However,

only two genera (Saguinus and Cercopithecus)

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consisted of more than one species, so, the information

is also essentially valid at species level, but reduces the

value of phylogenetic inferences. The summary table

(see appendix) lists the genera involved, together with

their common names, phylogenetic grouping, and

influential characteristics.

N.B. The body weight measurement for Lagothrix was increased

from 5,200 g to 7,300 g., as all other published data indicate that

this genus is much larger (data from Smith & Jungers 1997).

TOTAL BRAIN SIZE

There is a growing body of literature dealing with the

allometric relationships between brain and body size in

primates and other mammal orders. The reason why

this relationship is so scrutinised is, of course, that

primate brains are proportionately larger than in most

other mammals, and larger in humans than would be

expected in primates of a similar size.

Different authors have considered a whole range of

factors which appear determinant or influential in the

relatively large size of primate brains. Primates’

special visual and manual abilities have been a major

focus of research. But a whole range of other factors

appear to be involved, although in what degrees is

difficult to determine. They include the energetics of

dietary quality and metabolic rate (Clutton-Brock &

Harvey 1980; Aiello & Wheeler 1995); cognitively

complex foraging (Gibson 1986), activity timing,

vertical distribution, home range size, mating systems

(Clutton-Brock & Harvey 1980), social complexity

(Aiello & Dunbar 1993; Dunbar 1995); life history

parameters (Harvey et al. 1987; Harvey & Krebbs

1990). Alternatively, as Deacon argues (1997), it may

also be that primates do not have especially enlarged

brains, but instead evolved relatively smaller bodies.

Total brain weight to body weight. A regression plot

of the haplorrhine taxa included in Stephan et al.

(Figure 1.0), shows that Homo, Erythrocebus,

Miopithecus, Cebus and Saimiri are significantly above

the predicted average for their body size. In contrast,

Gorilla, Nasalis and Alouatta are less encephalized.

Except for Papio and Tarsius, all the genera that have

noticeably smaller brains are classed as folivorous, and

all except Gorilla are non-extractive foragers. In

contrast, apart for Pithecia and Miopithecus, all the

significantly above-average taxa are either

omnivorous, extractive foragers, or both. Although

Miopithecus has been classed as neither, its dietary

quality (262.5) is in the same range as that of Cebus

(266) and Saimiri (284) (Sailer et al. 1985). It appears,

therefore, that ecological adaptations (diet and

foraging complexity) play a significant role in the

overall relative size of the brain, but there are

exceptions to this trend.

Despite an extremely high quality diet (335) Tarsius'

small brain can be related to the fact that the brains of

insectivores are smaller than animals that include a

proportion fruit in their diet This is consistently the

case in all mammalian orders (Clutton-Brock &

Harvey 1980; Harvey et al. 1987).

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There are two contradictions to the ecological trend.

Pithecia is a non-extractive forager and has a dietary

quality of 197.5, very close to Papio (198.6) which is

omnivorous and an extractive forager. Yet the former

has an above-average, and the latter a below-average,

brain size. So either there is some error in the data or

other factors are also involved.

In terms of phylogenetic patterns, all the New World

genera except for Alouatta are very close to the

predicted brain size or are above it. In contrast, the Old

World primates show more variation: 6 out 14 are well

below-average, 5 are close to the mean, and 3 above-

average. So, in this particular sample of Haplorrhines,

the New World Monkeys, as a group, have above-

average brain sizes relative to body weights.

Total brain measurements, however, cannot reveal any

of the structural changes that occur within the brain

itself.

Vertebrate brain evolution. Like the human brain, all

vertebrate brains are subdivided into three main areas:

the hindbrain, midbrain, and forebrain. But the relative

development of these areas and their constituent parts

vary widely across the evolutionary scale.

In early vertebrates, the sense of smell is most

important and their brains have extremely large

olfactory tracts. In fish the cerebrum is very small

being, essentially, a processing centre for input from

the senses. The cerebrum becomes more important

among amphibians and reptiles. In birds, smell is far

less important than vision, so they have small olfactory

tracts but highly enlarged optic lobes which have

further increased the size of the cerebrum. In

mammals, because of their increased cognitive

abilities, the cortical areas have become increasingly

important. In primates, the cerebrum is so much larger,

that it dominates the rest of the brain (Wooldridge

1963; Passingham 1981; Deacon 1995, 1997).

Thus, the cerebrum (overlaid by the neocortex), is the

largest of the three main brain areas in mammals,

primates and, in particular, humans. The other two

being the brainstem, in the lower centre (connecting

the cerebrum to the spinal cord), and the cerebellum at

the lower back of the brain (connecting to both the

brainstem and the neocortex). Variations in the relative

size of each these areas can, therefore, affect the

overall size the brain. However, the brain cannot

increase indefinitely, its relative growth is ultimately

limited by its body size. So, enlargements in certain

areas of the brain are generally accompanied by

reductions in other areas. These relative changes are

indicative of functional shifts within the brain and,

therefore, more informative than size measurements

(Deacon 1997).

NEOCORTEX

The greater size of primate brains is primarily due to

the enlargement of the neocortex. The neocortex is the

part of the cerebral cortex that is unique to mammals

because it is the most recently evolved part of the

brain, where the higher thought-functions are located

(Wooldridge 1963; Passingham 1981; Deacon 1995,

1997). Because the neocortex overlies the cerebral

hemisphere and is made up of deep, convoluted folds,

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it has been responsible for the greater part of primates’

brain expansion in evolutionary time.

In primates and humans the relative size of the

neocortex has been linked specifically to social group

size (i.e. social complexity), cognitively complex

foraging (Gibson 1986; Aiello & Dunbar 1993) and to

life history variables such as life span and the length of

the juvenile period (Joffe 1997).

The size of the neocortex has been observed to

increase with the size of the brain. As Passingham

(1981) comments, "the neocortex forms a smaller

percentage of the total brain in prosimians than in other

primates, and in monkeys than in apes. In general, the

proportion of neocortex to total brain increases in

primates as brain size increases". Figure 2.0 describes

this trend among the Haplorrhines and shows a very

strong correlation between the two (r2 = 0.9934).

Neocortex volume against rest of the brain. If the size

of the neocortex is highly correlated to the overall size

of the brain, one should expect to see a similar

distribution to the one in Figure 1.0. Overall, 13 out of

26 genera are above the average. Of these,

Erythrocebus, Macaca, Miopithecus and Saimiri are

measurably above the line. Homo, Pan, Papio, Cebus,

Cercopithecus and all the Callitrichines are also above-

average but much closer to the mean. Thus, although

above-average, Homo does not have a particular large

neocortex size for the size of its brain.

All the other taxa are either average or just below it,

except for Gorilla and Tarsius which are more

markedly so. The latter's deviation could be related to

the general prosimian trend mentioned above and to a

characteristic of insectivores. However, despite a

smaller overall brain size, as apes, the Gorilla should

have more neocortex than they exhibit.

Many of the genera that are above the predicted

average are predominantly omnivorous and, to a lesser

extent frugivorous, (high-quality diets), while all the

average taxa are folivorous and/or frugivorous. All

those that fall below the average (except Tarsius) are

almost exclusively folivorous (low-quality diets).

There is also a degree of correlation with foraging

strategies, as the vast majority of extractive foragers

are over the average; one, Lagothrix, is average, and

one, Gorilla, is below.

Vertical distribution is another characteristic which

could be linked to this trend, as the genera that exhibit

a greater degree of terrestriality have, in the great

majority of cases, larger than predicted neocortex, or

(as in Colobus) are average. Again, only Gorilla

(terrestrial) have a smaller neocortex size.

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In terms of taxonomic groups, the primates that

conform to the predicted size of the neocortex are:

The lesser apes

Lophocebus

All the Colobines (except Pygathrix)

All the Atelines

The primates that are above the predicted value are:

The Hominoids (except Gorilla)

All the Cercopithecines (except Lophocebus)

All the Cebides (except Alouatta)

All the Callitrichines

The primates that are most significantly below

predicted size are:

Gorilla

Pygathrix

Alouatta

Tarsius

From these lists it can be seen that among these

Haplorrhines the overall trend is for average to above-

average neocortex sizes and that most related genera

share a particular tendency either to the average or

above-average. In contrast, all the significantly below-

average taxa are lone representatives of their greater

phylogenetic group and therefore appear as exceptions.

They are 2 Catarrhines, 1 Platyrrhine, and 1 Prosimian.

They are also the same genera that, for ecological

reasons, had smaller overall brain sizes.

Neocortex ratio against body weight. Figure 2.1 shows

the neocortex ratios plotted against body weight. The

coefficient of determination has dropped to 0.7374,

indicating a greater range of variation from the

predicted values. At first glance, the obvious pattern to

emerge is that the Callitrichines are very close to the

predicted average; either on the line or just above. The

larger New World taxa are predominantly below, with

Alouatta significantly below-average. The highest is

Ateles which sits on the line. But the two Cebines,

Cebus and Saimiri are exceptions, as they are well

above-average, especially the latter. These patterns are

consistent with the trend in overall brain to body size,

discussed above, with one exception being Pithecia,

which is well above average in total brain size but

slightly below-average in neocortex volume in relation

to the rest of the brain.

Among the Old World, all the Cercopithecines have

significantly more neocortex in relation to their body

size (excpet for Papio which is on the line), but they

vary in the degree. The folivorous apes (Hylobates and

Gorilla) are below-average, notably Gorilla. Pan has

more and Homo drematically more neocortex than

predicted for itheir body sizes.

The broad pattern of variations in the relative size of

the neocortex indicates that, as phylogenetic groups,

the New World primates are more homogenous than

the Old World, and the Old World species display

more variations. This has also been commented upon

in relation to their respective ecological and

morphological adaptations and has much to do with the

greater variety of environmental niches available in the

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Old World and the long isolation of the South

American species during their 30 million years of

independent (and at times convergent) evolution

(Napier & Napier 1986; Fleagle 1988).

The distribution of Old World taxa shows the same

trend discussed above: omnivorous and/or extractive

foragers have higher than average neocortex size

(Miopithecus, Erythrocebus, Macaca, Pan and Homo).

Again, Papio is average for a primate of this size. So

the reason why it has a smaller brain size than

expected must be looked for elsewhere.

In conclusion, there is a high correlation between

neocortex size and overall brain size. Deviations from

the mean appear related to ecological adaptations:

dietary quality, foraging strategy and vertical

distribution, rather than to phylogenetically derived

differences between Old World and New World

species. Within taxonomic families and sub-families

there are consistent trends. However, these may be due

to the similar nature of the generic adaptations, which

may be phylogenetically derived traits representing

general tendencies within the groups. Generic and

species variations occur in most families, and in these

cases, neocortex variation is accounted for by

ecological factors.

There are, however, two exceptional cases Tarsius and

Gorilla. The former is the more easily accounted

because it is both nocturnal and insectivorous. Gorilla,

on the other hand appears to defy all the trends.

We need, therefore, to look at other brain structures

which may account for the peculiarities exhibited by

some species, notably Pithecia's above-average brain

size and below-average neocortex size, Papio's smaller

than predicted brain size, but average, neocortex size

and Gorilla’s smaller brain and neocortex sizes.

CEREBELLUM

After the neocortex the cerebellum is the second

largest area in the human brain. It is the principal

component of the hindbrain. As in the cerebrum the

cerebellum is divided into two hemispheres. This

structure is older, in evolutionary terms, than the

neocortex. It is particularly well developed in higher

vertebrates and in humans still largely retains the

functions it does in other animals. The cerebellum is

the centre for the coordination of skilled muscular

movements, such as locomotion and the maintenance

of posture and balance (Wooldridge 1963; A.B.T.A.

1991; Deacon 1997). However, in humans the

cerebellum is also closely connected to the neocortex

and involved in learning abilities (Passingham 1981;

Deacon 1997). Because of its evolutionary importance,

the size of the cerebellum may be a significant factor

in the overall brain size of other primates.

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Cerebellum volume against the rest of the brain. In

Figure 3.0. the cerebellum volumes are plotted against

the rest of the brain. The coefficient of determination

is, again, very high (0.9905), so that, overall, the

correlation between the scaling of the brain and that of

the cerebellum is very close.

The overall pattern of deviation is broadly reverse to

that of the neocortex. Except for Pan, all the taxa

which have above-average neocortex for their brain

size have below-average cerebellum: Homo,

Erythrocebus, Macaca, Cercopithecus, Miopithecus

and Saimiri. The greatest positive deviations in

neocortex correspond to the greatest negative

deviations in the cerebellum (Erythrocebus and

Miopithecus). However, the New World Saimiri do not

display this inverse relationship to the same degree.

Conversely, all the taxa with below-average neocortex

measurements appear to have above-average

cerebellum size. Furthermore, Tarsius, Pithecia and

Gorilla fit the trend particularly well. This

demonstrates one of the principles of brain evolution,

which Deacon (1997) refers to as ‘displacement’.

Within the brain, irrespective of its overall size, extra

growth in one area must be accompanied by a

corresponding reduction in other parts (Deacon 1997).

Gorilla is a particularly good case in point. In the same

context, Papio, displays more negative deviation in the

cerebellum than positive deviation in the neocortex,

which begins to explain its small overall brain size but

relatively large neocortex. Thus, where there is more

than average neocortex, there is a marked tendency to

have less cerebellum, but there are variations in the

degree to which this is so. There is, however, one

exception. Pan has slightly above-average neocortex

but also above-average cerebellum. So, we should

expect to see a proportional reduction in another

structure.

As for the neocortex, there is no overall trend in the

Haplorrhines as a whole, but the New World primates

are more consistently above-average, while the Old

World show more variation. This again can be related

to the more restricted and uniform ecological

circumstances in the South American continent, as

well as to the more uniform trend in neocortex

discussed above.

The importance of the cerebellum, may be related to

motor behaviours, such as locomotion in Gorilla, but it

is does not appear to be a significant factor in other

species. Because of the displacement effect, the factors

that appear influential in the relative size of the

neocortex must have an indirect effect on the size of

the cerebellum and other structures. This becomes

apparent when the cerebellum ratio to the rest of the

brain is plotted against body weights (Figure 3.1) and

the coefficient of determination drops to 0.273.

Although the trend here is the same as the one

described above, it is so poorly correlated with actual

body weights that the relative size of the cerebellum

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does not appear particularly influenced by the size of

the body as such.

MESENCEPHALON

The third major area of the brain, the midbrain

(mesencephalon), is a particularly important area in

primates. It acts as the relay centre for the senses input

to the cerebral hemispheres and contains, for instance,

the origins of the 3rd and 4th cranial nerves

responsible for eye movements (A.B.T.A. 1991). As

Deacon explains (1997:230), "the midbrain is the first

point, ascending from the spinal cord, where the long-

distance senses, vision and hearing, are integrated with

information about touch and movement". The input for

these senses (eyes and ears) are located in the head.

The midbrain is also related to primate vocalisations,

which are an important part of their behaviours, and in

humans has developed into full-scale language. In

many vertebrates, the midbrain is specifically involved

in the automatic expression of arousal and emotional

states. In primates, many emotional states are

expressed vocally, and involve both oral and

respiratory control. The automatic regulation of these

actions occurs in the midbrain (Deacon 1995; 1997).

Midbrain volume against rest of the brain. Figure 4.0

reveals a very close correlation between the size of the

midbrain to that of the overall size of the brain (r2 =

0.9944). Strong positive deviations occur only in

Papio , Lophocebus and Tarsius, and to much lesser

extent in Procolobus, Pygathrix, Lagothrix, Cebus and

Callicebus. Negative deviations are only evident in

Saimiri and Aotus and to a lesser extent in Hylobates,

Macaca, Ateles, and Callimico.

The marked increase in midbrain areas in Papio, is

consistent with the reduced importance of the

cerebellum. Lophocebus, on the other hand, is

otherwise average in overall brain, neocortex and

cerebellum size. This is, therefore, a departure which

should have a correspondence in the reduction of one

or other areas. For Tarsius, there is a marked negative

deviation from the mean in neocortex size. This is

partly accounted for by an above-average cerebellum

size and by significantly larger midbrain areas.

The Macaca deviation is particularly interesting, as the

macaques are well known to have particularly

sophisticated visual and vocal communicative

behaviours; both in terms of output (calls and facial

expressions) and in the processing of this information.

This slight reduction, in the midbrain areas, suggests

that the control of these functions may have been

slightly shifted to other areas of the brain. Indeed, there

is much evidence to suggest that several non-human

primate species have specialised cortical areas for the

processing of species-specific auditory information and

the macaques are one of the best examples. Several

studies have also revealed that, not only are they adept

at social sound recognition (communicative calls), but

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that, like humans, they process this information in the

left cerebral hemisphere (Zimmermann 1995; Deacon

1995)

A similar process may be responsible for Saimiri’s

much more pronounced negative deviation in midbrain

areas. As in Macaca, this suggests a more ‘conscious’

level of sound information processing. In Saimiri

sciureus (the species which supplies the measures used

in this analysis), Zimmermann explains, “the same

subcortical areas of the brain are involved in the motor

control of the production of certain sounds in this

highly vocal primates species as in humans”

(1995:126).

The strong negative deviation in Aotus may also be

related to specific and specialised vocal

communication requirements in this nocturnal species,

such as the importance of individual call patterns for

mate attraction and recognition at long-distance, and

for maintaining spacing between non-group individuals

(they live in monogamous groups) (Zimmermann

1995).

In contrast, Tarsius, which is also nocturnal but does

not live in groups, does not require more sophisticated

auditory mechanisms.

Mesencephalon ratio against body weight. The ratio

of midbrain to total brain volume is strongly correlated

with bodyweights (r2 = 0.9134). Figure 4.1 shows that

this trend, however, is a negative one. The larger the

body the smaller the ratio. This slope may be related to

the midbrain function as a relay station for input from

the long-range senses. As Deacon (1997:211)explains, The eyes, for example, are not proportionally larger

in large animals, in fact, they get proportionally

smaller as the body increases in size. Eyes are

therefore negatively allometric with body size, and

their corresponding projections in the brain are

proportionally reduced in larger animals.

BULBUS OLFACTORIUS

The olfactory bulbs which relay smell information are

extensions of the primitive cortex present in all

vertebrates and they have dramatically changed in size

during the course of vertebrate evolution. The shift to a

diurnal lifestyle in anthropoid primates has resulted in

the greater importance and specialisation of the visual

apparatus, and in a reduction in the sense of smell. All

diurnal species (including the prosimians) have smaller

olfactory bulbs than nocturnal. All haplorrhine

primates have smaller olfactory bulbs than the

prosimians and have lost the rhinarium (damp nasal

skin). And, of all the primate species, humans have the

smallest olfactory bulbs (Deacon 1995:114).

Main olfactory bulbs size against the rest of the

brain. This variability in the size of the olfactory bulbs

is evident in figure 5.0. Of all the structures considered

this correlation with the data is the weakest. This is in

agreement with Stephan et al.’s observation (1981:25)

that “the highest variability of structure consisting of

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true brain tissue is found in the olfactory bulbs (main

and accessory bulbs).” But this variability has led to an

analytical problem. When a polynomial trendline is

used the coefficient of determination is 0.8146, with a

power trendline it drops to 0.588. Thus, the former fits

the data better but appears to ‘accommodate’, or else

deviate strongly in favour of Homo. Because power

trendlines were used in all the other analyses of

structure size in relation to the rest of the brain, it will

be used here too. Incidentally, when the same graph is

plotted without Homo, the coefficient of determination

increases to 0.6094, but the general pattern remains

essentially the same.

The greatest deviations occur negatively in Pygathrix,

Nasalis and Homo, and positively in Tarsius, Aotus,

Cercopithecus, Hylobates, Papio, Pan and Gorilla.

Except for Hylobates, the negative deviations occur in

all the folivorous species, but some omnivores also

have smaller olfactory bulbs (Cebus, Miopithecus,

Erythrocebus, Lophocebus, Homo). The other

omnivores are above-average. Except for Homo, all

extractive foragers are above the line. Thus, diet is less

clearly a factor a factor, while complex foraging result

in greater sizes in the olfactory bulbs in relation to the

size of the brain.

In terms of phylogenetic patterns, The New World taxa

are tend to be grouped below the line. Exceptions are

Ateles and Lagothrix, which are the two heaviest in

this group, and Lagothrix is extractive. The New

World exception is Aotus, which also nocturnal

therefore requiring a more developed sense of smell.

The small-bodied Callithrix and Callimico are also

above-average, but less significantly so.

The Old World taxa do not follow as clear a pattern.

The nocturnal Tarsius is clearly above-average, which

is expected. All the Colobines have small olfactory

bulbs, ecpecially Pygathrix, and Nasalis, but Colobus

is closer to the mean. The Cercopithecines range from

well below the line (Miopithecus, Lophocebus,

Erythrocebus), to well above it (Papio, Cercopithecus

and Macaca). All the apes, however are well over the

average, especially Gorilla.. Homo deviates from the

Hominoid pattern and has extremely small olfactory

bulbs in relation to brain size.

Main olfactory bulbs ratio against body weights.

When the ratios of main olfactory bulbs are plotted

against body weights (Figure 5.1.), again the

correlation is weak (r2 = 0.5114) but is shows a an

overall reduction trend as body sizes increase.

Essentially the pattern of deviation is the same as

above. But their are slight differences. Except for some

Saguinus, Alouatta and Ateles, all the New World

genera fall below the line, and all the folivorous Old

World taxa, including Hylobates, are below-average.

Lophocebus is now above-average.

The overall trend indicates that except for Homo, all

the larger-bodied species (Atelines, Cercopithecines

and great apes) have larger ratios to body weights than

the mean.

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AREA STRIATA

If the neocortex is the most important part of primate

brains, the primary visual cortex, (area striata, striate

cortex, V1 or Area 17) is most developed in primates

in comparison to other mammals.

The brain areas most liable to change in size are the

sensory and motor regions of the cortex because, as

Deacon comments, they are "among the most

appropriate in size to their peripheral connections and

the most reduced with respect to typical predictions for

brain size”.

All primates have sophisticated stereoscopic vision.

This feature appears ancestral to all and probably

developed as an adaptation to nocturnal life, as it has in

other mammals (e.g. owls, bats and cats). However, the

processing of that information lies in the superior

collicus of the brainstem, not in the cortex itself

(Deacon 1995). The visual cortical areas of primate

brains, however, have become of greater importance

because they process colour information, which is rare

in mammals, but common to all anthropoid primates

except for the nocturnal Aotus. This ability to see a

whole range of colours is an adaptation to the diurnal

lifestyle adopted by the 'higher' primates. Unlike 3-

dimentional vision, the processing of colour

information is located in the cerebral cortex.

However, all visual analysis is not located in any one

cortical area. Instead the retina has correspondences in

multiple visual areas outside of the primary visual

cortex (Zeki 1993). As Deacon observes (1995:113), The primate visual cortices are the most complex

visual-processing system ever evolved. Nearly half

the cerebral cortex in macaques is directly involved

in visual processing and there are around two dozen

cortical visual areas in its brain, each receiving and

analysing different aspects of the visual world.

One of the principal functions of the primary visual

cortex is to process colour and pattern information and

to relay it to other cortical areas, but it does not appear

directly involved in visual learning (Zeki 1993;

Deacon 1995).

Visual cortex size to rest of the brain. Figures 6.0 and

6.1 describe the variation in the size of the primary

visual area against the rest of the brain across 19

haplorrhine genera. The coefficient of correlation

(0.9608) indicates a fair degree of individual variation

within the overall group in comparison to the other

structures (except the olfactory bulbs). The pattern of

deviations indicates that, on the whole, the majority of

New World species are average or below-average,

except for Saimiri, Cebus, and Lagothrix, and to a

lesser extent Saguinus. While the majority of Old

World species are average or above-average, except

for Homo, and Tarsius, and to a lesser extent Gorilla

and Procolobus. Moreover, there are only two average

cases (Pan and Callicebus). Apart from Homo, Gorilla

12

and Procolobus, all the genera that are below the line

are New World primates, while above-average taxa

include most of the Old World species.

The greatest sizes of visual cortex in relation to the rest

of the brain occur in all the Cercopithecines included

in this sample (Lophocebus, Macaca, Cercopithecus

and Miopithecus). Only one hominoid, Pan, shows a

slight positive deviation, while Gorilla is just below-

average. Aotus and Tarsius are also significantly

below-average, which is explained by their nocturnal

lifestyle.

All the omnivorous species are significantly above-

average. These include all the Cercopithecines, and

Cebides (Saimiri and Cebus). Frugivorous species are

also represented (Lagothrix and Saguinus). Also, all

the extractive genera are markedly above-average,

except for Gorilla. On the other hand, all the below-

average genera are either folivorous (insectivorous),

nocturnal or non-extractive, again except for Gorilla

and Homo.

To summarise this pattern, as in the overall size of the

neocortex, diet and foraging complexity seem to be

highly influential factors. The combination of

omnivorous-frugivorous diet with extractive foraging

strategies seem to correlate strongly with the size of

the primary visual cortex. This visual area specialises

in the processing of colour and texture information.

Such information is precisely what is required in order

to locate a whole range of foods, all of which have

different colours and textures. Colour and textural

clues are less important in species that live at night, or

feed predominantly on one resource (leaves, or

insects). Homo shows the greatest negative deviation,

and is on a par with the leave-eater Alouatta. This may

be related to the fact that humans have developed other

areas of the cerebral cortex to a much greater extent.

All the extractive foragers in this sample are non-

specialist feeders. They are omnivorous or include a

wide variety of plant foods as well as some animals.

Gorilla is an exception because it feeds primarily on

one type of vegetation; therefore, it does not need to

recognise a range of different coloured leaves. The

same is true of other folivores all of which are below-

average.

Thus variety in the diet, rather than the complexity of

the foraging strategy, per se, seems to be the

determinant factor here. The fact that these species are

extractive foragers reflects what is necessary to do in

order to retrieve the resources, after they have been

searched, located and recognised. The variety of food

resources can also be linked to a greater variety in

habitat exploration, as extractive foraging and

omnivory involves a degree of terrestriality, or at least

the ability to exploit ground-level resources as well.

This confirms the trend in Old World primate

adaptations towards ecological variety and the

continuing New World trend in essentially arboreal

life-styles, with all that this entails.

13

SUMMARY OF TRENDS

Overall, the poorest correlations in terms of structural

areas plotted against the rest of the brain (i.e. the

greatest range of deviations from the predicted values)

were, in decreasing order:

The main olfactory bulbs 0.8156

The visual cortex 0.9608

The cerebellum 0.9905

The neocortex 0.9934

The midbrain 0.9944

When plotted against body weights, the structures

under consideration showed much greater deviations

from the expected mean.

The cerebellum 0.273

The olfactory bulbs 0.5114

The neocortex 0.7374

The visual cortex 0.831

The midbrain 0.9134

On the whole, there does not appear to be a single

trend among the Haplorrhines, phylogeny appears less

important than ecological adaptations. But there are

some trends at family level.

The Callitrichines appear to be a homogenous group.

All are small-bodied and fit the predicted values for

brain size. In a range of brain structures they also fall

close to the mean expected for their total brain size.

Larger-bodied New World genera are more diverse

but, overall, show less variability than the Old World

primates. The Cebines Saimiri share the same patterns.

They have larger brains and neocortex ratios to the rest

of the brain than expected for their small body sizes.

Within the neocortex they have significantly more

primary visual cortex than expected for their brain size.

Both species share the same ecological characteristics.

The larger Atelines show the greatest variability,

which can be accounted for by their greater body size

and different foraging strategies; in this respect they

more closely resemble the ape patterns.

As a group the Old World genera display considerable

variation in all the structures. They are fairly equally

distributed below and above the mean predicted, but

whether they have more or less than the mean appears

dependent not on phylogeny but on environmental

adaptation.

The prosimian Tarsius is a consistent and expected

exception. It has a small overall relative brain size,

neocortex and visual neocortex ratio to brain size, but

average visual cortex relative to the body, large

cerebellum and midbrain ratios and olfactory bulbs.

The Colobines are medium-bodied and folivorous and

non-extractive; therefore they tend to have relatively

small overall brains, neocortex and visual neocortex

ratios, above-average cerebellum and midbrains, and

reduced olfactory bulbs. The Cercopithecines tend to

have above-average neocortex and visual cortex ratios,

below-average cerebellum, and average or above-

average midbrain ratios. But they display variety in the

size of the olfactory bulbs.

There is no consistent pattern among the hominoids.

Hylobates and Gorilla have very different patterns,

although both are folivorous. Hylobates in some ways

are closer to the Colobine patterns (neocortex size,

cerebellum and midbrain) except that they have larger

olfactory bulbs. Gorilla, on the other hand, displays

characteristics which are not easily accounted for by its

ecological or social circumstances. It has a very small

brain and neocortex size relative to body size, below-

average neocortex and visual neocortex ratios to the

rest of the brain, an average midbrain area, but

significantly larger than expected olfactory bulbs ratios

to the rest of the brain. But it also has the largest

cerebellum in this haplorrhine sample be it relative to

the body or the whole brain. This last feature may well

be related to another exceptional feature in Gorilla: its

enormous size, since the cerebellum is important in the

control of body movements. Pan also follows a pattern

of its own . It has an average brain size relative to its

body, slightly above-average neocortex and visual

cortex ratios to the rest of the brain (but above-average

in relation to body size), average cerebellum and

midbrain and olfactory bulbs (although the latter are

above-average in relation to body size). Homo have

very large brains for their body size and a very large

neocortex ratio in relation to body size. But when the

main constituent parts are considered within the brain,

they do have a larger neocortex, cerebellum or

midbrain than expected for their particular brain size.

However, they have less primary visual cortex and

significantly smaller olfactory bulbs than the

haplorrhine trend predicts.

These patterns might be partially explained by the

evolutionary trend in body size increase, leading to

more potential variation in behavioural adaptations.

The more homogenous groups are the most ‘archaic’

groups, and the smallest. Groups which include

relatively large primates, the Atelines and

Cercopithecines, show a higher degree of variety in

adaptive behaviours. The most varied of all, the apes,

are the largest and were also the last to evolve. Within

this trend, Homo, does not seem particular distinctive,

merely an aspect of the variety which characterises the

Old World primates, and the apes in particular.

CONCLUSION

This small survey only gives a very broad indication of

some of the trends in this selected group of primates.

However, it does show the potential in such allometric

analyses when more structures are analysed, more

refined analytical methods and a larger sample are

used.

Such investigations are also interesting when focusing

on the haplorrhine primates alone, (there is a much

greater variation when the prosimians are included)

since this group includes only the more recently

derived evolutionary characteristics in the primate

order, and the ones resulting in the most successful

adaptations.

The patterns that have emerged are often in accordance

with known trends, but not always. This may be a

consequence of using the Least Squares method, but it

may reflect specific haplorrhine trends, from which

14

humans, for instance are not especially different. The

analysis of the structural areas relative to each other

may, therefore, be more telling if functional

differences are looked for, rather than a simple analysis

of brain size relative to body weights.

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