Some macaques and capuchins are able to discriminate appearance from reality; seems that the evolutionary apparition of this cognitive ability was sooner than commonly believed

Are monkeys able to discriminate appearance from reality? Marie Hirel et al. Cognition, Volume 196, March 2020, 104123. https://doi.org/10.1016/j.cognition.2019.104123

Abstract: The understanding that the perceptual appearance of the environment can differ in several ways from the reality underlies the ability to discriminate appearance from reality. Being able to realize when a misperception can lead us to behave in inappropriate ways confers an evolutionary advantage and may be a prerequisite to develop a Theory of Mind. Understanding that our own perception can differ from reality seems indeed necessary to attribute to others perceptions or beliefs different than ours. This appearance-reality discrimination ability has recently been demonstrated in great apes but no information is currently available regarding this ability in other nonhuman species. In a comparative study, we tested Tonkean macaques (Macaca tonkeana), an Old World primate species, and brown capuchins (Sapajus apella), a New World primate species. We provided monkeys with two experiments using visual illusions of size and quantity to test their ability to discriminate appearance from reality, with an experimental setup similar to the one developed by Krachun et al. (2016) on chimpanzees. A large number of brown capuchins, from different ages and both sexes, as well as two Tonkean macaques succeeded in the two experiments. By ruling out all alternative explanations (i.e. visual tracking or associative learning), our study brings the first evidence that some Old World and New World monkeys are able to discriminate appearance from reality. Our results suggest moving the evolutionary apparition of this cognitive ability earlier in time. Finally, it suggests that humans could share more Theory of Mind components with more nonhuman species than we previously thought.

4. Discussion
This study brings the first evidence that monkeys are able to discriminate
appearance from reality. All our subjects passed the preference
tests of both the Lens and Mirror experiments and thus demonstrated
a strong natural preference for larger or higher number of
food items, as well as a good size and quantity discrimination ability.
Then, in the Lens experiment, all but two subjects of each species
passed successfully the basic test and the tracking control tests, demonstrating
that they were capable of ignoring the misleading appearance
of the magnified grape to choose the truly bigger one, without
being able to visual track the grapes (see Fig. 2). Afterwards, the large
number of successful brown capuchins, from different ages and both
sexes, in the last learning control brings strong evidence that they are
able to discriminate appearance from reality. In Tonkean macaques, our
results are less clear, with only one individual succeeding in the avoidlens
control (see Fig. 2). Thus, we are unable to say with confidence
whether or not this species possesses appearance-reality discrimination
ability. However, our procedure with lenses might have not allow us to
highlight AR discrimination ability in a larger scale in this species and
could provide results underestimating it (see methodological issues
discussed below). This is supported by Tonkean macaques’ good performances
in the Mirror experiment. Indeed, the two Tonkean macaques
and all but one brown capuchin that were tested in this second
experiment passed the visual tracking and the avoid-mirror tests. By
validating all controls, they demonstrated they are able to discriminate
perceived from real quantity.
We found that all except two individuals who were successful in the
Mirror experiment had also succeeded in the Lens experiment.
Successes in both of our experiments provides evidence for a general
understanding in our animals, that perceptual appearance of objects
can be different in several ways from reality. Nevertheless, we should
approach this conclusion with caution for the few individuals that
needed more than two sessions to succeed. Even by limiting the number
of sessions allowed to reach a success, our and other procedures of
progressive sessions generate an increasing probability of false positives.
To account for this multiple testing issue, one option is to look out
group performances. In this respect, brown capuchins succeeded significantly
in all tests of the Lens and Mirror experiments. For Tonkean
macaques, their succeeded significantly in all tests except for the avoidlens
tests n°1 and n°2. These results confirm our inability to conclude of
an AR discrimination ability presence for Tonkean macaques with the
Lens experiment. However, we still able to maintain confidence in our
results demonstrating AR discrimination ability in both experiments for
brown capuchins and in the Mirror experiment for Tonkean macaques.
In summary, even if more subjects of both species are necessary to make
a reliable conclusion at a species scale, results of the Mirror experiment
confirmed those of the Lens experiment and together suggest that these
monkeys could be able to discriminate appearance from reality.
The ability to discriminate appearance from reality was demonstrated
in great apes by previous studies of Karg et al. (2014) and
Krachun et al. (2009, 2016). Now, our study suggests the presence of
this ability in Tonkean macaques, an Old World monkey species, and
brings strong evidence in brown capuchins, a New World monkey
species. Therefore, the hypothesis of the emergence of AR discrimination
ability in a common ancestor dating back to at least the capuchin
monkey genus is conceivable. However, our results certainly need to be
strengthened by further research on more individuals and other species
of macaques to make a more reliable conclusion. Since only two Tonkean
macaques were compared to eight brown capuchins in both experiments,
alternative hypotheses of convergent evolution cannot be
completely ruled out. Thus, instead of looking at phylogenetic relatedness
only, our interest should go towards the socio-ecological aspects
that are characteristic of these species in order to improve our knowledge
about the development of such cognitive abilities during evolution.
Indeed, as example, many similarities were found between genus
Sapajus and Pan: long life spans, explorative and manipulative behaviours,
tool using, omnivorous diet, socially complex behaviours such
as coalitions and cooperation and so forth (Visalberghi & McGrew,
1997).
One of the major aims of this study was to compare performances of
monkey species with those of chimpanzees (Krachun et al., 2016) using
a same experimental paradigm. Like chimpanzees, brown capuchins
performed high scores in the two AR experiments and passed each test
within a small amount of sessions. Not all of them succeeded but the
proportion of successful brown capuchins is still greater than observed
in chimpanzees. Hence, the performance of brown capuchins is likely to
be comparable to those of chimpanzees in these AR discrimination
experiments. It brings more evidence that monkeys can perform like
apes in demanding cognitive tasks, for example like prerequisite ToM
tests, contrary to previous scientists’ common beliefs. These previous
studies that found differences between performances of monkeys and
apes in cognitive tasks, have normally compared apes that are highly
habituated to experiments with naive monkeys (Amici et al., 2010). In
addition to using similar standardized paradigm, our study tested
highly habituated monkeys. Thereby, a comparison between our results
and those on chimpanzees appears more reliable and appropriate.
Several recent studies on cognitive abilities comparing different
monkey and ape species found no strong evidence of a difference between
their performances (Amici et al., 2010; Meunier, 2017; Schmitt
et al., 2012; Tomasello et al., 1998). Instead, Amici et al. (2010) revealed
a link in their results between cognitive capacities and social
organisation: performances of species living in systems with fissionfusion
dynamics (e.g. chimpanzees, bonobos, orangutans, and spider
monkeys) exceeded those of species living in more stable groups (e.g.
long-tailed macaques, gorillas and capuchin monkeys). Thereby, the
type of social organisation seems to impact the physico-cognitive skills
of primates (i.e. spatial memory, quantities, causality, etc.) and may
provide better predictor of performance in some cognitive tasks than
phylogenetic relatedness (Schmitt et al., 2012). This led to the development
of the social intelligence hypothesis, which claims that primate
intelligence evolved in response to challenges of living in large and
complex groups (Byrne & Bates, 2010; MacLean et al., 2012; Schmitt
et al., 2012). However, both for Tonkean macaques and brown capuchins,
this explanation does not apply because they are not living in
fission-fusion dynamics but instead in stable female-bonded groups
with comparable social complexity, and are described as socially tolerant
(Hare et al., 2003). These other social features could then interfere
in their cognitive abilities’ development. Thus, as socio-ecological
conditions might better explain the presence of some cognitive abilities,
instead of comparing monkeys and apes, we should focus on comparison
between particular species. Studying with the same paradigm other
nonhuman primates either closely related or presenting different social
organisations (e.g. lemurs, white-faced capuchins, or long-tailed macaques)
should provide insights about the origin of this ability and
could help to clarify the social intelligence hypothesis (Byrne & Bates,
2010; Humphrey, 1976; MacLean et al., 2012; Schmitt et al., 2012).
The positive results in both experiments could be explained by
several alternative mechanisms of learning. First of all, an association
learning between large or big food item and negative outcome could be
a possibility. However, it seems to be an unlikely explanation because
our successful subjects have chosen the item that appeared larger or
bigger in the avoid tests, and they continued to choose the bigger or
larger amount of items in each warm up preference trials before each
session. Secondly, some might argue that successful individuals could
have done reverse contingency learning, i.e. choose the smaller food
item to obtain the larger one. However, this assumption is highly unlikely
for the following reasons. First, the avoid control test clearly rules
out this possibility. In fact, to validate this control, subjects needed to
choose the apparent bigger or larger food item to obtain the truly bigger
or larger one, and not the apparent smaller one as in previous tests.
Second, several studies have already demonstrated that this type of
contingency learning for both size and quantity of items is really difficult
for these species, even for great apes, and require hundreds of
trials to succeed in it (Anderson, Hattori, & Fujita, 2008; Boysen,
Berntson, & Mukobi, 2001; Krachun et al., 2009; Vlamings, Uher, &
Call, 2006).
In the Lens experiment, a few subjects did not succeed in different
tests. First, a significant left pointing bias can explain the failure of two
brown capuchins, one in the basic and the other one in the seen
tracking test. The fact that this bias was not present in the initial conditions
might indicate they do not understand the situation in the
follow-up conditions and thus could also suggest that a more ecological
procedure may have been necessary for these individuals for AR discrimination
to be revealed. Second, Tonkean macaques and brown capuchins
seem to have failed the Lens experiment in the last learning
control because they have performed learning strategies based on different
stimuli. Two Tonkean macaques and one brown capuchin obtained
really low scores, demonstrating a significant preference for the
truly smaller grape. This could be explained by a learning process to
avoid the magnifying lens or to choose the grape that appeared with the
size of the small one through the lenses. The other five unsuccessful
Tonkean macaques and one brown capuchin obtained medium scores,
which reflect a learning to choose the minimizing lens or the grape that
appeared with the size of the bigger one through the lenses. Because
neither the minimizing lens nor the grape appearing the size of the
bigger one through lenses were no more available in this control, individuals
could not anymore use these stimuli to succeed and so they
chose randomly. Moreover, these individuals who failed the test still
choose preferentially the bigger grape in warmup preference trials
before each session, suggesting their failure was not due to a change of
preference to smaller grapes.
In order to compare performances with those of chimpanzees, we
carried out a second avoid-lens test at the end of the Lens experiment
using exactly the same procedure as Krachun et al. in their study of
2016. Tonkean macaques’ results obtained in the avoid-lens test n°2 are
quite inconsistent with those of avoid-lens test n°1. In fact, one individual
succeeded in both but two individuals that failed avoid-lens
test n°1 then succeeded in the avoid-lens test n°2, within one or two
sessions only. For these two subjects, we carried out one more session
with the unseen test procedure, in order to check whether by changing
again sizes and lenses used, they will succeed (as before in the same
unseen tracking test) and thus demonstrate a truly understanding of the
illusion phenomena. However, both of them drastically failed by never
choosing the truly larger grape in this session. These results highlight a
learning strategy they must have developed during the four sessions of
the avoid-lens test n°1. Because avoid-lens test n°2 was carried out after,
individuals had the possibility to learn the new rule (larger grape
placed behind magnifying lens). In addition, the only subject that
passed the first avoid-lens control test needed four sessions to succeed
in this last control. His result should be interpreted with caution because
he could have also learned, faster than the others, i.e. within only
three sessions. Surprisingly, the other Tonkean macaques and brown
capuchins that have failed did not realise this potential quick learning:
they both failed the avoid-lens n°1 and the avoid-lens n°2. A comparison
between avoid-lens n°1 performances of Tonkean macaques and brown
capuchins with avoid-lens test performances of chimpanzees in the
study of Krachun et al. (2016) seems thus more reliable.
Instead of an absence of AR discrimination, individuals’ failure
could be interpreted by other explanations corresponding to methodological
issues like too many experimenter’s manipulations or isolation
from their social group. Our test procedure could have required too
much concentration, motivation and short-term memory for these animals,
difficulties faced by Krachun et al. (2016) in their study on
chimpanzees. Notably, poor performances of Tonkean macaques (poor
success ratio, higher means of sessions to succeed in each test) compared
to brown capuchins and chimpanzees may support this assumption:
as we carried out half-sessions for brown capuchins, they had
twice as many demo trials as Tonkean macaques and chimpanzees,
hence more opportunities to understand the effects of stimuli illusion.
Moreover, all brown capuchins came to the experimental room at least
once per day, whereas with some Tonkean macaques, several days
sometimes separated two successive sessions because they did not come
back in the experimental room regularly. Because of those delays,
Tonkean macaques might have faced memory challenges about the
impact of illusion. Our results could thus underestimate their AR discrimination
ability.
Given the pointing bias of some brown capuchins and the large
failure of Tonkean macaques in the Lens experiment, ecological relevance
of our paradigm has to be questioned. The better success ratio
in the Mirror experiment could be due to the applied illusion. The
mirror effect indeed creates a false presence of two raisins, which do not
exist in reality. Whereas lens is modifying properties of grapes that
already exist, it does not create new food items. Thereby, it is maybe
easier to understand the effect of a mirror than the subtle modification
of existent items created by lenses. One alternative paradigm to test size
illusion understanding could be the one developed by Karg et al.
(2014). In their comparative study between great apes and children on
AR discrimination, they created a size illusion using completion illusion,
i.e. part of an object is partially occluding by another, in order to
inverse size relation. As Tonkean macaques and brown capuchins are
semi-arboreal primates, they might more regularly face size illusion
challenges by completion illusion because of the dense vegetation in the
canopy rather than by distortion.
Further research using different complementary types of illusion,
e.g. colour or auditory illusions, could now bring more information
about the scope of the AR understanding of these species. Another
notable result is that several capuchins of various ages succeeded. Thus,
AR discrimination ability seems to appear early in the development of
brown capuchins. Further experiences on even younger individuals will
be helpful to determine if the development of AR discrimination occurs
around the same development stage as for human children and with the
same developmental pattern (e.g. Hansen & Markman, 2005; Karg
et al., 2014; Moll & Tomasello, 2012).
To conclude, our results support those of apes, demonstrating that
this AR discrimination ability is not unique to great apes. As we have
now demonstrated that even some monkey species seem to possess this
understanding, it seems these abilities are perhaps more evolutionary
ancestral than previously thought. More research on different monkey
species with similar standardized procedure is now more than ever
necessary to better understand evolution of our remarkable social
cognition.