Hand preferences in Barbary macaques
Vanessa Schmitt, Sandra Melchisedech, Kurt Hammerschmidt,
and Julia Fischer
German Primate Center, Go ¨ttingen, Germany
Nearly 90% of humans are right-handed, raising the question of the evolutionary
origins of this trait. While lateralisation of certain actions appears to be widespread
in vertebrates, the question of whether nonhuman primates exhibit hand
preferences at the population level is often contested. We observed Barbary
macaques (Macaca sylvanus) living in the outdoor enclosure ‘‘La Fore ˆt des Singes’’
at Rocamadour, France, while performing simple unimanual and coordinated
bimanual tasks. For the unimanual task, we recorded continuously which hand they
used reaching for grains. For the coordinated bimanual tasks, a semi-transparent
box and a tube baited with peanut butter were presented to the macaques and the
hand used to open the box or reach into the tube, respectively, was recorded. We
found no significant hand preference in any of the tasks at the population level, but
found individual hand preferences, the extent of which varied among individuals.
For the unimanual, but not the bimanual task, we found that the handedness index
increased with age. Our results add to the growing body of evidence that monkeys
do not show hand preference at the population level.
About nine out of ten humans primarily use their right hand when they
perform tasks with one hand (Annett, 1985). However, such estimations are
usually based on measures of tool use, and observations of everyday
activities do not show such a strong bias (Marchant, McCrew, & Eibl-
Eibesfeldt, 1995). Different theories have been developed to explain this
‘‘right shift’’ in humans, taking into account the asymmetry of the inner
organs as well as effects of learning, or the influence of genes (Annett, 1985,
2002). Most vertebrates (Flowers, 1975), including amphibians (Bisazza,
Cantalupo, Robins, Rogers, & Vallortigara, 1996; Bisazza, Cantalupo,
Robins, Rogers, & Vallortigara, 1997), show a certain amount of hand or
Address correspondence to: Vanessa Schmitt, Research Group Cognitive Ethology, German
Primate Center, Kellnerweg 4, D-37077 Go ¨ttingen, Germany. E-mail: firstname.lastname@example.org
We thank Anika Dreier, Katharina Peters, and Tina Jensen, who conducted the second part of
the study in the outdoor enclosure ‘‘La Fore ˆt des Singes’’ in Rocamadour, France.
LATERALITY, 2008, 13 (2), 143?157
#2008 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business
leg preference for specific activities. From toads and tortoises (Robins,
Lippolis, Bisazza, Vallortigara, & Rogers, 1998; Stancher, Clara, Regolin, &
Vallortigara, 2006) to birds (Rogers & Workman, 1993) and dogs (Quaranta,
Siniscalchi, Frate, & Vallortigara, 2004), nearly all vertebrates exhibit a
preference for one limb. In some species, preferences are found not only on
the individual level but also at population level, for instance in rats (Gu ¨ven,
Elalmis, Binokay, & Tan, 2003). Recently, the hypothesis has been put
forward that hand or leg preferences reduce the cognitive effort for action
planning and initiation. Automated hand or leg preferences are supposed to
save the time and energy needed for coordination; thus, a reliable preference
for a certain hand or leg could be advantageous (Papademetriou, Sheu, &
Michel, 2005). McGrew, Marchant, Wrangham, and Klein (1999) provided
evidence for this hypothesis as they showed that chimpanzees with an
asymmetry in hand usage were more efficient in termite fishing than
ambidextrous animals. However, this lateralisation at the individual level
provides no explanation for the emergence of population-level biases,
because increased individual efficiency is not related to the adjustment of
lateralisation at the population level (Ghirlanda & Vallortigara, 2004).
Some anthropologists assume that the preference for the right hand in our
ancestors can be traced back to more than 1.8 million years ago (McManus,
2002). This assumption is based on evidence of tools utilised at that time
(Annett, 1985). In addition, handedness has been linked to hemispheric
lateralisation of the brain. In right-handed people, the left hemisphere is
predominant for speech processing and also controls the motor activity of
the right hand. Possibly, handedness paved the way for the areas that control
speech production, particularly if one assumes that speech may have evolved
via gestural communication (Arbib, 2005; Corballis, 2002). Corballis (2003)
proposed that first humans communicated via gestures, then added vocal
elements until speech was fully developed. In conclusion, the investigation of
the origin of handedness in humans may contribute to an understanding of
the origins of speech as well (MacNeilage, Studdert-Kennedy, & Lindblom,
However, handedness may have evolved earlier than in the human lineage.
A number of studies have addressed the issue of hand preferences in
nonhuman primates (e.g., Box, 1977; Deuel & Dunlop, 1980; Fletcher, 2006;
Hopkins, 1993; Hopkins, Wesley, Russell, & Schapiro, 2006; Kubota, 1990;
Lonsdorf & Hopkins, 2005; Meunier & Vauclair, 2007; Singer & Schwibbe,
1998; Tokuda, 1969). Most of these studies reported handedness at an
individual level. Whether or not nonhuman primates exhibit handedness
at the population level is still a controversial issue. Current evidence suggests
a population specific right-hand bias in chimpanzees, Pan troglodytes
(Hopkins, 1993; Hopkins et al., 2006). Captive chimpanzees have shown a
2:1 distribution of right-handedness in captive chimpanzees (Hopkins, 1993;
SCHMITT ET AL.
Hopkins et al., 2006). Recently, this finding was replicated in wild
chimpanzees (Lonsdorf & Hopkins, 2005). Rhesus monkeys, M. mulatta,
were found to exhibit a preference for the left hand (Westergaard & Lussier,
1999; but see Papademetriou et al., 2005). In summary, the degree of
handedness appears to vary between different primate species (Vallortigara
& Bisazza, 2002), with an indication of population-level hand preferences in
chimpanzees, but not monkeys (Annett, 1985).
It has also been suggested that the degree of handedness at the population
level might be related to the complexity of the task. Fagot and Vauclair
(1991) suggested that hand preferences at the population level may only
become apparent when more complex or novel bimanual tasks are used. In a
task similar to the tube task conducted by Hopkins with chimpanzees, where
the subjects held a short PVC pipe with one hand while extracting peanut
butter from it with the other, Spinozzi, Castorina, and Truppa (1998)
detected a significant increase in right-hand use from the unimanual
quadrupedal reaching task to the coordinated bimanual task in capuchin
monkeys. Westergaard and Soumi (1996) found a population-level bias
towards use of the right hand in a tube task in rhesus monkeys but not in
capuchin monkeys, Cebus apella. These findings support the idea that an
ancient basis exists in primate evolution for right-hand preferences in
In our study, we aimed to expand the evidence for hand preferences in
Old-world monkeys. We analysed the use of the right vs the left hand in a
unimanual and two different coordinated bimanual tasks in Barbary
macaques. For the unimanual task, handedness was assessed by observing
simple reaching for grains. For the bimanual task, we observed which hand
subjects used to open a plastic box, and which they used to retrieve a peanut
and peanut butter from a plastic tube. We expected no handedness at the
population level, but some preferences at the individual level. Following
Fagot and Vauclair, we expected a right-hand preference in the coordinated
As handedness has frequently been linked to hemispheric lateralisation in
the brain, we also compared our observations of hand preferences to a recent
study of orienting asymmetries in this species. Orienting asymmetries have
been viewed as an expression of lateralised processing of acoustic stimuli (for
reviews, see Teufel, Hammerschmidt, & Fischer, 2007; Weiss, Ghazanfar,
Miller, & Hauser, 2002). Rhesus macaques, for instance, exhibit a right head-
turning bias in response to playbackof natural conspecific vocalisations, and
a left head-turning bias in response to one heterospecific stimulus and
several manipulated conspecific calls (Hauser & Agnetta, 1998; Hauser &
Andersson, 1994; Ghazanfar, Smith-Rohrberg, & Hauser, 2001). This
finding was related to a hemispheric specialisation for processing conspecific
versus heterospecific vocalisations. A recent study on orienting asymmetries
HAND PREFERENCES IN BARBARY MACAQUES
in Barbary macaques did not find preferred head turns in response to
conspecific or heterospecific sounds played from 1808 behind the animal
(Teufel et al., 2007). However, it is possible that within an individual,
orienting asymmetries are linked to hand preferences. Therefore, we also
assessed the contingency of individual hand preference and head turning in
We conducted this study on Barbary macaques living in the outdoor
enclosure ‘‘La Fore ˆt des Singes’’ in Rocamadour, France. The individuals
inhabit an area of 15 hectares and are divided into three groups (GB, PB,
VOL). For observing the unimanual task, we followed 52 different
individuals, 25 from the GB group (5 males, 20 females) and 27 from the
PB group (11 males, 16 females). The coordinated bimanual task consisted
of two experiments. In Experiment 1, the box task, we observed 41 animals
from all three groups (21 males, 20 females). In Experiment 2, the tube task,
we observed 30 animals from all three groups (15 males, 15 females). All
individuals were aged between 4 and 26 years.
The observations were carried out during 10 days in May 2006. We observed
each of the 52 individuals picking up pieces of grain from the ground. The
hand used was recorded continuously until a sequence of 100 food reaches
per animal had been made. We made sure that the individual was in a
position that did not afford the use of a special hand (e.g., resting on the
side), so that it was certain the animal could use both hands equally and
flexibly. The sequences were recorded on tally sheets to also note alterations
of hand use (changes from left hand use to right or vice versa). A sequence
was finished when the 100 picks were achieved or when the individual
interrupted its foraging activity for more than 60 seconds, respectively. In the
latter case, we discarded the sequence and started a new one, to make sure
that we recorded one entire sequence for each of the 52 individuals. To assess
handedness at the individual level, we observed 20 of the 52 individuals for
an additional six sequences (a total of seven sequences per individual).
Additionally, we noted for these 20 animals the preferred hand use for other
behaviour patterns, like scratching with one hand, grooming, picking up
objects (e.g., fruits), or taking popcorn from tourists. We did not gather
sufficient data points from these observations to allow further analysis.
SCHMITT ET AL.
The observations were carried out in May 2007. Two experiments were made
to test if handedness is shown in coordinated bimanual tasks.
coloured opaque lid (standard ‘‘Tupperware’’ lunch box) was attached to a
rope (to prevent the animals taking the box and walking away) and baited
with a peanut. It was placed in front of the test subject so that the animal
had the opportunity to open it and obtain the reward. Animal responses
were filmed on video (Sony DCR-HC90E) and later analysed on a frame-by-
frame basis. To assess handedness, we recorded with which hand the box was
touched first, as well as the time it took from the first touch until the peanut
was taken. We counted every touch on the box with the right and left hand,
respectively, during the whole session. When opening the box, we noted
which hand was used to push the lid of the box (‘‘push hand’’), and which
was used for holding the box.
A semi-transparent plastic box (size 15?15?8 cm) with a
containing peanut butter and a peanut was attached to a rope. The tube was
then put in front of each individual. We recorded with which hand the
subjects first touched the tube, and which hand was used and inserted to
actively remove the peanut butter and nut from the inside of the tube
(referred to as ‘‘preferred hand’’).
A 0.2-m long polyvinyl-chloride (PVC) tube (diameter 4 cm)
population level, each individual was categorised as either left- or right-
handed, irrespective of the degree of individual handedness. We used a
binomial test (SPSS 10.0) to test for preferences at the population level. For
this analysis, we used only one sequence from those individuals that were
observed repeatedly (the first). To assess the degree of handedness, we
calculated a manual preference index for each individual as follows:
For statistical analysis of hand preferences at the
HI?R ? L
R ? L
where R represents the number of times the right hand was used, and L the
number of times the left hand was used (Alonso, Castellano, & Rodriguez,
1991). The Handedness Index (HI) reveals the direction of manual
preference and varies continuously from ?1 (totally left-handed) to ?1
(totally right-handed). Its absolute value, ABS-HI, indicates the strength of
preference without taking the direction of preference into account. We used
HAND PREFERENCES IN BARBARY MACAQUES
the Kolmogorov-Smirnov Test to assess whether the distribution of the
Handedness Index differed significantly from a normal distribution.
For the subjects that were observed repeatedly, each sequence was defined
as a ‘‘right preference’’ or ‘‘left preference’’ sequence, respectively. We then
used a binomial test to examine within-subject preferences. To correct for
multiple testing, we applied the Step-up Hochberg procedure (Westfall &
Young, 1993). To assess individual consistency of hand preferences, we first
calculated the preference within each sequence and then calculated the
coefficient of variation across the seven sequences (SD/mean). We also
examined whether the average Handedness Index values for these 20 subjects
differed significantly from a normal distribution, using the Kolmogorov-
Smirnov Test. We analysed the correlation between the number of
alterations and a strong or weak hand preference, respectively, (ABS-HI)
using the program Statistica 6.0. To test if age has an effect on hand
preference, we used the Pearson Correlation test. Sex differences were
assessed with the Mann-Whitney U test. To compare hand preferences with
orienting asymmetries (Teufel et al., 2007), we used the chi-square test to
assess the contingency between hand preference and the direction of head-
turn. This was possible for a total of 19 individuals that took part in both
right-handed regarding the ‘‘push hand’’ in the box task and the ‘‘preferred
hand’’ in the tube task, respectively. To test for laterality at the population
level, we used the binomial test. As we observed only one occasion of lifting
the lid of the box for every individual, we determined the Handedness Index
only for the tube task, using the number of times the fingers of the left or
right hand were inserted, respectively, into the tube. We used the
Kolmogorov-Smirnov Test to assess whether the distribution of the
Handedness Index differed significantly from a normal distribution. To
test if age has an effect on the hand preferred, we used a Pearson correlation
coefficient. Whether sex has an effect on hand preference was tested with the
Mann-Whitney U test.
First we categorised all individuals as either left- or
At the population level, we found no significant preference for the right or
left hand (Binomial test, N?52; p?.890). A total of 48% of the animals
favoured the right hand, 52% the left. Figure 1 shows the distribution of the
Handedness Index (HI) within one sequence for each individual. The mean
Handedness Index score for this task was 0.11 (SE?0.075). A one-sample
SCHMITT ET AL.
t-test revealed that overall HI scores did not differ significantly from a
chance distribution with a mean of 0, t(52)?1.52, p?.134. The study
revealed a normal distribution with an approximately equal number of left-
and right-handers. While some individuals showed a strong preference for
the left or right hand, respectively, there were also several individuals with no
within-sequence hand preference. Overall, this distribution did not differ
significantly from a normal distribution (Kolmogorov-Smirnov Test: N?52,
p?.783). At the individual level, four subjects revealed a significant
preference for the right hand (p?.016), and three subjects for the left
hand (p?.016). The remaining 13 individuals showed no significant
preferences. However, after correction for multiple testing, none of the
p-values remained significant (all p?.16).
We found a significant negative correlation between the degree of hand
preference (ABS-HI) and intra-individual variation (CV) in hand use
(Pearson r??.826, N?20, pB.001). For instance, a subject that used
the left hand consistently within one sequence tended to use the left hand
preferentially in all sequences. Conversely, subjects who used both hands in
one sequence also showed a high degree of intra-individual variation across
sequences (Figure 2). Overall, the distribution of the Handedness Index for
these 20 subjects did not differ significantly from a normal distribution
(Kolmogorov-Smirnov Test: N?20, p?.931); mirroring the results of the
We also observed a significant negative correlation between the number of
alterations of hand use and absolute Handedness Index (ABS-HI) (Pearson
r??.66, N?52, pB.001). Individuals with a high degree of hand
preference showed few hand changes, while subjects with a low degree of
Hl unimanual task
A value of ?1 stands for fully left-handed, a value of ?1 stands for fully right-handed.
Unimanual task: Handedness Index (HI) at population-level for each of the 52 individuals.
HAND PREFERENCES IN BARBARY MACAQUES
hand preference varied in their number of alterations. During our observa-
tions, we noticed a decrease in the number of alterations with increasing age.
Individuals older than 20 years changed their hands very seldom, whereas the
number of alterations was higher in younger macaques (Pearson r?.61, N?
52, pB.001). This tendency was also shown in the strength of handedness,
which increased with age (Pearson: r?.44, N?52, p?.001) (Figure 3). We
found no significant difference between the sexes, neither in direction of hand
preference (U?202.5, N1?36, N2?16, p?.090) nor in the strength of
handedness (U?268, N1?36, N2?16, p?.702). Finally, there was no
significant relationship between the direction of head turn in a previous
playbackexperiment and individual hand preference (n?19, x2?0.540, df?
1, p?.463). Of the eight individuals that had turned right, five preferentially
used the left hand and three the right hand; of the eleven individuals that had
turned left, six preferentially used the left hand and five the right.
For the box task, we analysed only 28 of the 41 observed animals, as 10
animals failed to open the box and 3 animals opened it with the mouth. For
the tube task, we analysed 28 of 30 individuals, as 2 of the subjects did not act
on the tube after the first touch. We found no significant preference for the
right or left hand at the population level, neither in the box task (Binomial
test, N?28, p?.286) nor in the tube task (Binomial test, N?28, p?.172).
Figure 4 shows the distribution of the Handedness Index (HI) for each
individual in the tube task. The distribution of handedness does not differ
Coefficient of Variation
Variation and ABS-HI. For each of the 20 individuals, the coefficient is plotted against the Absolute
Consistency of hand preferences: Correlation analysis concerning the coefficient of
SCHMITT ET AL.
significantly from a normal distribution (Kolmogorov-Smirnov Test: N?28,
p?.234). The mean HI score for the tube task was ?0.098 (SE?0.134). A
one-sample t-test revealed that overall HI scores do not differ significantly
from a chance distribution, with a mean of 0, t(27)??0.73, p?.467.
Neither age nor sex had an effect on hand preference in the tube task (age:
r??.058, N?28, p?.766; sex: U?94.5, N1?.14, N2?14, p?.874), and
age and sex did not influence the strength of laterality either (age: r?.116,
N?28, p?.557; sex: U?71, N1?14, N2?14, p?.227).
HI tube task
fully left-handed, a value of ?1 stands for fully right-handed.
Tube task: Handedness Index (HI) for each of the 28 individuals. Avalue of ?1 stands for
19 23 27
handedness (ABSHI). For each individual (points), the age is plotted against the Absolute
Influence of age on ABSHI: Correlation analysis concerning the age and the strength of
HAND PREFERENCES IN BARBARY MACAQUES
We did not find a significant hand preference at the population level in the
group of Barbary macaques we observed, neither in the unimanual nor in the
coordinated bimanual task. The population of Barbary macaques showed a
balanced distribution of individual right and left hand preference for picking
up the pieces of grain and removing peanuts from a tube and box,
respectively. In contrast to Hopkins and his colleagues (1993, 2006) and
Westergaard and Suomi (1996), who found a hand bias for chimpanzees and
rhesus macaques, our results add to the body of studies that failed to find
handedness in non-human primates (see overview in Papademetriou et al.,
At the individual level, we found significant hand preferences for some of
the animals we observed. Of the 20 animals observed repeatedly in the
unimanual task, 3 individuals revealed a significant bias for the left hand,
and 4 individuals for the right hand. As the distribution of the Handedness
Index does not differ significantly from a normal distribution, this was to be
expected. Notably, after correcting for multiple testing, none of the
individual preferences remained significant. The same tendency could be
observed for the coordinated bimanual task, showing that the complexity of
the task does not influence hand preference.
Furthermore, a conspicuous aspect in our results is the fact that, at least
for the unimanual task, we found a strong hand preference significantly
more often for older individuals, who changed between hands less frequently
than younger ones. While longitudinal studies are needed to explore the
consolidation of individual lateralisation in motor tasks, these results
tentatively suggests a positive feed-forward mechanism where increasing
practice with one hand leads to increased use of that hand. All in all, we
found a significant correlation between the alteration of hands and the
extent of handedness. Obviously, individuals that have a strong bias for one
hand will not show many changes in hand use. However, individuals with a
low degree of hand preference showed both frequent and few alterations
within a sequence. Therefore, a larger degree of hand preference cannot
simply be explained by a lower tendency to switch between hands.
We found no significant correlation between the preferred hand and the
direction of head-turn as examined by Teufel and colleagues (2007), refuting
the hypothesis that orienting asymmetries might be linked to handpreference.
Although rhesus macaques (Macaca mulatta) do exhibit significant orienting
asymmetries, there was also no link between an individual’s orienting and its
hand preference (Hauser & Andersson, 1994). Thus, although hand pre-
ference at the population level is rarely found in monkeys, many studies have
shown that these species exhibit hemispheric lateralisation (Gil-da-Costa
et al., 2004; Inoue, Mikami, Ando, & Tsukada, 2004; Poremba, 2006;
SCHMITT ET AL.
Vallortigara & Rogers, 2005). Apparently, even some invertebrates exhibit
brain lateralisation (Letzkus et al., 2006). Thus, the phenomenon of
lateralised brain functions has presumably evolved several times indepen-
dently, and hemispheric lateralisation does not necessarily seem to be linked
with handedness (see for example Hook-Costigan & Rogers, 1998).
In summary, we detected a hand preference in Barbary macaques at an
individual level, but not at the population level. According to the
assumptions of Fagot and Vauclair (1991), we should have found stronger
hand preferences in the complex bimanual task. They argued that only
complex or novel tasks could reveal a bias at the population level and cause
significant hand biases, while basic activities are not correlated with the
lateralisation of the brain. Blois-Heulin, Guitton, Nedellec-Bienvenue,
Ropars, and Vallet (2006) supply evidence for this assumption, as they
found hand preferences at the population level in red-capped mangabeys,
Cercocebus torquatus torquatus. The number of monkeys with hand
preferences and the strength of the preference increased with the complexity
of the tasks. However, a recent study on chimpanzees showed that ant
fishing, a highly complex task, also revealed no hand preferences at the
population level (Marchant & McGrew, 2007), indicating a greater degree of
variability between species and tasks than initially assumed.
The fact that only a few studies found hand preference at a population
level in primates may be due to the fact that primate hand use did not
experience selective pressures during evolutionary history, forcing them to
adjust their individual asymmetries to group lateralisation. In contrast, fish
(De Santi, Sovrano, Bisazza, & Vallortigara, 2001), toads (Lippolis, Bisazza,
Rogers, & Vallortigara, 2002), and chickens (Evans, Evans, & Marler, 1993)
react faster to predators approaching from the left, showing a population-
level left-side bias. This population-level bias may have evolved as
‘‘evolutionary stable strategy’’ (Ghirlanda & Vallortigara, 2004; Vallortigara
& Rogers, 2005). Populations consisting of left- and right-type individuals in
unequal number can be evolutionary stable if being lateralised in one or the
other direction has frequency-dependent costs and benefits (Raymond,
Pontier, Dufour, & Moller, 1996). If there is no selective pressure,
individuals can benefit from their individual asymmetry in the absence of
population-level lateralisation. Faurie and Raymond (2005) suggest further
that human handedness evolved just because of selective pressures. Left-
handers suffer from fitness costs (see Aggleton, Kentridge, & Neave, 1993;
Coren & Halpern, 1991), but benefit from advantages in fights and, today,
in sport (Raymond et al., 1996). Because of these costs and benefits, a stable
quantity of left-handers is maintained in current populations. Faurie and
Raymond (2005) discovered a positive correlation between the frequency of
left-handers and the level of violence across different cultures. Therefore, it
seems reasonable at least to consider evolutionary stable strategies when
HAND PREFERENCES IN BARBARY MACAQUES
arguing about the reasons for lateralisation of organisms. MacNeilage
(2006) suggested that there may be a left-hemispheric specialisation for
whole-body control, for example, in approaching behaviour. His hypothesis
follows from Vallortigara and Rogers’ (2005) survey of a large array of
studies in fish, amphibians, and birds. According to Vallortigara and
Rogers, the left hemisphere controls responses that require considered
discrimination between stimuli and manipulation of objects, and they state
that this specialisation is manifested in hand preferences in primates. The
human right-handedness may have arisen from this ancient evolutionary
Obviously such theories are difficult to evaluate empirically. Future
research might benefit from clarifying the neural circuits underlying
handedness, as well as the emergence of hand preferences during ontogenetic
development, to shed more light on the origins of the intriguing phenom-
enon of population-level handedness.
Manuscript received 26 January 2007
Revised manuscript received 20 September 2007
First published online 1 February 2008
Aggleton, J. P., Kentridge, R. W., & Neave, N. J. (1993). Evidence for longevity differences between
left handed and right handed men: An archival study of cricketers. Journal of Epidemology and
Community Health, 47, 206?209.
Alonso, J., Castellano, M. A., & Rodriguez, M. (1991). Behavioural lateralisation in rats: Prenatal
stress effects on sex differences. Brain Research, 539, 45?50.
Annett, M. (1985). Left, right, hand and brain: The right shift theory. Hove, UK: Lawrence Erlbaum
Annett, M. (2002). Myths of first cause and asymmetries in human evolution. Behavioural and
Brain Research, 26, 208?209.
Arbib, M. (2005). From monkey-like action recognition to human language: An evolutionary
framework for neurolinguistics. The Behavioral and Brain Sciences, 28, 105?167.
Bisazza, A., Cantalupo, C., Robins, A., Rogers, L. J., & Vallortigara, G. (1996). Right-pawedness in
toads. Nature, 379, 408.
Bisazza, A., Cantalupo, C., Robins, A., Rogers, L. J., & Vallortigara, G. (1997). Pawedness and
motor asymmetries in toads. Laterality, 2, 49?64.
Blois-Heulin, C., Guitton, J. S., Nedellec-Bienvenue, D., Ropars, L., & Vallet, E. (2006). Hand
preference in unimanual and bimanual tasks and postural effect on manual laterality in captive
red-capped mangabeys (Cercocebus torquatus torquatus). American Journal of Primatology, 68,
Box, H. O. (1977). Observations on spontaneous hand use in the common marmoset (Callithrix
jacchus). Primates, 18(2), 395?400.
Corballis, M. C. (2002). From hand to mouth. Princeton, NJ: Princeton University Press.
Corballis, M. C. (2003). From mouth to hand: Gesture, speech, and the evolution of right-
handedness. The Behavioral and Brain Sciences, 26, 199?208; discussion 208?260.
SCHMITT ET AL.
Coren, S., & Halpern, D. F. (1991). Left-handedness: A marker for decreased survival fitness.
Psychological Bulletin, 109, 90?106.
De Santi, A., Sovrano, V. A., Bisazza, A., & Vallortigara, G. (2001). Mosquitofish display
differential left- and right-eye use during mirror-image scrutiny and predator-inspection
responses. Animal Behaviour, 61, 305?310.
Deuel, R. K., & Dunlop, N. L. (1980). Hand preferences in the rhesus monkey: Implications for the
study of cerebral dominance. Archives of Neurology, 37, 217?221.
Evans, C. S., Evans, L., & Marler, P. (1993). On the meaning of alarm calls: Functional reference in
an avian vocal system. Animal Behaviour, 46, 23?28.
Fagot, J., & Vauclair, J. (1991). Manual laterality in nonhuman primates: A distinction between
handedness and manual specialization. Psychological Bulletin, 109, 76?89.
Faurie, C., & Raymond, M. (2005). Handedness, homicide and negative frequency-dependent
selection. Proceedings of the Royal Society of London: Series B. Biological Sciences. 272, 25?28.
Fletcher, A. W. (2006). Clapping in chimpanzees: Evidence of exclusive hand preference in a
spontaneous, bimanual gesture. American Journal of Primatology, 68, 1081?1088.
Flowers, K. (1975). Handedness and controlled movement. British Journal of Psychology, 66,
Ghazanfar, A. A., Smith-Rohrberg, D., & Hauser, M. D. (2001). The role of temporal cues in
rhesus monkey vocal recognition: Orienting asymmetries to reversed calls. Brain Behavior and
Evolution, 58, 163?172.
Ghirlanda, S., & Vallortigara, G. (2004). The evolution of brain lateralisation: A game-theoretical
analysis of population structure. Proceedings of the Royal Society of London: Series B.
Biological Sciences. 271, 853?857.
Gil-da-Costa, R., Braun, A., Lopes, M., Hauser, M. D., Carson, R.E., Herscovitch, P., et al.
(2004). Toward an evolutionary perspective on conceptual representation: Species-specific calls
activate visual and affective processing systems in the macaque. Proceedings of the National
Academy of Sciences of the United States of America, 101, 17516?17521.
Gu ¨ven, M., Elalmis, D. D., Binokay, S., & Tan, U ¨. (2003). Population-level right-paw preference in
rats assessed by a new computarized food-reaching test. International Journal of Neuroscience,
Hauser, M. D., & Agnetta, B. (1998). Orienting asymmetries in rhesus monkeys: The effect of time?
domain changes on acoustic perception. Animal Behaviour, 56, 41?47.
Hauser, M. D., & Andersson, K. (1994). Left hemisphere dominance for processing vocalizations
in adult, but not infant, rhesus monkeys: Field experiments. Proceedings of the National
Academy of Sciences of the United States of America, 91, 3946?3948.
Hook-Costigan, M. A., & Rogers, L. J. (1998). Lateralised use of the mouth in production of
vocalizations by marmosets. Neuropsychologia, 25, 1267?1273.
Hopkins, W. D. (1993). Posture and reaching in chimpanzees (Pan) and orangutans (Pongo).
Journal of Comparative Psychology, 107, 162?168.
Hopkins, W. D., Wesley, M. J., Russell, J. L., & Schapiro, S. J. (2006). Parental and perinatal factors
influencing the development of handedness in captive chimpanzees. Developmental Psychobiol-
ogy, 48, 428?435.
Inoue, M., Mikami, A., Ando, I. & Tsukada, H. (2004). Functional brain mapping of the macaque
related to spatial working memory as revealed by PET. Cerebral Cortex, 14, 106?119.
Kubota, K. (1990). Preferred hand use in the Japanese macaque troop, Arashiyama-R, during
visually guided reaching for food pellets. Primates, 31, 393?406.
Letzkus, P., Ribi, W. A., Wood, J. T., Zhu, H., Zhang, S-W., & Srinivasan, M. V. (2006).
Lateralisation of olfaction in the honeybee Apis mellifera. Current Biology, 16, 1471?1476.
Lippolis, G., Bisazza, A., Rogers, L. J., & Vallortigara, G. (2002). Lateralisation of predator
avoidance responses in three species of toads. Laterality, 7, 163?183.
HAND PREFERENCES IN BARBARY MACAQUES
Lonsdorf, E. V., & Hopkins, W. D. (2005). Wild chimpanzees show population-level handedness for
tool use. Proceedings of the National Academy of Sciences of the United States of America, 102,
MacNeilage, P. F. (2006). Evolution of whole-body asymmetry related to handedness. Cortex, 42,
MacNeilage, P. F., Studdert-Kennedy, M. G., & Lindblom, B. (1987). Primate handedness
reconsidered. Behavioral and Brain Sciences, 10, 247?303.
Marchant, L. F., McCrew W. C., & Eibl-Eibesfeldt I. (1995). Is human handedness universal?
Ethological analysis from three traditional cultures. Ethology, 101, 239?258.
Marchant, L. F., & McGrew, W. C. (2007). Ant fishing by wild chimpanzees is not lateralised.
Primates, 48, 22?26.
McGrew, W. C., Marchant, L. F., Wrangham, R. W., & Klein, H. (1999). Manual laterality in anvil
use: Wild chimpanzees cracking Strychnos fruits. Laterality, 4, 79?87.
McManus, C. (2002). Right hand, left hand: The origins of asymmetry in brains, bodies, atoms and
culture. London: Weidenfeld & Nicolson.
Meunier, H., & Vauclair, J. (2007). Hand preferences on unimanual and bimanual tasks in white-
faced capuchins (Cebus capucinus). American Journal of Primatology, 69, 1?6.
Papademetriou, E., Sheu, C. F., & Michel, G. F. (2005). A meta-analysis of primate hand
preferences, particularly for reaching. Journal of Comparative Psychology, 119, 33?48.
Poremba, A. (2006). Auditory processing and hemispheric specialization in non-human primates.
Cortex, 42, 87?89.
Quaranta, A., Siniscalchi, M., Frate, A., & Vallortigara, G. (2004). Paw preference in dogs:
Relations between lateralised behaviour and immunity. Behavioural Brain Research, 153, 521?
Raymond, M., Pontier, D., Dufour, A., & Moller, A. P. (1996). Frequency-dependent maintenance
of left handedness in humans. Proceedings of the Royal Society of London B, 263, 1627?1633.
Robins, A., Lippolis, G., Bisazza, A., Vallortigara, G., & Rogers, L. J. (1998). Lateralised agonistic
responses and hindlimb use in toads. Animal Behaviour, 56, 875?881.
Rogers, L. J., & Workman, L. (1993). Footedness in birds. Animal Behaviour, 45, 409?411.
Singer, S. S., & Schwibbe, M. H. (1998). Right or left, hand or mouth: Genera-specific preferences
in marmosets and tamarins. Behaviour, 136, 119?145.
Spinozzi, G., Castorina, M. G., & Truppa, V. (1998). Hand preferences in unimanual and
coordinated-bimanual tasks by tufted capuchin monkeys (Cebus apella). Journal of
Comparative Psychology, 112, 183?191.
Stancher, G., Clara, E., Regolin, L., & Vallortigara, G. (2006). Lateralised righting behavior in the
tortoise (Testudo hermanni). Behavioural Brain Research, 173, 315?319.
Teufel, C. R., Hammerschmidt, K., & Fischer, J. (2007). Lack of orienting asymmetries in Barbary
macaques: Implications for lateralised auditory processing. Animal Behaviour, 73, 249?255.
Tokuda, K. (1969). On the handedness of Japanese monkeys. Primates, 10, 41?46.
Vallortigara, G., & Bisazza, R. J. (2002). How ancient is brain lateralisation? In L. J. Rogers & R. J.
Andrew (Eds.), Cerebral vertebrate lateralisation (pp. 9?69). New York: Cambridge University
Vallortigara, G., & Rogers, L. J. (2005). Survival with an asymmetrical brain: Advantages and
disadvantages of cerebral lateralisation. Behavioral and Brain Sciences, 28, 575?589; discussion
Weiss, D., Ghazanfar, A. A., Miller, C. T., & Hauser, M. D. (2002). Specialized processing of
primate facial and vocal expressions: Evidence for cerebral asymmetries. In L. J. Rogers & R. J.
Andrew (Eds.), Cerebral vertebrate lateralisation (pp. 480?530). New York: Cambridge
SCHMITT ET AL.
Westergaard, G. C., & Lussier, I. D. (1999). Left-handedness and longevity in primates.
International Journal of Neuroscience, 99, 79?87.
Westergaard, G. C., & Suomi, S. J. (1996). Hand preference for a bimanual task in tufted capuchins
(Cebus apella) and rhesus macaques (Macaca mulatta). Journal of Comparative Psychology, 110,
Westfall, P. H., & Young, S. S. (1993). Resampling-based multiple testing: Examples and methods for
p-value adjustment. New York: John Wiley & Sons.
HAND PREFERENCES IN BARBARY MACAQUES