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Hand preference in simple reaching among the Arashiyama West troop of Japanese macaques (Macaca fuscata)

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Hand preference in simple reaching among the Arashiyama West troop of Japanese macaques (Macaca fuscata)
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Forrester, Anastasia
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Denver, CO
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University of Colorado Denver
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English
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vi, 54 leaves : illustrations ; 29 cm

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Laterality ( lcsh )
Left- and right-handedness ( lcsh )
Japanese macaque ( lcsh )
Japanese macaque ( fast )
Laterality ( fast )
Left- and right-handedness ( fast )
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bibliography ( marcgt )
theses ( marcgt )
non-fiction ( marcgt )

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Bibliography:
Includes bibliographical references (leaves 46-54).
Thesis:
Submitted in partial fulfillment of the requirements for the degree, Master of Arts, Anthropology
General Note:
Department of Anthropology
Statement of Responsibility:
by Anastasia Forrester.

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|University of Colorado Denver
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|Auraria Library
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ocm37887163
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Hand Preference in Simple Reaching among the Arashiyama West Troop
of Japanese Macaques (Macaca Juscata)
by
Anastasia Forrester
B. A., University of Colorado at Denver 1990
A thesis submitted to the
University of Colorado at Denver
in partial fulfillment
of the requirements for the degree of
Master of Arts
Anthropology
1997


This thesis for the Master of Arts
degree by
Anastasia Forrester
has been approved
f by /r
Duane Quiatt
Date


Forrester, Anastasia (M. A., Anthropology)
Hand Preference in Simple Reaching among the Arashiyama West Troop of Japanese
Macaques (Macacafitscala)
Thesis directed by Professor Duane Quiatt
ABSTRACT
A free ranging troop of Japanese macaques {Macacafitscala), consisting of about 500 members
and residing in Dilley Texas, was observed from February to April of 1993. This study reports
on the hand preferences of Japanese macaques during visually guided reaching for food. Hand
preference was assessed for 317 bouts consisting of 10-105 reaches per bout. Hand preference
across gender was shown to be more pronounced among adult monkeys when compared to
younger monkeys (p=0.033). Adult males were shown to have a significant left hand bias
(p=0.0003) when compared with adult females. The presence of lateralized reaching is in
agreement with the literature pertaining to this species.
This abstract accurately represents the content of the candidateyihesis
publication.
Signed
ie Quiatt


DEDICATION
I dedicate this thesis to my mother for her unending support and belief in my ability, and
Trygve for helping find the chutzpah to finish.


ACKNOWLEDGMENT
I would like to thank the anthropology department at the University of Colorado at Denver, for
support during this research. Thanks also to Lou Griffin and Tracy Wyman of the South Texas
Primate Observatory for access to their facility and for assistance in conducting research.
Thanks also to Sean M. Mallory for assistance with the creation and interpretation of statistical
results. Deepest thanks to my thesis advisor and my committee.


CONTENTS
CHAPTER
1. INTRODUCTION__________________________________________1
Why is Manual Laterality Important?__________2
What is Manual Laterality?...................-3
2. BACKGROUND TO THE STUDY.......~m.................................6
Non-Primate Laterality..__________________________________________8
Primate Laterality_______________________________________________ 9
Japanese Macaque Studies.--------------------------------------- 14
METHODS__________________________________________ 19
Locale and Subjects----------------------- 20
Sample.. 23
Data Collection_____________________________27
Sampling Limitations........................29
RESULTS___________________________________________31
5. DISCUSSION AND CONCLUSION..................................................................40
APPENDIX
A. MONKEY FACE AND MATRIUNES___________44
BIBLIOGRAPHY
,46


CHAPTER 1
INTRODUCTION
Until the last decade there was a widely held belief that primates do not express manual
laterality, that they do not exhibit a greater tendency to use one hand or the other for any
particular task, or across any known set of tasks. Indeed, until ten years ago, this assumption
appeared to be upheld by the available data. It also fit nicely with the concept that humans are
somehow special, different in a fundamental biological sense from other animals. In this context
there was little motivation to collect new data or to further scrutinize existing data in search of
evidence for manual laterality in nonhuman primates. Yet even in the absence of data, such an
assumption is difficult to support given the apparent presence of lateral behavior in nonprimate
vertebrates. That assumption contradicts evolutionary parsimony and would require the de
novo development of lateralized behavior in humans. The goal of this research was to discover
if the Japanese macaques at Arashiyama West would show the same patterns of manual
laterality that have been observed for Japanese macaques elsewhere, as well as compare their
laterality patterns with those other primate species.
l


Why is Manual Laterality Important?
Among humans, lateralized behaviors have been correlated with a variety of cognitive
processes including some association with learning disabilities and autoimmune disorders.
Geshwind and Behan (1982) observed that left handed people had 10 times the rate of learning
disabilities, 2.5 times the rate of autoimmune disorders, and a higher incidence of migraines than
the general population. Such disorders also had a much higher incidence among the relatives of
left handers. Additionally, disorders such as dyslexia, stuttering and autism are found in higher
proportion among left handers than among right handers (Durden-Smith and Desimone 1983).
This lends strong support to an intimate connection between lateralized behavior and numerous
cognitive and physiological processes in humans.
There are several reasons why the existence of laterality in nonhuman primates is
important. First, knowledge about whether the brain functions responsible for laterality are
specific only to humans, or are possessed by nonhuman animals as well, can be useful in
designing studies for which nonhuman subjects are used in lieu of human subjects. Second,
evolutionary models can be improved upon when there is some knowledge about the
evolutionary development of brain functions, including laterality. Last, the existence of laterality
in nonhuman primates argues against the philosophical perspective that humans are unique and
in some manner significantly different and better than other primates.
2


What is Manual Laterality?
It is necessary to use some term to indicate the use of one hand rather than another
when engaging in a task. When observing humans, this term is generally called handedness.
However, increasing knowledge about the variability of such behavior has led to a plethora of
definitions of handedness and the use of alternative terms. For example, Ward et al. (1993:45)
used the terms hand preference and hand performance.
Hand preference measures reflect relative incidence of use. Hand performance
measures are typically efficiency measures that make possible comparison of the
manner of performance and/or outcome of use of the left or right hand. (Ward et. al.
1993:45).
This means that hand preference refers to the quantity of reaches made with a particular hand in
a particular task, whereas hand performance refers to the ability of a particular hand to
successfully complete a given task. Hence, picking up food from the ground would likely be an
hand preference task, while successfully manipulating an object to obtain food would be a
performance task (one could, of course, with repeated trials, do a preference analysis on the
latter task as well as a performance analysis).
Harris and Carlsen (1993) defined hand preference in a similar way as Ward while
adding the requirement that such preference be present across tasks to qualify as handedness.
By handedness, we ordinarily mean that the hands are asymmetric in use and
function so as to reliably favor one hand or the other across a range of skillful
acts, [and] by [hand preference]... we mean only that an individual consistently
uses one hand rather than the other for a given task (Harris and Carlsen 1993:285).
3


Preilowski (1993:127) used different terms to describe the same phenomena as Ward:
Qualitative handedness [is] defined as a difference between right and left hand in
quality and speed of performance; it was previously called performance
handedness....Quantitative handedness [is the] difference in the frequency of
using right and left hand; it was called preference handedness before, since it was
determined in situations in which the subject could choose to use one or the other
hand.
Using these three researchers definitions it is possible to conclude that there are at least
three different ways in which manual laterality can be measured. A researcher can look for hand
preference while an animal is engaged in a single activity by counting the number of times that
animal uses one or the other hand; this would be called preference handedness, quantitative
handedness, or hand preference. The speed or success rate of performing a particular activity
can be compared between the two hands; this is performance handedness or qualitative
handedness. The frequency with which one hand is used preferentially over a number of tasks
or activities is called simply handedness.
To help fill out the available literature on primate hand preference this paper reports the
hand preferences found among a feral troop of Japanese macaques located in the United States.
Monkeys were observed eating grains they picked up from the ground (Figure 1.1). This type
of activity conforms with the definition ofhand preference as used by Harris and Carlsen
(1993), with data gathered via focal animal observations (Altman 1974) of an individual
performing the same task repeatedly.


Figure 1.1 Japanese macaques eating grain.
5


CHAPTER 2
BACKGROUND TO THE STUDY
Traditionally, handedness has been viewed as a uniquely human characteristic
(MacNeilage, 1993). Early primate studies indicated only weak lateral tendencies and those
were only observed at the level of the individual, rather than at the population level. In those
few studies which did reveal manual preferences, the prevailing assumption was that this was an
artifact of some other part of the study (conditioning training etc.). In 1987 MacNeilage,
Studdert-Kennedy, and Lindblom published a meta-analysis of primate laterality studies, finding
that primates do indeed express hand preference and further, that the lack of consensus in the
literature was likely a result of poor, inconsistent, or incorrect methodology. The results of this
meta-analysis revealed some lateral hand bias across species and tasks. This conclusion brought
about a flurry of renewed interest in the subject of primate manual laterality.
It has been widely presumed that the predominance of right-handed people was a result
of some unique human cognitive function. Laterality has commonly been considered a species-
specific trait associated with language and/or tool-making and -use, two other behavioral traits
assumed to be unique to our species. The most common notion is that handedness first
evolved with hominid tool construction and use, and that language then either evolved directly,
6


via sign language (Hewes, 1973), or indirectly, via spoken language. (MacNeilage, 1993:326).
Additionally, the strong role of language in the conveyance of culture (including tool-use and
tool-making) and its known association with lateralized brain function suggested a late
evolutionary development of manual laterality.
The implications of nonhuman asymmetries for human behavior are profound because
they suggest that the presently accepted conclusion that hominid-specific lateralized
brain specializations are keys to our uniqueness is wrong, and therefore needs to be
replaced. The problem is most serious for handedness, which has hitherto been one of
the main cornerstones of arguments for human uniqueness. (MacNeilage, 1993:319-
320)
Although the particulars of MacNeilages argument have been the subject of much debate,
continuing research is forcing theorists to abandon the notion that manual laterality is unique to
humans. It is clear that individual nonhuman primates often exhibit lateral behaviors, including
hand-use asymmetry, and that the mechanisms producing behavioral asymmetry may have deep
evolutionary origins.
Nonprimate Laterality
Indeed, manual asymmetry and lateralized behavior are present not only in nonhuman
primates, but in many nonprimate species as well (reviewed by Bradshaw and Rogers, 1993).
Paw preference has been observed among rats {Rains ratus) and mice {Mus sp.) both at the
individual level and at the population level for particular tasks. There is evidence for lateralized
behavior in laboratory rats in tasks such as leading limb in rotation or locomotion (Glick 1985).
Domestic cats show paw preference on an individual level (Tan and Kutlu, 1991) as do
domestic dogs (Tan, 1987). Sugar gliders {Petaurus breviceps), koalas (Smith 1979), and


possums (Trichosurus vulpecula, Megjrian et al., 1977) also exhibit strong individual
lateralization without significant population asymmetry (which was found in only one study for
each of the last three species noted). Thus, though data are rather limited for nonprimate
mammals other than rats and mice, available data indicate at least individual asymmetries. This
is clearly an area in which more studies need to be undertaken.
Lateral limb preferences have also been observed in birds. Rogers (1986) reviewed
lateralized behavior in a variety of avian species (parrots, chickens, and cockatoos). Such
lateralization ranged from footedness (only in species which use their feet during feeding) to
lateralized behaviors associated with ocular processing. Such findings indicate that conditioning,
fetal development, and hormone production may all contribute to lateralized behaviors displayed
by chicks or adult birds. Are we then to assume that lateralized limb use evolved in mammals
(including primates and humans) independently from its evolution in birds? Although there
could be convergence for this type of behavior it seems more parsimonious to assume that
laterality of function was present in the common ancestors of both birds and mammals.
In fact, when the data for fish, reptiles, and amphibians are reviewed, it becomes
obvious that these creatures also possess lateralization of behavior and, in some cases, limb use.
For example, toads (Bufo bufo, B. maritms, B. viridis) show front limb preference at the
population level (Bisazza et al., 1996). Chameleons (Anolis carolinesis, A. sagrei) show
lateralization of aggressive behavior (Deckel, 1996). Fish show lateralized escape (Jenynsia
Iineala, Bisazza et al., 1997, Girardinusfalcatus, Cantalupo et al ), rotational (Oreochromys
mossambicus), and detour behavior (Gambusia holbrooki, Bisazza & Vallortigalla, 1996). The
only conclusion that can be drawn from laterality studies over such a wide range of species, is
that laterality is plesiomorphic for fish, amphibians, reptiles and birds, and mammals. Thus, it
8


seems reasonable to expect that humans and other primates would exhibit lateralization of the
brain with accompanying specialized behaviors.
Primate Laterality
Postural and manual asymmetries among primates are almost certainly due in part to the
evolution of the hand and a grasping type of locomotion and feeding activity. Like binocular
vision, the flexible grasping five digit hand is an ancestral plesiomorphy for primates. This type
of hand is extremely useful for arboreal locomotion as well as for effective foraging in an
arboreal substrate. The earliest primates were vertical dingers and leapers with visiospatiomotor
spedalizations for unimanual predation (Fleagle, 1988). As MacNeilage et al. pointed out, this
would initiate an entirely new feeding arrangement for primates: Although having a heritage of
about half a billion years of bilaterally symmetrical midline predation involving the mouth, they
switched to the hand as the organ of predation... (1993:329). In this situation the stronger limb
might be used first for postural support while the other hand would be used for activities
requiring more predse motor control (hunting, for instance), causing a physiological asymmetry
of function to arise. This manual spedalization would then constitute a plesiomorphy for the
primate order.
Numerous studies have been conducted to investigate the possibility that laterality is
indeed a primitive character for primates. Prosimians have been the subjects of a variety of
studies which have shown hand preference (see Ward et al., 1993 for a review). For example,
among ring-tailed lemurs (Lemur catta), Masataka (1989) found that 20 out of 22 had a strong
left hand bias and Milliken et al. (1989) found that left hand preferences were retained across
9


tasks. Six species of lemur (L. catta, L. coromtus, L. macaco, L. mongoz, L. ntbriventer, and
five subspecies of L. fulvus) were surveyed for hand use by Ward et al. (1990); this sample of
194 subjects showed a left hand bias. In 1984, Sanford found that among 25 lesser bushbabies
{Galago senegalensis) there was little laterality when animals were in a quadrupedal stance, but
when tested bipedally they tended to have a left hand bias. More recently, Mason et al. (1995)
found a tendency to lateralized feeding among sifakas (Propilhecus verreauxi coquereli). All of
these researchers have shown that prosimians do show laterality on the individual level and that
they may have a left hand bias at the population level across all prosimian species.
Functional laterality has also been found in New World monkeys. Matoba et al. (1991)
looked at the relationship between hand preference and matriline among common marmosets
(Callithrixjacchus). They found a consistent correlation between mothers hand preference and
that of her infant in 23 family groups (they found no such correlation between fathers and
infants). In 1990 Fragaszy observed capuchins (Cebus apella) and found that they exhibited a
left hand preference during simple visually guided reaching tasks and a right hand preference
when engaged in nonvisual or novel tasks. Capuchin monkeys have also been studied
extensively by Westergaard et al. (1996,1993) who have demonstrated that capuchins show
lateral preferences in tool use and manufacture with the right hand being preferred for
demanding tasks. King and Laudau (1993) observed squirrel monkeys {Scdmiri sciureus) and
found increased preference, either left or right, with demanding tasks and little preference with
simple reaching. In goldfish catching-a demanding, highly visual, posturally unstable, and
ballistically performed (that is, the trajectory of the reach was not modified after initiation) task in
which the monkeys used three limbs to balance on the edge of a tank and one hand to attempt to
catch the goldfishproduced a strong left hand preference, whereas pronounced right hand
preferences were found with vertical clinging tasks. Thus, among New World monkeys there
appears to be lateralization of hand preference on the individual level, and in some species'tasks
10


at the population level, with the left or right preference appearing as highly task-specific in some
cases.
Old World monkeys also express asymmetrical laterality. In 1987 Fagot and Vauclair
studied a troop of baboons (,Papio papio) and observed that, while individuals strongly preferred
one hand over another, there was no population bias toward either hand. In another study
conducted in 1988 they found that baboons exhibited a left hand preference in tasks which were
intensively visuospatial. Fragaszy and Adams-Curtis (1993) observed crab-eating macaques
{Macaca facicularis), and found no significant hand bias across tasks or by sex or age of
animals. In another study Fagot (1991), observed that rhesus macaques exhibited a left hand
preference while hanging or sitting, but exhibited no preference while standing bipedally.
According to Fagot, ...the requirement to use one hand to carry the monkeys weight or
maintain balance does not appear to predict the degree of hand bias. (p. 266). Forrester and
Quiatt (1994) observed that rhesus macaques (Macaca mulatto) lifting the lids of feeder bins
and removing food showed a preference for reaching with the left and lifting lids with the right.
Similarly, non-lifting macaques in this study showed an equal frequency of either left or right
hand use when a lid-lifting companion held the lid up. Studies of Old World monkeys seem to
indicate a strong tendency for the individual to be handed, but so & data suggests no population
level asymmetries.
Manual laterality in apes varies widely across species. For example, a right hand
preference was found in adult female gibbons (Hylobates lar), adult males showed little
lateralized manual preference when reaching for food, and neither showed any asymmetry for
leading limb during brachiation (Stafford et al., 1990). Orangutans (Pongopongo\ who have
been little studied as of this writing, have not been observed to demonstrate manual laterality
(Olson et al., 1990). Out of 47 captive lowland gorillas {Gorillagorilla beringei), 72%
11


exhibited a strong right hand preference across a range of activities (Shafer, 1988), whereas
Byrne (1991) saw no evidence of laterality among wild mountain gorillas (Gorilla gorilla
gorilla) when engaged in natural behaviors. While chimpanzees (Pan troglodytes) show a
preference for one side or the other, there has been no observed consistency as to which side
they prefer (Boesch, 1991, and see Marchant and McGrew, 1991, for a review), although it
appears that infants have a slight right hand bias when observed for hand to mouth, one hand
grasping the other hand, defensive grasp, and first step (Bard et al., 1990). Bonobos (Pan
paniscus) showed no lateralization across a wide range of behaviors and showed only a slight
preference for right leading limb in quadrupedal locomotion (Hopkins and De Waal, 1995). So
far the ape literature is rather contradictory, with gorillas having shown the highest degree of
laterality in captivity and with all field studies showing mixed results that tend toward laterality at
the individual level rather than at the population level.
The majority of human handedness studies have shown an adult population right hand
bias estimated to range from 85 to 92 percent (Annett, 1985; Bryden, 1982; but see McGrew
and Marchant, 1994). Harris and Carlson (1993) made the observation that simple visually
guided reaching assessments are the most common measures of handedness used with human
infants and with nonhuman primates. In an effort to help balance the literature they set about
testing adult humans using simple visually guided reaching for a variety of objects placed at
various orientations to the body. When an object was placed at the mid-line of the subjects
body the dominant hand was used from 68 to 85 percent of the time. When an object was
placed on the dominant side there was a 90 percent use of the dominant hand, versus 60 to 75
percent dominant hand us when the object was placed on the nondominant side. Distance of the
object from the subject had no effect and the size of the object only affected hand use if the
object was large. Lateralization was slightly stronger for women. The measures used in this
study are comparable to those used most commonly to assess manual preference in nonhuman
12


primates. That is, the individuals were engaged in a simple reach wherein an object was
simply picked up and released; this bears more resemblance to many nonhuman primate studies
which focus on simple reaching for food objects (the main difference being the mouth as the
terminal receptacle among the majority of primate studies). Unlike earlier estimates, this study
showed the adult human population to be less handed than previous estimates. It is significant
that dissimilar methodologies may have contributed to the difference observed between humans
and nonhuman primates.
McGrew and Marchant (1994) found a wide range of variation in human handedness
estimates published in a number of studies (p. 179). Interestingly, they found that estimates of
handedness varied from less than 1% left handed (Katanga, Zaire) to more than 22% left handed
(Kwakiutl, British Columbia, Canada). This is in contrast to the common belief that 10% of
humans are left handed. In fact, in their study in 1995 of videotapes of individuals in three
traditional societies, humans were ambilateral in non-tool-using activities with only tool use and
tool use with a precision grip gaining significant laterality (reviewed in McGrew and Marchant,
1996:270). This evidence is not unlike the hand preference evidence for some nonhuman
primates such as Japanese macaques (Itakura 1992), baboons (Fagot and Vauclair 1987), and
capuchins (Westergaard 1993,1996), suggesting that the perceived difference in hand
preference between humans and nonhuman primates may indeed be methodological.
A review of the literature across primate species leads to the conclusion that hand
preference is an expected part of primate behavior. To quote MacNeilage, there are enough
instances of lateralized behavior in nonhuman primates at the population level to demand the
conclusion that this phenomenon exists, although there will, no doubt, continue to be tenacious
resistance to this conclusion (1993:319). I would also propose that lateralization at the
individual level may be as important as lateralization at the population level. The feet that
13


animals are lateralized one way for some tasks and a different way for other tasks, is in and of
itself interesting and may provide clues about cerebral lateral function.
This study measures hand preference among monkeys by counting reaches made during
feeding. The data are then used to analyze the pattern of hand preference among the
Arashiyama West troop so that it may be compared with other research done on manual
laterality in Japanese macaques as well as in other primate species. I have not attempted to
identify which hand is being used across a range of tasks, but rather, have looked for frequency
of same hand use in one task. According to Harris and Carlsen, in their discussion of visually
guided reaching tasks: insofar as human adults show hand preference on this task consistent
with their known handedness, it suggests that the task, at least in principle, would be appropriate
as a test of handedness in other primates (1993:301). Thus a simple reaching task has been
used to detect hand preference among several categories of Japanese macaque.
Japanese Macaque Studies
The data for individual species vary enough between those species that it is necessary to
compare the findings of this study most closely with the studies done on Japanese macaques in
the past. Research on hand preference in Japanese macaques (Macacafiscata) has been
pursued in Japan with provisioned animals. Studies have used three provisioned groups:
Takasakiyama (Itani, 1957; Itani et al., 1963), Koshima (Tokuda, 1967; Kawai, 1969;
Watanabe et al., 1993), and Katsuyama (Takeda, 1994). Three captive studies have also been
conducted: one of a group known as Arashiyama-R (Kubota, 1990), one of two animals at the
14


Primate Research Institute in Kyoto (Itakura, 1992), and one of nine monkeys housed at the
Zoological Garden, Berlin (Harigel, 1994). To better interpret this research, I will summarize
the data from all of these studies.
Two studies were conducted using the Takasakiyama troop as the sample population.
In 1957 Itani submitted the first report on hand preference among Japanese macaques in which
he assessed lateral bias for picking up wheat grains (Itani, 1957, dted in Kubota 1990; I have
used Kubotas summary because the original text is in Japanese). Itani observed 81 adult
animals and found that there were significantly more monkeys with a left hand preference than
there were monkeys with a right hand preference (30 left, 16 right; p<0.05). In 1963 Itani
conducted another study in which peanuts were thrown to monkeys, and after the peanut hit the
ground the hand used to pick up the peanut was recorded. Monkeys were classified into four
age groups and though there was no indication of a population level asymmetry, monkeys did
show an increased tendency to use the left hand in the older age categories. Both of these
studies have been criticized for failing to explain by what method hand preference was
determined (MacNeilage, 1987; Kubota, 1990).
The Koshima troop has been used in three different studies to date. In the first,
monkeys were thrown sweet potatoes and the hand(s) used to catch them were recorded.
Initially, monkeys caught potatoes with both hands, but later tended to use only one hand. Nine
monkeys caught the potato with either both hands or the left hand, 11 caught the potato with
both or either hand, and four used both or the right hand to catch (Kawai, 1967). Tokuda also
did research on this troop in which peanuts were thrown to individuals and the hand used to
pick up the peanut was recorded (following Itanis research). Each animal had 10-20 peanuts
for which hand preference was recorded. Hand preference was determined by having 8 of 10
reaches with the same hand. If a monkey failed to show a strong preference within the first 10
15


throws, an additional 10 throws were administered to see if the animal would exhibit a
preference. The total number of monkeys observed was 41, with 17 preferring the left, 8
preferring the right and 16 showing no preference. In 1993 the Koshima monkeys were the
subjects of a hand preference study conducted by Watanabe et al. In this study the researchers
focused on hand preference in 1) picking up wheat, 2) washing wheat, and 3) washing potatoes:
...our data suggest that feral monkeys display a general left hand preference in picking up wheat
grains, washing wheat grains, and washing sweet potatoes (Watanabe et al., 1993:191).
Unlike Itani 1963 this study did not find any preference bias that correlated with the age of the
subject.
A third provisioned group, Katsuyama, was observed by Takeda in 1994. In this study
the researcher observed social grooming behavior among members of this free-ranging troop.
Takeda noted which hand was used for picking during grooming and found that there were no
significant asymmetries for the population. The sex of the monkey showed no correlation with
hand preference. Takeda did observe a slight tendency for older animals to use the left hand, but
this finding was not statistically significant. Further, there appeared to be no correlation between
a mother monkeys hand preference and that of her offspring. Individual animals did show
preference, thus confirming the presence of laterality on an individual level. Overall, this study
would suggest that either monkeys at this location do not display significant population-level
manual laterality, or that grooming may not be an activity useful for measuring laterality.
In 1990 Kubota conducted a hand preference study using the group of monkeys called
the Arashiyama-R troop. These monkeys are housed in an outdoor enclosure in a large social
group. For this study 45 monkeys were observed and the sample was broken down by both sex
and age. Monkeys were shown to have more preference for either one hand or the other
(versus lack of preference) in older classes. While this study confirmed an increase in hand
16


preference with age, it failed to show that preference to be to the left. The only sex related
finding suggested than among young females there was a tendency for no preference while
among older females some preference was more common (Kubota 1990).
In a series of controlled laboratory experiments, Itakura (1992) looked for hand
preference in two captive bom adult male monkeys. The two subjects were given several tasks
which included simple reaching and simple reaching using a mirror for guidance (the piece of
fruit could only be seen in a mirror). In these two tasks both of the monkeys used their left
hands more than 95% of the time. Three further tasks were also presented in which the monkey
had to locate a piece of fruit using a mirror for guidance while reaching around a large barrier.
This meant that the monkeys could not see either the fruit or their hand directly, but were
required to use the mirror to obtain the reward. In contrast to the first two tasks, these three
tasks resulted in 88-99% of the reaches being performed with the right hand. While there were
only 2 subjects involved in this study, the dramatic change between preference for the first two
tasks and the latter three suggests that the complexity of the task may determine the amount of
observed asymmetry. Unlike studies on feral animals, these two monkeys showed a very
consistent hand preference on the first two tasks, whereas feral monkeys have seldom been
observed to demonstrate such consistency during simple reaching. The small number of
subjects does not warrant assuming a population-level asymmetry, but it suggests that such an
asymmetry may exist.
Harigel (1994) observed a captive group of 14 juvenile Japanese macaques while
engaged in simple reaching for food. These animals did not show sex-related differences in
asymmetry. They may have some age-related asymmetry; one- and two-year-old animals
showed strong preferences in either one direction or the other, while three-year-old monkeys
displayed no hand preference. Harigel also found that lower-ranking animals were more likely to
17


have a strong preference for one hand or the other. Like the research by Itakura, this study has
few enough subjects that extrapolation of data to a population would be highly speculative at
best. However, this study does indicate that individual animals have hand preferences.
At the time of this writing there had been a total of nine studies which reported hand
preference among Japanese macaques. In a number of studies macaques were observed to have
a slight left over right hand preference (Itani 1957, Kawai 1967, Watanabe et al. 1993), though
in two studies this was only seen among older monkeys (Itani 1963, Takeda 1994). Even in
studies where there were more monkeys who preferred the left to the right hand, there was still a
nearly equal or greater number of animals who exhibited no preference (Kawai 1967, Kubota
1990), while Watanabe et al. (1993) found no correlation between hand preference and the age
of his subjects. The association between handedness and the sex of Japanese macaques has not
been extensively analyzed. There have been three studies that sought to correlate sex with hand
preference. Takeda (1994) found no hand preference differences between males and females,
Harigel (1994) found females had a slightly higher number of right-handers when compared to
males (not, however, enough to be statistically significant), and Kubota found a slight right hand
preference in adult female monkeys when compared to male monkeys. Finally, it is interesting
to note that Itakura (1992) found that two male macaques had a left hand preference during
visually guided reaching and a right hand preference when visual guidance could only be
accomplished by looking in a mirror. Taken together, these data suggest that among Japanese
macaques there may be a slight hand use preference to the left which may increase with the age
of the subjects, there may be a difference correlated with the sex of the subjects, and task
complexity may influence hand preference.
18


CHAPTER 3
METHODS
A field study of hand preference was
conducted during the months of February and
March of 1993 at the South Texas Primate
Observatory in Dilley, Texas. This facility
supports a troop of Japanese macaques (Figure
3.1) known as the Arashiyama West troop.
Data on hand preference were collected on 22
days during daily feedings between February 4th
and March 15th of 1993. Subjects were
categorized by age and sex. Monkeys were
observed while eating grain and the number of
times each hand was used for this task was
recorded.
igure 3.1 Adult male macaque at Arashiyama
test in Dilley Texas.
19


Locale and Subjects
In the late 1960s a troop of monkeys in Japan called the Arashiyama troop increased in
number and eventually split into two groups. The animals from one of the newly created troops
began to interfere with human settlements in the area. Rather than exterminate the animals,
efforts to find the troop a new home were pursued, and in 1972 its members were trapped and
transported to North America where they became known as the Arashiyama West troop
(Fedigan, 1991). Edward Dryden, Jr., an American rancher, arranged to take the troop and
maintain it for both commercial and scientific purposes on his south Texas ranch. About two
years after the troop arrived, Mr. Dryden died and his wife, Clementina, took over support of
the troop. She later transferred care and ownership to the Arashiyama West Institute, a group
of interested researchers who moved the troop in 1980 to the Dilley, Texas site. Since that time
an organization has been formed called the South Texas Primate Observatory. At the time of
this study, the monkeys were maintained at the Dilley location under the management of the
South Texas Primate Observatory
The Arashiyama West troop is the only troop to have been studied in Japan before
being trapped as an intact group and shipped and released in the United States. It has been
studied intensively since its arrival here in 1972. The number of animals originally shipped was
150. When the troop was relocated to Dilley, it had grown to about 300 animals, doubling the
initial population in eight years (Fedigan, 1991). Research on this troop is especially interesting
because it can be compared with the original main troop-known today, particularly in the
United States, as the Arashiyama East troopwhich was left intact and is still under observation
in Japan. Thus, the two groups can serve as genetically close comparison populations. In 1974,
the troop maintained a male-to-female ratio of 1:2. At that time about 3% of the population
20


was over 18 years of age. In 1989 The troop was estimated to have 470 animals with about
46% of those being under 4 years of age. There is no estimate of the number of animals over 18
years old available at the time of this writing (Fedigan, 1991:66).
At the time of this hand preference study the Arashiyama West troop lived in a free
ranging state about 12 miles from the town of Dilley, Texas. The site had at one time been an
electrified enclosure, but the fence had fallen into disrepair, leaving the monkeys free to roam.
The area where the monkeys were fed was cleared of vegetation to enable vehicle access. Near
the main feeding area were two ponds which had vegetation growing all around them and which
supplemented water tanks for drinking. The Arashiyama West troop was provisioned daily with
150 pounds of grain, either cracked com or milo, and with 50 pounds of monkey chow; once
per week, they were provisioned with a truckload of fruit (Figure 3.2). The animals were
always at this site during feeding times.
Figure 3.2 Monkeys following feeding truck
21


The population at the South Texas Primate Observatory consisted of three groups
totaling an estimated 500+ individuals. The bulk of the population, approximately 300-400
individuals, formed the main troop. The alpha male of the main troop when I arrived was
Fang (Figure 3.3), the beta was Rocky, and the third in command was Ran. These three
most central males were older, Japanese-born monkeys who had reasonably stable social
relationships. The alpha female of the dominant matriline was Lady Di. By the end of this
study the troop had undergone great social change, attributed to cougar predation. Both the
alpha and beta males were killed, leaving Ran as the leader. These circumstances seemed to
make the monkeys jumpy and hard to observe for extended periods; this reduced the number of
total reaches per monkey as well as the total number of bouts observed per day.
Figure 3.3 Alpha male Fang eating com.
A splinter troop known as the Pelka troop had split from the main troop in 1990. This
troop was usually separated from the main troop by at least 50 yards and had about 70
22


members. The Pelka troop did not suffer the same degree of loss as the main troop and was
somewhat more socially stable during the end portion of the research.
The third group of monkeys consisted mainly of peripheral males: adult and sub-adult
males who maintained a distance of at least 20 yards from the main and Pelka troops at most
times. Occasionally, a female would be observed with one or more members of this group of
males. For the most part, this subset of monkeys seemed to be a loosely organized coalition
which might be spread out over great distances. Monkeys migrated out of this group with
regularity (presumably intending to migrate to other troops as they would in their native
environment); these would be caught and kept in cages to prevent their trying to leave again,
since there are no other troops in Texas for these monkeys to migrate to.
One way in which this study differs from the majority of other laterality studies is that
the subjects are free ranging. The vast majority of laterality studies have been conducted with
captive animals. There are a variety of reasons for this, including the greater ease of creating
demanding taskswhich have been shown to bring out lateral biasin a captive environment.
Notably, however, there have been a number of previous laterality studies on free ranging
Japanese macaques. The Arashiyama West troop is free ranging, provisioned, and heretofore
unstudied for hand preference and is well suited to being used as a comparison group to the
aforementioned studies.
Sample
Observations were taken after the monkeys had been fed, generally mid- to late
morning. Feeding usually took several hours with monkeys dispersing in the late afternoon.
23


The area where the monkeys were fed was flat and dry with vegetation consisting mainly of
sagebrush and mesquite. Daytime temperatures remained within the 70s and 80s (Fahrenheit).
Access to the facility was poor during wet weather, so nearly all observation periods were
initiated when the weather was warm and dry.
For data collection and subsequent hand preference analysis, observed monkeys were
categorized by age and sex. Tattoo identifications (see Appendix A) of individuals were noted
whenever possible to afford checks for accuracy of age and sex categories. Young monkeys
were difficult to sex and occasionally sex could not be identified. Thus, three codes were used:
male, female, and unknown, the last for animals whose sot was not determined (infants and
some juveniles). Adult males and females were readily distinguished; fully adult males are
generally larger than females and had obvious genitalia and a full muscular shoulder girdle which
extends around the shoulder and neck area of the animal. Adult females were most easily
identified when they had infants or juvenile offspring or when there were obvious signs of estrus
or lactation. Sub-adult males and females were difficult to differentiate; these animals, typically
not mature in appearance, were not as strongly marked by the secondary sex characteristics
described above. Sub-adult males tended to associate in a peripheral same-sex group, which
helped in identifying sex, but the only conclusive diagnosis was provided by sighting genitalia or
tattoo identification. Infants and juveniles by and large were not tattooed so there was no
secondary method to check for correct sex identification. Very young animals, then, were not
distinguished by sex, only by age.
Monkeys were categorized as old, adult, sub-adult, juvenile, or infant. Old animals
were those monkeys which were bom before 1972 and had been brought over to the U S. from
Japan. Old females were generally very gray and decrepit-looking and past reproductive age
(though some would still exhibit signs of estrus). There were fewer old males than old females
24


and they tended to be fairly robust in appearance with a very pronounced shoulder girdle of
muscle.
Adult animals were those monkeys of reproductive age bom in Texas after 1972, but
before 1984. Adult females were detected by body size, appearance of nipples, signs of estrus,
having offspring, or by individual identification (Figure 3 .4). There were considerably fewer
adult males than adult females due to the high death rate among males in this age group. Adult
males were distinguished by a muscular shoulder girdle and by being generally larger than
females and subadults, but without the robustness of old males.
Figure 3.4 Lactating adult female macaque.
25


Sub-adult monkeys were generally pre-reproductive and lacked obvious secondary sex
characteristics. They were larger than juveniles and infants and had been bom between 1984
and 1988. Sub-adult females were recognized as having smaller than adult body size,
undeveloped nipples, and no signs of estrus, with confinmation when possible by identification of
the individual. Sub-adult females stayed close to females of their matriline and were not often
seen outside the troop. Sub-adult males tended to be smaller and had an overall lighter body
frame than fully adult males. They were usually found on the periphery of the main or Pelka
troops and roamed together in a troop consisting mainly of males of this age.
Infants and juveniles were
newborn to approximately five years of
age (Figure 3.5). Sex was coded as
unknown for animals in this age group.
Initially monkeys were placed in separate
categories if they were under one year in
age, one to two years, two to three years,
and four or five years. Later, these four
categories were combined in the single
category infant/juvenile for the purpose
of analysis. The reason for combining
these groups was twofold: first, when
broken into four groups, there were very
few bouts within some of these categories (for example, there were a total of only 12 bouts with
infants as focal animals), secondly, since all animals with unknown sex were within these
categories, they made a natural category which could be compared with the adult population of
both sexes.
Figure 3.5 Infant macaque, bom in 1992.
26


Monkeys at the Arashiyama West site are identified by fecial tattoos which were
developed from a coding system used in Japan for monkey identification. They also have a
number tattooed on the inside of the right thigh. Very few adult animals did not have tattoos;
however, a great number of infants and juveniles had not been so marked. Unfortunately tattoos
are often hard to read without disturbing the animal enough to end the observation session.
Visible tattoos were transcribed onto observation sheets and later decoded using the decoding
monkey face (see appendix A). Tattoo identifications showed a near perfect correlation with
sex and age assessments, leading to a high degree of confidence that assignments of sex and of
age were correct.
Data Collection
Monkeys were only selected for observation while sitting and eating grain. Grain was
poured out of the back of a truck along a dirt road that was approximately one mile long. Daily
observations usually began at the end of this feeding area, furthest from the grain storage area.
This furthest point generally attracted the largest number of monkeys, those more socially
dominant and able to compete in a more densely populated feeding area. Focal subjects were
selected on the basis of proximity while moving back toward the grain storage area. Each day
efforts were made to sample individuals from the largest number of age and sex categories
possible. Observations were conducted until the monkeys left the area, until observer fatigue set
in, or until the weather precluded further observations. As a result of how focal animals were
27


chosen, members of the main troop were more heavily sampled than those of the Pelka troop or
of the peripheral group.
Once a focal animal was selected for sampling, an observation sheet was started (Figure
3.6) and the animals sex, age, and tattoos were recorded. Monkeys were observed while
picking grains up and eating grains from the ground, the hand used by the monkey to pick up
grains during 10-110 sequential reaches was recorded. Additionally, information about the type
of grain being eaten and the position of the monkey throughout the bout were recorded (each
observation sheet equaled one bout). Each monkey was observed until one of two terminating
acts occurred: 1) the animal moved to a location that made continued observation impossible,
or 2) the end of the data recording sheet was reached. In a few cases, the 100 reach limit of the
observation sheet was extended by using a single square for two entries, but observation of an
individual was usually stopped after 100 entries to prevent any single monkey from contributing
a disproportionate fraction of the total data collected. When the observation sheet was
completed, another monkey was chosen and the process began again.
28


Age
Sex
#
Stress
Feed
Figure 3.6 Sample observation sheet used in the field for recording monkey
hand usage. The grid was used to record each instance of hand use as either R
or L; color codes (using a 4 color pen) were used to distinguish between sitting
and standing and between com and milo. The face was used to record
information about the monkeys facial tattoos, thigh tattoos were recorded if
readable.
Sampling Limitations
Due to limited observation time and resources, monkeys were not identified on an
individual basis (except to verify age and sex assessments made in the field). Every attempt was
made to sample as many individuals as possible. To accomplish this, no single individual was
29


ever observed twice in one day. Data were taken by moving from one section of the troop to
another in a methodical manner, observing monkeys who were ever more distant from the
starting point. Whenever there was some doubt as to whether the animal had already been
observed, no further sample was taken and that bout was not included in the analysis. An
observation period in which a monkey made less than 10 reaches or in which the age or sex
categorization was undetermined or in doubt was discarded from analysis.
30


CHAPTER 4
RESULTS
A total of20,283 reaches for grain by monkeys over 314 behavioral bouts recorded
during 22 days of observation were analyzed. The majority of animals observed were sub-
adults, adults, or old animals (72%) with about 28% of the bouts representing infant or juvenile
monkeys. About 54% of the observations were of females, about 37% were of males with the
remaining 9% being of unknown gender. The age and sex breakdown of the sample is shown in
table 4.1.
Infant Sex Female 0 Male 1 Unknown 11 Total 12 (.04)
Juvenile 24 32 17 73 (.23)
Age Sub-adult 47 55 0 102 (.32)
Adult 80 23 0 103 (33)
Old 19 5 0 24 (.08)
Total 170 (.54) 116(37) 28 (.09) 314 (1.00)
Table 4.1 Number of monkeys in each age^sex category (n=314).
31


Figure 4.1 describes the number of reaches made by monkeys per bout. There were no
bouts with less than 10 reaches, nor were there any bouts with more than 110 reaches. There
were more bouts within the 90-100 reaches per bout range than within any other range.
Figure 4.1 shows the number of reaches (N=20,283) within each of the 314 bouts.
Density plots have been used to describe the patterns of laterality present in the sample
population. The number across the horizontal axis shows the proportion of left to right handed
reaches, with 0 being all reaches made with the left hand and 1 being all reaches made with the
right hand. The vertical axis is a function of density within the population. It describes the
32


portion of the population at any given point which deviates from the expected density. 1.0 on
the vertical axis represents the expected value for the population. Each number vertically is the
number of monkeys with an observed degree of hand preference compared to or divided by the
expected number from pure chance. Each of the small circles lined above the horizontal axis
represents one bout in the described sample. The line above the circles describes the density of
bouts (circles) at any given point and how that density deviates from the expected value.
The density plot (Figure 4.2) shows the placement of each bout on the horizontal left to
right continuum. Notice that the distribution of the population is skewed toward the left,
indicating a tendency for left hand preference. There are notable spikes at both the left and right
side of the plot which indicate that some bouts were entirely left or right handed.
33


Population Density
1
1
1
1
J.
Degree of Lateral Preference
Figure 4.2 approximate density function for ratio of reaches in the entire sample
population, N=314 bouts. Across the horizontal axis 0 represents all reaches with the
left hand, 1 represents all reaches with the right hand. The vertical axis represents the
approximate density function for the population (average = 1).
Infant and juvenile monkeys have been split out from adults and combined into one
group in the density plot shown in figure 4.3. Combining these groups seemed appropriate
because a significant proportion of the bouts recorded for infants and juveniles were of monkeys
whose sex was unknown, and there were only 12 infant observations, none of which contained
more than 60 reaches. The monkeys in this group were spread out nearly evenly along the
34


Population Density
horizontal axis indicated a lack of strong preference for either hand for this group, although
clearly a few individuals were strongly biased to either the right or the left.
Degree of Lateral Preference
Figure 43 approximate density function for ratio of reaches in the infant/juvenile
population, N=85 bouts. Across the horizontal axis 0 represents all reaches with the
left hand, 1 represents all reaches with the right hand. The vertical axis represents the
approximate density function for the population (average = 1).
The next density plot (Figure 4.4) shows hand preference for the entire sample of adults
without regard to sex. This plot shows a substantial skew in the population toward the left. It is
especially noticeable how few of this sample prefer the right hand.
35


Degree of Lateral Preference
Figure 4.4 approximate density function for ratio of reaches in the adult population,
(both male and female) N=229 bouts. Across the horizontal axis 0 represents all
reaches with the left hand, 1 represents all reaches with the right hand. The vertical axis
represents the approximate density function for the population (average = 1).
Differences between the density plots of the young monkeys (infants and juveniles) and adult
monkeys (subadults, adults and old animals) are striking, showing a much greater trend toward
left hand use in the adult population. When compared using a t-test, a p value of .03333 was
found, indicating a statistically significant tendency toward left hand usage in the adult monkey
portion of the sample when compared to the young monkey portion of the sample.
Next, the adult population was broken down by sex of monkey. The adult female
density plot (Figure 4 5), shows a fairly even distribution of hand preference across this sub-
36


Population Density
population. Adult females were most often in the middle of the plot without substantial obvious
hand preference, although there were a few individual bouts which showed very strong
preference to either the left or the right.
Degree of Lateral Preference
Figure 4.5 approximate density function for ratio of reaches in the adult female
population, N=146 bouts. Across the horizontal axis 0 represents all reaches with the
left hand, 1 represents all reaches with the right hand. The vertical axis represents the
approximate density function for the population (average = 1).
37


When a density plot was run for adult males (Figure 4.6), they showed a very significant
skew to the left, with a majority of monkeys falling between the exclusively left side of the plot
and the center.
Degree of Lateral Preference
Figure 4.6 approximate density function for ratio of reaches in the adult male
population, N=83 bouts. Across the horizontal axis 0 represents all reaches with the
left hand, 1 represents all reaches with the right hand. The vertical axis represents the
approximate density function for the population (average = 1).
When compared to the adult female density plot the adult male density plot showed an
extremely obvious tendency to use the left hand, while females were distributed more evenly
between left and right hand preference. These two groups were analyzed using a t test which
38


yielded a p value of .0003. This test demonstrates that in this sample adult males have a
significant left hand preference when compared to adult females who showed no significant
hand bias.
Thus, the sample analyzed indicates that males are significantly more left handed than
females and that adults are generally more left handed than infants and juveniles.
39


CHAPTER 5
DISCUSSION AND CONCLUSION
Significant differences were found between the young monkeys and the adult monkeys
(of both sexes) when reaching for grain. This finding is consistent with other research on
Japanese macaques (Itani 1963, Takeda 1994). The finding that adult males in this troop are
significantly more lateralized to the left than are adult females is unexpected and suggests that
there may be a sexual component to the determination of hand preference among these
monkeys.
Kubota (1990) found that adults as a group tended to have stronger preferences than
younger monkeys. This is in agreement with Itani (1957), who noted a greater left hand bias in
the adult population of the monkeys at Takasakiyama, but is at odds with Watanabe (1993),
who found no correlation between age and manual laterality for the Koshima population but did
find a slight left hand bias at the population level. Hand preference in the Arashiyama West
troop was consistent with Itanis and Kubotas findings in that there was a greater tendency
toward manual lateralization in adult animals, along with a tendency toward left hand bias.
40


Unlike any of the previous studies with Japanese macaques, the Arashiyama West troop
showed that adult males as a group have a distinct preference for using the left hand for eating.
That sex differences in hand preference have not been correlated in the literature is in part due to
the infrequency of analysis based on sex differences (Kawai 1967, Tokuda 1969, Watanabe et
al. 1993). In the study by Takeda (1994) differences in sex were looked for, but not found.
Harigel (1994) found that males were likely to prefer either hand whereas females had a slight
majority of right-handers (though not enough more to be statistically significant). Kubota
(1990) found that male monkeys did not show any significant preference for either hand
whereas adult female monkeys had a greater frequency of left hand preference.
It is unclear why the adult males of the Arashiyama West troop would be significantly
different from the subjects studied in other research. It is certainly possible that it is the result of
a dramatically different environment and/or related to some physiological process (possibly
hormonal) or due to the small genetic pool from which this population is derived (150 animals,
some related). It is also possible that the observed bias is the result of some type of arousal
process. Future researchers might do well to investigate correlation of hand preference with
dominance and states of arousal or activity. These types of emotional environmental indicators
have been little studied, though Haringel (1994) has found preliminary evidence that such a
relationship may exist in a captive environment.
In the last decade researchers have begun to question earlier assumptions about hand
preference. Traditionally, hand preference in nonhuman primates has been assessed by
observing an individual eating. That is, the monkey picks up a food item and places it in its
mouth. The number of times a monkey uses one hand in preference to the other is tallied and
the monkey is assigned the label of either being ambidextrous or preferring either the right or left
41


hand. My analysis has avoided categorizing the animals themselves as either left, right or
ambidextrous, based upon a single bout (10-110 reaches), instead considering bouts of reaches
on a continuum. This technique follows McGrew and Marchant (1996) and allows detection of
variations which might not be apparent using a simple trichotomy.
Recently, McGrew and Marchant (1996) added a new dimension to the issue of
handedness, stating that there are five levels of laterality. While I think that the word levels in
this context is a misstatement since they seem to be describing patterns of behavior, their
framework is useful for the analysis of population level laterality. They state:
Level 1 is the simplest, in which virtually all members of a population show no hand
preferences, that is, when the norm for individuals is ambilaterality.... Level 2 is when a
significant proportion of individuals are significantly lateralized to either side, but overall
the distribution remains symmetrical. Level 3 is when a significant proportion of a
population show not only laterality, but exclusive use of one hand or the other while still
retaining symmetry. Through this level the overall distribution is still one of hand
preference, as there is no sign of skew to the left or right. Level 4 is when the
distribution of lateralized individual is asymmetrical; that is, there are significantly more
right- than left-preferent members of a population or vice-versa. Finally, Level 5 is
Level 4 carried a step further, in which the distribution of exclusive users is
asymmetrical, either biased to left or right. (McGrew and Marchant, 1996:266)
Although the use of the word level seems inappropriate, thinking of these as patterns is a useful
framework for looking at laterality in groups. Using this method of interpretation, the
Arashiyama West monkeys as a population showed only the first pattern of laterality for simple
reaching for grain. When adults are considered separately from young monkeys, the older
monkeys approached the second pattern of hand preference. When adults are further
subdivided by sex the male sub-population reached the second pattern of laterality while the
females, although somewhat skewed towards the second pattern, remained most closely
described by the first pattern. Thus, the Arashiyama West monkey troop does not reach a
42


population pattern of manual laterality that is significant when using this method of
interpretation.
The literature would lead one to expect mild left hand bias in at least some segments of
the target population, and this study fulfills that expectation. Most literature on old world
monkeys shows that monkeys have varying degrees of handedness at the individual level. We
believe that most monkeys have some general tendency to use either the left or right hand which
may become more apparent according to the situation and/or just by chance in continued
examinations. However, these preferences are reflected as a matter of degree rather than
exclusive right- or left-handedness (Watanabe, 1993:190). The monkeys at the Arashiyama
West do show significant but nonexclusive hand biases at the individual level, further supporting
the conclusions of Watanabe and others.
This study highlights potentially fruitful directions for further research. It would be
interesting to design tests that could be used to detect hand preference in the wild; naturalistic
experimentation is entirely missing in field studies of laterality and could provide information
about whether feral monkeys will display the same degree of laterality recorded among captive
primates. Further, gathering data which would correlate hand preference with dominance and
arousal state may also prove illuminating. Finally, Rawlins (1989) and McGrew and Marchant
(1992) conducted studies in which data on spontaneous hand use in free ranging primates
(rhesus macaques and chimpanzees respectively) were collected and analyzed. This type of
study would be especially interesting with Japanese macaques, since they show a fairly
consistent level of hand preference across studies which measure simple reaching.
43


Appendix A
The original Japanese
system of numbering used a
fecial dot system and an inner
thigh tattoo. The animals
number is written out on the
inner tight thigh and then
repeated in code on the
animals face. The location of
the dot indicates a numerical
value. The dots are then
summed to find the tattoo
number. Thus, an animal with
a dot over each eye and under
the left eye would be number
118.
Numbers greater than
200 are indicated by placing
two dots on the sites
indicated. An animal with dot
under his nose and two
dots under the right eye
would be 210.
Each troop member has a unique name which consists of its mothers family name, the
birth years of its matriline and the last two digits of its birth year. Thus Matsu 586374 is of the
family Matsu, her grandmother was bom in 1958, her mother was bom in 1963, and she was
bom in 1974. Many animals also receive a nickname such as Rocky D, Fatsu Matsu, or
Kleenex.
44


Appendix A (continued)
This is a sample matriline chart from the Matsu matriline.
Ma6069F #46 Maudie Mae Ma606978F #283 Cataract Ma60697883F
Ma606986F No tattoo #634 Magrite Ma60697885M #542 Ma6069788389M
Ma606987F No tattoo Ma6069788390M
No tattoo Ma60697887F #835
Ma606990M No tattoo Ma6069788391F
No tattoo Ma60697889M #583 Ma60697891F #No tattoo No tattoo
If monkey number 283 was observed in the field, this chart could be used to learn that that
monkey is named Cataract, that she is an adult female of the Matsu lineage who was bom in
1978.
This information in this appendix was taken from a worksheet given to me while conducting
research.
45


BIBLIOGRAPHY
Altman, J. (1974). Observational study of behavior: Sampling methods. Behavior
49, 227-267.
Anderson, J.R., Degiorgio, C., Lamarque, C., and Fagot, J. (1996). A Multi-task
assessment of hand lateralization in capuchin monkeys (Cebus apella). Primates
37(1), 97-103.
Annett, M. (1985). Left, Right, Hand, and Brain: The right shift theory. Erlbalm,
Hillsdale, N.J.
Annett, M., and Annett, J. (1991). Handedness of eating in gorillas. Cortex 27, 269-
275.
Bard, K.A., Hopkins, W.D., and Fort, C.L. (1990). Lateral bias in infant chimpanzees
(Pan troglodytes). J. Comp. Psychol. 104, 309-321.
Bernstein, I. S (1991). An empirical comparison of focal and ad libitum scoring with
commentary on instantaneous scans, all occurrence and one-zero techniques. Anim.
Behav. 42, 721-728.
Bisazza, A., Cantalupo, C., Robins, A., Rogers, L.J., and Vallortigara, G. (1996).
Right-pawedness in toads. Nature 379(65641), 408.
Bisazza, A., Pignatti, R, and Vallortigara, G. (1997). Detour tests reveal task and
stimulus specific neural lateraliztion in mosquito fish (Gambusia holbrooki). Behav.
Brain Res (in press).
Bisazza, A., Rogers, L.J., and Vallortigara, G. (in review). The origins of cerebral
asymmetry: A review of evidence of behavioural and brain lateralization in fishes,
reptiles, and amphibians. Neurosci. Biobehav. Rev.
46


Bisazza, A., Cantalupo, C., Rogers, L.J., and Vallortigara, G. (in press). Lateral
asymmetries during escape behaviour in a species of teleost fish (Jenynsia lineata).
Physiol. Behav.
Boesch, C. (1991). Handedness in wild chimpanzees, bit. J. Primatol. 12, 541-558.
Bradshaw, J., and Rogers, L. (1993). The evolution of lateral asymmetries, language,
tool use, and intellect. Academic Press, San Diego.
Bresard, B., and Bresson, F. (1987). Reaching or manipulation: Left or right?
Behavioral Brain Sci. 10, 265-266.
Bryden, M. (1982). Laterality: Functional asymmetry in the intact brain. Academic
Press, New York.
Byrne, R.W., and Byrne, J.M. (1991). Hand preferences in the skilled gathering tasks
of mountain gorillas. Cortex 27, 521-546.
Cantalupo, C., Bisazza, A., and Vallortigara, G. (1995). Lateralization of predator-
evasion response in teleost fish (Girardinusfalcatus). Neuropsychologia 33(12),
1637-1646.
Chow, S.L. (1987). Meta-analysis of pragmatic and theoretical research: A critique.
J. Psychol. 121, 259-271.
Cole, J. (1957). Laterality in the use of the hand, foot, and eye in monkeys. J. Comp.
Physiol. Psychol. 50, 296-299.
Corballis, M.C. (1989). Laterality and human evolution. Psychol. Rev. 96, 492-505.
Corballis, M.C. (1991). The lopsided ape: Evolution of the generative mind.
University Press, Oxford.
Dimond, S., and Harris, R. (1984). Face touching in monkeys, apes, and man:
Evolutionary origins and cerebral asymmetry. Neuropsychologia 22, 227-233.
Dodson, D.L., Stafford, D., Forsythe, C., Seltzer, C.P., and Ward, J.P. (1992).
Laterality in quadrupedal and bipedal prosimians: Reach and whole-body turn in the
mouse lemur (Microcebus murinus) and the Galago (Galago moholi). Amer. J.
Primat. 26, 191-202.
47


Dreckel, A.W. (1995). Laterality of aggressive responses in Anolis. J. Exp. Zool. 272,
194-200.
Durden-Smith, J., and Desimone, D. (1983). Sex and the Brain. Arbor House, New
York.
Ettlinger, G. (1988). Hand preference, ability, and hemispheric specialization: In how
far are these factors related in the monkey? Cortex 24, 389-398.
Fedigan, L.M. (1991). History of the Arashiyama West Japanese macaques in Texas.
In The Monkeys of Arashiyama: Thirty-five Years of Research in Japan and the West
(pp. 54-73), Fedigan, L.M., and Asquith, P.J. (eds). State University of New York
Press, New York.
Fagot, J., and Vauclair, J. (1987). Spontaneous hand usage and handedness in a troop
of baboons. Cortex 23,265-274.
Fagot, J., and Vauclair, J. (1988). Handedness and manual specialization in the
baboon. Neuropsychologia 26, 795-804.
Fagot, J,. and Vauclair, J. (1991). Manual laterality in nonhuman primates: A
distinction between handedness and manual specialization. Psychological Bulletin
109, 76-89.
Falk, D. (1987). Brain lateralization in primates and its evolution in hominids.
Yearbook Phys. Anthrop. 30, 107-125.
Fleagle, J.G. (1988). Primate adaptation and evolution. Academic Press, New York
Forrester, A., and Quiatt, D. (1994). Rhesus monkey hand preferences in lifting lids
and reaching for food. In Current Primalology Vol. Ill: Behavioural Neuroscience,
Physiology, and Reproduction (pp. 17-21). Anderson, J.R., Roeder, J.J., Thierry, B.,
and Herrenschmidt, N. (eds.). University Louis Pasteur, Strasbourg.
Forsythe, C., and Ward, J.P. (1988). Black lemur (Lemur macaco) hand preference in
food reaching. Primates 29 (3), 369-374.
48


Forsythe, C., Milliken, G.W., and Ward, J.P. (1988). Posturally related variations in
the hand preferences of the ruffed lemur (Varencia variegata varigata). J. Comp.
Psychol. 102, 248-250.
Fragaszy, D M., and Mitchell, S.R. (1990). Hand preference and performance on
unimanual and bimanual tasks in capuchin monkeys (Cehus apella). J. Comp.
Psychol. 104, 275-282,
Galaburda, A M., Lemay, M., Kemper, T.L., and Geschwind, N. (1978). Right-left
asymmetries in the brain. Science 199, 852-856.
Geschwind, N., and Behan, P. (1982). Left-handedness: association with immune
disease, migraine, and developmental learning disorder. Proceedings of the National
Academy of Sciences, USA 79, 5097-5100.
Glick, S.D., and Shapiro, R.M. (1985). Functional and neurochemical mechanisms of
cerebral lateralization in rats. In Cerebral Lateralization in Nonhuman Species (pp.
158-184), Glick, S.D. (ed ). Academic press, New York.
Glick, S.D. (1993). Rotational behavior in children and adults. In Primate Laterality:
Current Behavioral Evidence of Primate Asymmetries (pp. 307-317), Ward, J.P., and
Hopkins, W.D. (eds). Springer-Verlag, New York.
Harigel, E.R. (1994). Hand preference in juvenile Japanese macaques (Macaca
fuscata) as a function of sex, age, and rank. In Current Primatology Vol. Ill:
Behavioural Neuroscience, Physiology, and Reproduction (pp. 23-30). Anderson,
J.R., Roeder, J.J., Thierry, B., and Herrenschmidt, N. (eds ). University Louis
Pasteur, Strasbourg.
Harris, L.J., and Carlson D.F. (1993). Hand preference for visually guided reaching in
human infants and adults. In Primate Laterality: Current Behavioral Evidence of
Primate Asymmetries (pp. 285-305), Ward, J.P., and Hopkins, W.D. (eds ). Springer-
Verlag, New York.
Hatta, T., and Koikke, M., (1991). Left-hand preference in frightened mother
monkeys in taking up their babies. Neuropsychologia 29, 207-209.
Hewes, G.W. (1973). Primate communication and the gestural origin of language.
Curr. Anthrop. 14, 5-29.
49


Holloway, R.L., and de la Coste-Lareymondie, M.C. (1982). Brain endocast
asymmetry in pongids and hominids: Some preliminary findings on the paleontology
of cerebral dominance. Am. J. Phys. Anthrop. 58, 101-110.
Hopkins, W.D. (1991). Handedness and laterality in apes and monkeys. Primatology
Today 271-274
Hopkins, W.D., and Morris, R. (1989). Laterality for visual-spatial processing in two
language trained chimpanzees (Pan troglodytes). Behav. Neurosci. 103, 227-239.
Hopkins, W.D., Washburn, D.A., and Rumbaugh, D.M. (1989). Note on hand use in
the manipulation of joysticks by rhesus monkeys (Macaca mulatto) and chimpanzees
(Pan troglodytes). J. Comp. Psychol. 103, 91-94.
Hopkins, W.D., Washburn, D.A., and Rumbaugh, D.M. (1990). Processing of form
stimuli presented unilaterally in humans, chimpanzees (Pan troglodytes), and monkeys
{Macaca mulatto). Behav. Neurosci. 104,577-582
Hopkins, W.D., and de Waal, F.B. (1995). Behavioral laterality in captive bonobos
(Pan paniscus): Replication and extension. International Journal of Primatology
16(2), 261-276.
Ihobe, H. (1989). How social relationships influence a monkey's choice of feeding
sites in the troop of Japanese macaques (Macaca fuscata) in Koshima Islet. Primates
30(1), 17-25.
Itakura, S. (1992). Task-specific hand preferences of two Japanese macaques on
mirror-guided reaching. The Psychological Record 42, 173-178.
Itani, J. (1957). Personality of Japanese monkeys. Primates 11, 29-33 (in Japanese,
summary in Kubota, 1990).
Itani, J., Tokuda, K., Furuya, Y., Kano, K., and Shin, Y. (1963). The social
construction of natural troops of Japanese monkeys in Takasakiyama. Primates 4, 2-
42.
Kawai, M. (1967). Catching behavior observed in the Koshima troop: A case of
newly acquired behavior. Primates 8, 181-186.
50


King, J.E., and Landau, V.I. (1993). Manual preference in varieties of reaching in
squirrel monkeys. In Primate Laterality: Current Behavioral Evidence of Primate
Asymmetries (pp. 107-124), Ward, J.P., and Hopkins, W.D. (eds). Springer-Verlag,
New York.
Kubota, K. (1990). Preferred hand use in the Japanese macaque troop, Arashiyama-R,
during visually guided reaching for food pellets. Primates 31 (3), 393-406.
MacNeilage, P.F. (1991). The "postural origins" theory of primate neurobiological
asymmetries. In The Biological Foundations of Language Development (pp. 319-
341), Krasnegor, N., Rumbaugh, D. M., Studdert-Kennedy, M.G., and Schiefelbusch,
T. (eds.). Academic Press, New York.
MacNeilage, P.F. (1993). Implications of primate functional asymmetries for the
evolution of cerebral hemispheric specializations. In Primate Laterality: Current
Behavioral Evidence of Primate Asymmetries (pp. 319-341), Ward, J.P., and
Hopkins, W.D. (eds.). Springer-Verlag, New York.
MacNeilage, P.F., Studdert-Kennedy, M.G., and Lindblom, B. (1987). Primate
handedness reconsidered. Behavioral and Brain Sciences 10, 247-303.
Marchant, L.F., and McGrew, W.C. (1991). Laterality of function in apes: A meta-
analysis of methods. J. Human Evol. 21, 425-438.
Marchant, L.F., and McGrew, W.C. (1992). Laterality of limb function in wild
chimpanzees of Gombe National Park: Comprehensive study of spontaneous
activities. J. Human Evol. 30, 427-443.
Masataka, N. (1989). Population-level asymmetry of hand preference in lemurs.
Behavior 110, 245.
Mason, A M., Wolfe, L.D., and Johnson, J.C. (1995). Hand preference in the Sifaka
(Propilhecus verreauxi coquereli) during feeding in captivity. Primates 36(2), 275-
280.
Matoba, M., Masataka, N., and Tanioka, Y. (1991). Cross-generational continuity of
hand-use preferences in marmosets. Behavior 117(3-4), 281-286.
McGrew, W.C., and Marchant, L.F. (1992). Chimpanzees, tools, and termites: Hand
preference or handedness? Curr. Anthro. 33, 114-119.
51


McGrew, W.C., and Marchant, L.F. (1994). Primate ethology: A perspective on
human and nonhuman handedness. In Handbook of psychological anthropology (pp.
171-184), Bock, P.K. (ed.). Greenwood Press, Westport, CT.
McGrew, W.C., and Marchant, L.F. (1996). Laterality of hand use in great apes. In
Great Ape Societies (pp. 255-274), McGrew, W.C., Marchant, L.F., and Nishida, T.
(eds.). University Press, Cambridge.
Megirian, D., Weller, L., Martin, G.F., and Watson, C.R.R. (1977). Aspects of
laterality in the marsupial Trichosurus vulpecula (brush tailed possum). Annals of
the New York Academy of Sciences 299, 197-212
Milliken, G.W., Forsythe, C., and Ward, J.P. (1989). Multiple measures of hand-use
lateralization in the ring tailed lemur (Lemur cat (a). J. Comp. Psychol. 103,262-
268.
Morell, V. (1991). A hand on the bird and one in the bush. Science 254, 33-34.
Preilowski, B. (1993). Cerebral asymmetry, interhemispheric interaction and
handedness: Second thoughts about comparative laterality research with nonhuman
primates about a theory and some preliminary results. In Primate iMterality:
Current Behavioral Evidence of Primate Asymmetries (pp. 125-148), Ward, J.P., and
Hopkins, W.D. (eds.). Springer-Verlag, New York.
Quiatt, D., Dudgeon, D., and Quiatt, S. (1991). Rhesus monkeys prefer right hand for
lifting feeder bin lids. Amer. J. Phys. Anth, Supplement 13 (abstract only).
Rawlins, R.G. (1993). Locomotive and manipulative use of the hand in the Cayo
Santiago macaques (Macaca mulatto). In The primate hand (pp. 21-30), Preuschoft,
H., and Chivers, D.J. (eds ). Springer-Verlag, New York.
Rogers, L.J. (1989). Laterality in animals. Int. J. Comp. Psychol. 3, 5-25.
Seltzer, C., Forsythe, C., and Ward, J.P. (1990). Multiple measures of motor
lateralization in human primates (Homo sapiens). J. Comp. Psychol. 104, 159-166.
Stafford, D.K., Milliken, G.W., and Ward, J.P. (1990). Lateral bias in feeding and
brachiation in Hylobates. Primates 31(3), 407-414.
52


Takeda, S. (1994). Hand specialization in social grooming behavior in Japanese
macaques (Macaca fuscata). In Current Primatology Vol. Ill: Behavioural
Neuroscience, Physiology, and Reproduction (pp. 31-55). Anderson, J.R., Roeder,
J.J., Thierry, B., and Herrenschmidt, N. (eds.). University Louis Pasteur, Strasbourg.
Tan, U. (1987). Paw preference in dogs. International J. of Neuroscience 32, 325-
329.
Tan, U., and Kutlu, N. (1991). The distribution of paw preference in right-, left-, and
mixed-pawed male and female cats: The role of a female right-shift factor in
handedness. International J. of Neuroscience 59, 219-229.
Tokuda, K. (1969). On the handedness of Japanese monkeys. Primates 10,4146.
Toth, N. (1985). Archaeological evidence for preferential right-handedness in the
lower and middle Pleistocene and its possible implications. J. Hum. Evol. 14,607-
614.
Vallortigara, G., Regolin, L., Bortolomiol, G., and Tommasi, L. (1996). Lateral
asymmetries due to preferences in eye use during visual discrimination learning in
chicks. Behavioural Brain Research! A, 135-143.
Ward, J.P., Milliken, G.W., Dodson, D.L., Stafford, D.K., and Wallace, M. (1990).
Handedness as a function of sex and age in a large population of lemur. J. Comp.
Psych. 104, 167-173.
Ward, J.P, Milliken, G.W., and Stafford, D.K.,(1993). Patterns of lateralized
behavior in prosimians. In Primate Laterality: Current Behavioral Evidence of
Primate Asymmetries (pp. 43-74), Ward, J.P., and Hopkins, W.D. (eds.). Springer-
Verlag, New York.
Warren, J.M. (1980). Handedness and laterality in human and other animals.
Physiol. Psychol. 8, 351-359.
Watanabe, K., and Kawai, M. (1993). Lateralized hand use in the precultural
behavior of the Koshima Monkeys {Macaca fuscata) In Primate Laterality: Current
Behavioral Evidence of Primate Asymmetries (pp. 183-192), Ward, J.P., and
Hopkins, W.D. (eds ). Springer-Verlag, New York.
53


Welles, J.F. (1975). The anthropoid hand: A comparative study of prehension. In
Contemporary Primatology (pp. 30-33), Kondo, S., Kawai, N., and Ehara, A. (eds.).
S. Karger, Basel.
Welles, J.F. (1976). A comparative study of manual prehension in anthropoids.
Saugetierkundliche Mitteilungen 24,26-37
Westergaard, G.C. (1991). Hand preference in the use and manufacture of tools by
tufted capuchin (Cebus appella) and lion-tailed macaque (Macaca silenus) monkeys.
J. Comp. Psychol. 105, 172-176.
Westergaard, G.C., and Suomi, S.J. (1993). Hand preference in capuchin monkeys
varies with age. Primates 34(3), 295-299.
Westergaard, G.C., and Suomi, S.J. (1996). Hand preference for stone artifact
production and tool-use by monkeys: Possible implications for the evolution of right-
handedness in hominids. J. Comp. Psychol. 30, 291-298.
Yeni-Komshian, G.H., and Benson, D.A. (1976). Anatomical study of cerebral
asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys.
Science 192, 387-389.
54


Full Text

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Hand Preference in Simple Reaching among the Arashiyama West Troop of Japanese Macaques (Macacafuscata) by Anastasia Forrester B. A, University of Colorado at Denver 1990 A thesis submitted to the University of Colorado at Denver in partial fulfillment of the requirements for the degree of Master of Arts Anthropology 1997

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This thesis for the Master of Arts degree by Anastasia F arrester has been approved -; I ,., t' ,: "J. ,:-) ,.L I Date

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Forrester, Anastasia (M. A, Anthropology) Hand Preference in Simple Reaching among the Arashiyama West Troop of Japanese Macaques (Macaca fuscata) Thesis directed by Professor Duane Quiatt ABSTRACT A free ranging troop of Japanese macaques (Macaca fuscata), consisting of about 500 members and residing in Dilley Texas, was observed from February to April ofl993. This study reports on the hand preferences of Japanese macaques during visually guided reaching for food. Hand preference was assessed for 317 bouts consisting of 10-105 reaches per bout. Hand preference across gender was shown to be more pronounced among adult monkeys when compared to younger monkeys (p=0.033). Adult males were shown to have a significant left hand bias (p=O. 0003) when compared with adult females. The presence oflateralized reaching is in agreement with the literature pertaining to this species. This abstract accurately represents the content of the candidate;, .. thesis. I reco publication. Signed d its e Quiatt iii

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DEDICATION I dedicate this thesis to my mother for her unending support and belief in my ability, and to Trygve for helping find the chutzpah to finish.

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ACKNOWLEDGMENT I would like to thank the anthropology department at the University of Colorado at Denver, for support during this research. Thanks also to Lou Griffin and Tracy Wyman of the South Texas Primate Observatory for access to their facility and for assistance in conducting research. Thanks also to Sean M. Mallory for assistance with the creation and interpretation of statistical results. Deepest thanks to my thesis advisor and my committee.

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CONlENTS CHAPTER 1. INTRODUCllON ........ -Why is Manual Laterality Important? ..... 2 What is Manual Laterality? ............................................ 3 2. BACKGROUND TO THE STUDY ............... ........................... 6 NonPrimate Laterality ........... 8 Primate Laterality ............................................................. 9 Japanese Macaque Studies. ........................................... l4 3. l\'IE.TH.ODS ..................................................................................... l9 Wcale 31ld Subject:s .......................................................... 20 Sample.. ............................................ ............................... 23 Data. CoUection .................................................................. 27 Sampling Limitations .................................. 29 4. RESlJL TS ............................ --.31 5. DISCUSSION AND CONCLUSION ......................................... 40 APPENDIX A. MONKEY FACE AND MA TRll.JNES ..................................... 44 BffiUOGRAP.HY .................................................................................................... 46 vi

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CHAPTER! INTRODUCllON Until the last decade there was a widely held belief that primates do not express manual laterality, that they do not exhibit a greater tendency to use one hand or the other for any particular task, or across any known set of tasks. Indeed, until ten years ago, this assumption appeared to be upheld by the available data. It also fit nicely with the concept that humans are somehow special, different in a fundamental biological sense from other animals. In this context there was little motivation to collect new data or to :further scrutinize existing data in search of evidence for manual laterality in nonhuman primates. Yet even in the absence of data, such an assumption is difficult to support given the apparent presence oflateral behavior in nonprimate vertebrates. That assumption contradicts evolutionary parsimony and would require the de novo development oflateralized behavior in humans. The goal of this research was to discover if the Japanese macaques at Arashiyama West would show the same patterns of manual laterality that have been observed for Japanese macaques elsewhere, as well as compare their laterality patterns with those other primate species.

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Why is Manual Laterality Important? Among humans, lateralized behaviors have been correlated with a variety of cognitive processes including some association with learning disabilities and autoimmune disorders. Geshwind and Behan (1982) observed that left handed people had 10 times the rate ofleaming disabilities, 2. 5 times the rate of autoimmune disorders, and a higher incidence of migraines than the general population. Such disorders also had a much higher incidence among the relatives of left banders. Additionally, disorders such as dyslexia, stuttering and autism are found in higher proportion among left handers than among right handers (Durden-Smith and Desimone 1983). This lends strong support to an intimate connection between lateralized behavior and numerous cognitive and physiological processes in humans. There are several reasons why the existence oflaterality in nonhuman primates is important. First, knowledge about whether the brain functions responsible for laterality are specific only to humans, or are possessed by nonhuman animals as well, can be useful in designing studies for which nonhuman subjects are used in lieu ofhuman subjects. Second, evolutionary models can be improved upon when there is some knowledge about the evolutionary development ofbrain functions, including laterality. Last, the existence oflaterality in nonhuman primates argues against the philosophical perspective that humans are unique and in some manner significantly different and better than other primates. 2

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What is ManuaJ Laterality? It is necessary to use some term to indicate the use of one hand rather than another when engaging in a task. When observing humans, this term is generally called handedness. However, increasing knowledge about the variability of such behavior has led to a plethora of definitions of handedness and the use of alternative terms. For example, Ward eta!. (1993 :45) used the terms 'hand preference' and 'hand performance'. Hand preference measures reflect relative incidence of use. Hand performance measures are typically efficiency measures that make possible comparison of the manner of performance and/or outcome of use of the left or right hand. (Ward et. a!. 1993:45). This means that hand preference refers to the quantity of reaches made with a particular hand in a particular task, whereas hand performance refers to the ability of a particular hand to successfully complete a given task. Hence, piclcing up food from the ground would likely be an hand preference task, while successfully manipulating an object to obtain food would be a performance task (one could, of course, with repeated trials, do a preference analysis on the latter task as well as a performance analysis). Harris and Carlsen ( 1993) defined hand preference in a similar way as Ward while adding the requirement that such preference be present across tasks to qualify as handedness. By 'handedness,' we ordinarily mean that the hands are asymmetric in use and function so as to reliably favor one hand or the other across a range of skillful acts. [and] by ['hand preference']. .. we mean only that an individual consistently uses one hand rather than the other for a given task (Harris and Carlsen 1993 :285). 3

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Preilowski ( 1993: 127) used different tenns to describe the same phenomena as Ward: Qualitative handedness [is] defined as a difference between right and left hand in quality and speed of performance; it was previously called "performance handedness" .... Quantitative handedness [is the] difference in the frequency of using right and left hand; it was called "preference handedness" before, since it was detennined in situations in which the subject could choose to use one or the other hand. Using these three researchers' definitions it is possible to conclude that there are at least three different ways in which manual laterality can be measured. A researcher can look for hand preference while an animal is engaged in a single activity by counting the number of times that animal uses one or the other hand; this would be called preference handedness, quantitative handedness, or hand preference. The speed or success rate of perfonning a particular activity can be compared between the two hands; this is performance handedness or qualitative handedness. The frequency with which one hand is used preferentially over a number of tasks or activities is called simply handedness. To help fill out the available literature on primate hand preference this paper reports the hand preferences found among a feral troop of Japanese macaques located in the United States. Monkeys were observed eating grains they picked up from the ground (Figure 1.1 ). This type of activity conforms with the definition of'hand preference' as used by Harris and Carlsen ( 1993 ), with data gathered via focal animal observations (Altman 197 4) of an individual performing the same task repeatedly. 4

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Figure 1.1 Japanese macaques eating grain. 5

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CHAYfER2 BACKGROUND TO THE STUDY Traditionally, handedness has been viewed as a uniquely human characteristic (MacNeilage, 1993). Early primate studies indicated only weak lateral tendencies and those were only observed at the level of the individual, rather than at the population level. In those few studies which did reveal manual preferences, the prevailing asswnption was that this was an artifact of some other part of the study (conditioning, training, etc.). In 1987 MacNeilage, Studdert-Kennedy, and Lindblom published a meta-analysis of primate laterality studies, finding that primates do indeed express hand preference and further, that the lack of consensus in the literature was likely a result of poor, inconsistent, or incorrect methodology. The results of this meta-analysis revealed some lateral hand bias across species and tasks. This conclusion brought about a flurry of renewed interest in the subject of primate manual laterality It has been widely presumed that the predominance of right-handed people was a result of some unique human cognitive function. Laterality has commonly been considered a speciesspecific trait associated with language and/or tool-making and -use, two other behavioral traits assumed to be unique to our species. "The most common notion is that handedness first evolved with hominid tool construction and use, and that language then either evolved directly, 6

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via sign language (Hewes, 1973), or indirectly, via spoken language." (MacNeilage, 1993 :326). Additionally, the strong role oflanguage in the conveyance of culture (including tool-use and tool-making) and its known association with lateralized brain function suggested a late evolutionary development of manual laterality. The implications of nonhuman asymmetries for human behavior are profound because they suggest that the presently accepted conclusion that hominid-specific lateralized brain specializations are keys to our uniqueness is wrong, and therefore needs to be replaced. The problem is most serious for handedness, which has hitherto been one of the main cornerstones of arguments for human uniqueness. (MacNeilage, 1993:319320) Although the particulars ofMacNeilage's argument have been the subject of much debate, continuing research is forcing theorists to abandon the notion that manual laterality is unique to humans. It is clear that individual nonhuman primates often exhibit lateral behaviors, including hand-use asymmetry, and that the mechanisms producing behavioral asymmetry may have deep evolutionary origins. Nonprimate Laterality Indeed, manual asymmetry and lateralized behavior are present not only in nonhwnan primates, but in many nonprimate species as well (reviewed by Bradshaw and Rogers, 1993). Paw preference has been observed among rats (Ratus ratus) and mice (Mus sp.) both at the individual level and at the population level for particular tasks. There is evidence for lateralized behavior in laboratory rats in tasks such as leading limb in rotation or locomotion (Glick 1985). Domestic cats show paw preference on an individual level (Tan and Kutlu, 1991) as do domestic dogs (Tan, 1987). Sugar gliders (Petaurns breviceps), koalas (Smith 1979), and 7

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possums (Trichosurns vulpecula, Megirian et al., 1977) also exhibit strong individual lateralization without significant population asymmetry (which was found in only one study for each of the last three species noted). Thus, though data are rather limited for nonprimate manunals other than rats and mice, available data indicate at least individual asymmetries. This is clearly an area in which more studies need to be undertaken. Lateral limb preferences have also been observed in birds. Rogers ( 1986) reviewed lateralized behavior in a variety of avian species (parrots, chickens, and cockatoos). Such lateralization ranged from footedness (only in species which use their feet during feeding) to lateralized behaviors associated with ocular processing. Such findings indicate that conditioning, fetal development, and hormone production may all contribute to lateralized behaviors displayed by chicks or adult birds. Are we then to assume that lateralized limb use evolved in mammals (including primates and humans) independently from its evolution in birds? Although there could be convergence for this type ofbehavior it seems more parsimonious to assume that laterality of function was present in the common ancestors ofboth birds and mammals. In fact, when the data for fish, reptiles, and amphibians are reviewed, it becomes obvious that these creatures also possess lateralization ofbehavior and, in some cases, limb use. For example, toads (Bufo bufo, B. marim1s, B. viridis) show front limb preference at the population level (Bisazza et al., 1996). Chameleons (Anolis carolinesis, A. sagrei) show lateralization of aggressive behavior (DeckeL 1996). Fish show lateralized escape (Jenynsia lineata, Bisazza et al., 1997, Girardinusfalcatus, Cantalupo eta!.), rotational (Oreocluomys mossambicus), and detour behavior (Gcunbusia holbrooki, Bisazza & Vallortigalla, 1996). The only conclusion that can be drawn from laterality studies over such a wide range of species, is that laterality is plesiomorphic for fish, amphibians, reptiles and birds, and mammals. Thus, it 8

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seems reasonable to expect that humans and other primates would exhibit lateralization of the brain with accompanying specialized behaviors. Primate Laterality Postural and manual asyrrunetries among primates are almost certainly due in part to the evolution of the hand and a grasping type oflocomotion and feeding activity. Like binocular vision, the flexible grasping five digit hand is an ancestral plesiomorphy for primates. This type ofhand is extremely useful for arooreallocomotion as well as for effective foraging in an arooreal substrate. The earliest primates were vertical clingers and leapers with visiospatiomotor specializations for unimanual predation (Fleagle, 1988). As MacNeilage et al. pointed out, this would initiate an entirely new feeding arrangement for primates: "Although having a heritage of about half a billion years ofbilaterally symmetrical midline predation involving the mouth, they switched to the hand as the organ of predation ... (1993 :329). In this situation the stronger limb might be used first for postural support while the other hand would be used for activities requiring more precise motor control (hunting, for instance), causing a physiological asymmetry of function to arise. Ths manual specialization would then constitute a plesiomorphy for the primate order Nwnerous studies have been conducted to investigate the possibility that laterality is indeed a primitive character for primates. Prosimians have been the subjects of a variety of studies which have shown hand preference (see Ward et al., 1993 for a review). For example, among ring-tailed lemurs (Lemur catta), Masataka (1989) found that 20 out of22 had a strong left hand bias and Milliken et al. (1989) found that left hand preferences were retained across 9

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tasks. Six species oflemur (L. catta, L. coronatus, L. macaco, L. mongoz L. mbriventer, and five subspecies of L. fulvus) were surveyed for hand use by Ward et al. (1990); this sample of 194 subjects showed a left hand bias. In 1984, Sanford found that among 25 lesser bushbabies (Galago senegalensis) there was little laterality when animals were in a quadrupedal stance, but when tested bipedally they tended to have a left hand bias. More recently, Mason et al. (1995) found a tendency to lateralized feeding among sifakas (Propithecus ven-eauxi coquereli). All of these researchers have shown that prosimians do show laterality on the individual level and that they may have a left hand bias at the population level across all prosimian species. Functional laterality has also been found in New World monkeys. Matoba et al. (1991) looked at the relationship between hand preference and matriline among common marmosets (Callitfu-ixjacclms). They found a consistent correlation between mother's hand preference and that of her infant in 23 family groups (they foWld no such correlation between fathers and infants). In 1990 Fragaszy observed capuchins (Cebusapel/a) and found that they exhibited a left hand preference during simple visually guided reaching tasks and a right hand preference when engaged in nonvisual or novel tasks. Capuchin monkeys have also been studied extensively by Westergaard et al. ( 1996, 1993) who have demonstrated that capuchins show lateral preferences in tool use and manufacture with the right hand being preferred for demanding tasks. King and Laudau (1993) observed squirrel monkeys (Saimiri sciureus) and found increased preference, either left or right, with demanding tasks and little preference with simple reaching. In goldfish catching-a demanding, highly visual, posturally Wlstable, and ballistically performed (that is, the trajectory of the reach was not modified after initiation) task in which the monkeys used three limbs to balance on the edge of a tank and one hand to attempt to catch the goldfish-produced a strong left hand preference, whereas pronounced right hand preferences were found with vertical clinging tasks. Thus, among New World monkeys there appears to be lateralization ofhand preference on the individual leveL and in some specie&'tasks 10

PAGE 17

at the population leveL with the left or right preference appearing as highly task -specific in some cases. Old World monkeys also express asymmetrical laterality. In 1987 Fagot and Vauclair studied a troop ofbaboons (Papio papio) and observed that, while individuals strongly preferred one hand over another, there was no population bias toward either hand. In another study conducted in 1988 they found that baboons exhibited a left hand preference in tasks which were intensively visuospatial. Fragaszy and Adams-Curtis (1993) observed crab-eating macaques (Macaca facicularis), and found no significant hand bias across tasks or by sex or age of animals. In another study Fagot ( 1991 ), observed that rhesus macaques exhibited a left hand preference while hanging or sitting, but exhibited no preference while standing bipedally. According to Fagot, ... the requirement to use one hand to carry the monkey's weight or maintain balance does not appear to predict the degree ofhand bias." (p. 266). Forrester and Quiatt ( 1994) observed that rhesus macaques (Macaca mulatta) lifting the lids of feeder bins and removing food showed a preference for reaching with the left and lifting lids with the right. Similarly, non-lifting macaques in this study showed an equal frequency of either left or right hand use when a lid-lifting companion held the lid up. Studies of Old World monkeys seem to indicate a strong tendency for the individual to be handed, but so far data suggests no population level asymmetries. Manual laterality in apes varies widely across species. For example, a right hand preference was found in adult female gibbons (Hylobates far), adult males showed little lateralized manual preference when reaching for food, and neither showed any asymmetry for leading limb during brachiation (Stafford et al., 1990). Orangutans (Pongo pongo ), who have been little studied as of this writing, have not been observed to demonstrate manual laterality (Olson et al., 1990). Out of 47 captive lowland gorillas (Gorilla gorilla beringei), 72% 11

PAGE 18

exhibited a strong right hand preference across a range of activities (Shafer, 1988), whereas Byrne ( 1991) saw no evidence oflaterality among wild mountain gorillas (Gorilla gorilla gorilla) when engaged in natural behaviors. While chimpanzees (Pan troglodytes) show a preference for one side or the other, there has been no observed consistency as to which side they prefer (Boesch, 1991, and see Marchant and McGrew, 1991, for a review), although it appears that infants have a slight right hand bias when observed for hand to mouth, one hand grasping the other hand, defensive grasp, and first step (Bard et al., 1990). Bonobos (Pan paniscus) showed no lateralization across a wide range ofbehaviors and showed only a slight preference for right leading limb in quadrupedal locomotion (Hopkins and De Waal, 1995). So far the ape literature is rather contradictory, with gorillas having shown the highest degree of laterality in captivity and with all field studies showing mixed results that tend toward laterality at the individual level rather than at the population level. The majority ofhuman handedness studies have shown an adult population right hand bias estimated to range from 85 to 92 percent (Annett, 1985; Bryden, 1982; but see McGrew and Marchant, 1994). Harris and Carlson (1993) made the observation that simple visually guided reaching assessments are the most common measures of handedness used with human infants and with nonhuman primates. In an effort to help balance the literature they set about testing adult humans using simple visually guided reaching for a variety of objects placed at various orientations to the body. When an object was placed at the mid-line of the subject's body the dominant hand was used from 68 to 85 percent of the time. When an object was placed on the dominant side there was a 90 percent use of the dominant hand, versus 60 to 75 percent dominant hand us when the object was placed on the nondorninant side. Distance of the object from the subject had no effect and the size of the object only affected hand use if the object was large. Lateralization was slightly stronger for women. The measures used in this study are comparable to those used most commonly to assess manual preference in nonhuman 12

PAGE 19

primates. That is, the individuals were engaged in a "simple reach" wherein an object was simply picked up and released; this bears more resemblance to many nonhwnan primate studies which focus on simple reaching for food objects (the main difference being the mouth as the terminal receptacle among the majority of primate studies). Unlike earlier estimates, this study showed the adult human population to be less handed than previous estimates. It is significant that dissimilar methodologies may have contributed to the difference observed between humans and nonhuman primates. McGrew and ( 1994) found a wide range of variation in hwnan handedness estimates published in a number of studies (p. 179). Interestingly, they found that estimates of handedness varied from less than 1% left handed (Katanga, Zaire) to more than 22% left handed (Kwakiutl, British Columbia, Canada). This is in contrast to the common beliefthat 10% of humans are left handed. In fact, in their study in 1995 of videotapes of individuals in three traditional societies, humans were ambilateral in non-tool-using activities with only tool use and tool use with a precision grip gaining significant laterality (reviewed in McGrew and 1996:270). This evidence is not unlike the hand preference evidence for some nonhuman primates such as Japanese macaques (Itakura 1992), baboons (Fagot and Vauclair 1987), and capuchins (Westergaard 1993, 1996), suggesting that the perceived difference in hand preference between humans and nonhuman primates may indeed be methodological. A review of the literature across primate species leads to the conclusion that hand preference is an expected part of primate behavior. To quote MacNeilage, there are "enough instances oflateralized behavior in nonhuman primates at the population level to demand the conclusion that this phenomenon exists, although there will, no doubt, continue to be tenacious resistance to this conclusion" ( 1993 :319). I would also propose that lateralization at the individual level may be as important as lateralization at the population level. The fact that 13

PAGE 20

animals are lateralized one way for some tasks and a different way for other tasks, is in and of itself interesting and may provide clues about cerebral lateral fi.mction. This study measures hand preference among monkeys by counting reaches made during feeding. The data are then used to analyze the pattern ofhand preference among the Arashiyama West troop so that it may be compared with other research done on manual laterality in Japanese macaques as well as in other primate species. I have not attempted to identifY which hand is being used across a range of tasks, but rather, have looked for frequency of same hand use in one task. According to Harris and Carlsen, in their disrussion of visually guided reaching tasks: "insofar as human adults show hand preference on this task consistent with their known handedness, it suggests that the task, at least in principle, would be appropriate as a test of handedness in other primates" (1993 :301 ). Thus a simple reaching task has been used to detect hand preference among several categories of Japanese macaque. Japanese Macaque Studies The data for individual species vary enough between those species that it is necessary to compare the findings of this study most closely with the studies done on Japanese macaques in the past. Research on hand preference in Japanese macaques (Macacafuscata) has been pursued in Japan with provisioned animals. Studies have used three provisioned groups: Takasakiyama (ltani, 1957; Itani et al., 1963), Kashima (Tokuda, 1967; Kawai, 1969; Watanabe et al., 1993), and Katsuyama (Takeda, 1994). Three captive studies have also been conducted: one of a group known as Arashiyama-R (Kubota, 1990), one of two animals at the 14

PAGE 21

Primate Research Institute inK yoto (Itakura, 1992), and one of nine monkeys housed at the Zoological Garden, Berlin (HarigeL 1994). To better interpret this research, I will summarize the data from all of these studies. Two studies were conducted using the Takasakiyama troop as the sample population. In 1957 Itani submitted the first report on hand preference among Japanese macaques in which he assessed lateral bias for picking up wheat grains (Itani, 1957, cited in Kubota 1990; I have used Kubota's sununary because the original text is in Japanese). ltani observed 81 aduh animals and found that there were significantly more monkeys with a left hand preference than there were monkeys with a right hand preference (30 left, 16 right; p<0.05). In 1963 Itani conducted another study in which peanuts were thrown to monkeys, and after the peanut hit the ground the hand used to pick up the peanut was recorded. Monkeys were classified into four age groups and though there was no indication of a population level asymmetry, monkeys did show an increased tendency to use the left hand in the older age categories. Both of these studies have been criticized for failing to explain by what method hand preference was determined (MacNeilage, 1987; Kubota, 1990). The Koshima troop has been used in three different studies to date. In the first, monkeys were thrown sweet potatoes and the hand( s) used to catch them were recorded. Initially, monkeys caught potatoes with both hands, but later tended to use only one hand. Nme monkeys caught the potato with either both hands or the left hand, 11 caught the potato with both or either hand, and four used both or the right hand to catch (Kawai, 1967). Tokuda also did research on this troop in which peanuts were thrown to individuals and the hand used to pick up the peanut was recorded (following Itani's research). Each animal had 10-20 peanuts for which hand preference was recorded. Hand preference was determined by having 8 of 10 reaches with the same hand. If a monkey failed to show a strong preference within the first 10 15

PAGE 22

throws, an additional I 0 throws were administered to see if the animal would exhibit a preference. The total number of monkeys observed was 41, with 17 preferring the left, 8 preferring the right and 16 showing no preference. In 1993 the Koshima monkeys were the subjects of a hand preference study conducted by Watanabe et al. In this study the researchers focused on hand preference in 1) picking up wheat, 2) washing wheat, and 3) washing potatoes: ... our data suggest that feral monkeys display a general left hand preference in picking up wheat grains, washing wheat grains, and washing sweet potatoes" (Watanabe et al., 1993:191). Unlike Itani 1963 this study did not find any preference bias that correlated with the age of the subject. A third provisioned group, Katsuyama, was observed by Takeda in 1994. In this study the researcher observed social grooming behavior among members of this free-ranging troop. Takeda noted which hand was used for picking during grooming and found that there were no significant asymmetries for the population. The sex of the monkey showed no correlation with hand preference. Takeda did observe a slight tendency for older animals to use the left hand, but this finding was not statistically significant. Further, there appeared to be no correlation between a mother monkey's hand preference and that of her offspring. Individual animals did show preference, thus confinning the presence oflaterality on an individual level. Overall, this study would suggest that either monkeys at this location do not display significant population-level manual laterality, or that grooming may not be an activity useful for measuring laterality. In 1990 Kubota conducted a hand preference study using the group of monkeys called the Arashiyama-R troop. These monkeys are housed in an outdoor enclosure in a large social group. For this study 45 monkeys were observed and the sample was broken down by both sex and age. Monkeys were shown to have more preference for either one hand or the other (versus lack of preference) in older classes. While this study confirmed an increase in hand 16

PAGE 23

preference with age, it failed to show that preference to be to the left. The only sex related finding suggested than among young females there was a tendency for no preference while among older females some preference was more common (Kubota 1990). In a series of controlled laboratory experiments, Itakura ( 1992) looked for hand preference in two captive born adult male monkeys. The two subjects were given several tasks which included simple reaching and simple reaching using a mirror for guidance (the piece of fruit could only be seen in a mirror). In these two tasks both of the monkeys used their left hands more than 95% of the time. Three further tasks were also presented in which the monkey had to locate a piece of fruit using a mirror for guidance while reaching around a large barrier. This meant that the monkeys could not see either the fiuit or their hand directly, but were required to use the mirror to obtain the reward. In contrast to the first two tasks, these three tasks resulted in 88-9
PAGE 24

have a strong preference for one hand or the other. Like the research by Itakura, this study has few enough subjects that extrapolation of data to a population would be highly speculative at best. However, this study does indicate that individual animals have hand preferences. At the time of this writing there had been a total of nine studies which reported hand preference among Japanese macaques. In a number of studies macaques were observed to have a slight left over right hand preference (Itani 1957, Kawai 1967, Watanabe et al. 1993), though in two studies this was only seen among older monkeys (ltani 1963, Takeda 1994). Even in studies where there were more monkeys who preferred the left to the right hand, there was still a nearly equal or greater number of animals who exhibited no preference (Kawai 1967, Kubota 1990), while Watanabe et al. (1993) found no correlation between hand preference and the age of his subjects. The association between handedness and the sex ofJapanese macaques has not been extensively analyzed. There have been three studies that sought to correlate sex with hand preference. Takeda ( 1994) found no hand preference differences between males and females, Harigel ( 1994) found females had a slightly higher number of right -banders when compared to males (not, however, enough to be statistically significant), and Kubota found a slight right hand preference in adult female monkeys when compared to male monkeys. Finally, it is interesting to note that ltakura ( 1992) found that two male macaques had a left hand preference during visually guided reaching and a right hand preference when visual guidance could only be accomplished by looking in a mirror. Taken together, these data suggest that among Japanese macaques there may be a slight hand use preference to the left which may increase with the age of the subjects, there may be a difference correlated with the sex of the subjects, and task complexity may influence hand preference. 18

PAGE 25

CHAPTER3 M.EffiODS igure 3.1 Adult male macaque at Arashiyama fest in Dilley Texas. 19 A field study ofhand preference was conducted during the months ofF ebruary and March of 1993 at the South Texas Primate Observatory in Dilley, Texas. This facility supports a troop of Japanese macaques (Figure 3.1) known as the Arashiyama West troop. Data on hand preference were collected on 22 days during daily feedings between February 4th and March 15th of 1993. Subjects were categorized by age and sex. Monkeys were observed while eating grain and the number of times each hand was used for this task was recorded.

PAGE 26

Locale and Subjects In the late 1960s a troop of monkeys in Japan called the Arashiyama troop increased in number and eventually split into two groups. The animals from one of the newly created troops began to interfere with hwnan settlements in the area. Rather than exterminate the animals, efforts to find the troop a new home were pursued, and in 1972 its members were trapped and transported to North America where they became known as the Arashiyama West troop (F edigan, 1991). Edward Dryden, Jr., an American rancher, arranged to take the troop and maintain it for both commercial and scientific purposes on his south Texas ranch. About two years after the troop arrived, Mr. Dryden died and his wife, Clementina, took over support of the troop. She later transferred care and ownership to the Arashiyarna West Institute, a group of interested researchers who moved the troop in 1980 to the Dilley, Texas site. Since that time an organization has been formed called the South Texas Primate Observatory. At the time of this study, the monkeys were maintained at the Dilley location under the management of the South Texas Primate Observatory The Arashiyama West troop is the only troop to have been studied in Japan before being trapped as an intact group and shipped and released in the United States. It has been studied intensively since its arrival here in 1972. The number of animals originally shipped was 150. When the troop was relocated to Dilley, it had grown to about 300 animals, doubling the initial population in eight years (Fedigan, 1991). Research on this troop is especially interesting because it can be compared with the original main troop-known today, particularly in the United States, as the Arashiyama East troop-which was left intact and is still under observation in Japan. Thus, the two groups can serve as genetically close comparison populations. In 1974, the troop maintained a male-to-female ratio of I :2. At that time about 3% of the population 20

PAGE 27

was over 18 years of age. In 1989 The troop was estimated to have 4 70 animals with about 46% of those being under 4 years of age. There is no estimate of the number of animals over 18 years old available at the time of this writing (Fedigan, 1991 :66). At the time of this hand preference study the Arashiyama West troop lived in a free ranging state about 12 miles from the town ofDilley, Texas. The site had at one time been an electrified enclosure, but the fence had fallen into disrepair, leaving the monkeys free to roam. The area where the monkeys were fed was cleared of vegetation to enable vehicle access. Near the main feeding area were two ponds which had vegetation growing all around them and which supplemented water tanks for drinking. The Arashiyama West troop was provisioned daily with 150 pounds of grain, either cracked com or milo, and with 50 pounds of monkey chow; once per week, they were provisioned with a truckload of fruit (Figure 3.2). The animals were always at this site during feeding times. Figure 3.2 Monkeys following feeding truck. 21

PAGE 28

The population at the South Texas Primate Observatol)' consisted of three groups totaling an estimated 500+ individuals. The bulk of the population, approximately 300-400 individuals, formed the main troop. The alpha male of the main troop when I anived was 'Fang' (Figure 3 .3), the beta was 'Rocky,' and the third in corrunand was 'Ran.' These three most central males were older, Japanese-born monkeys who had reasonably stable social relationships. The alpha female of the dominant matriline was 'Lady Di.' By the end of this study the troop had undergone great social change, attributed to cougar predation. Both the alpha and beta males were killed, leaving Ran as the leader. These circumstances seemed to make the monkeys jumpy and hard to observe for extended periods; this reduced the number of total reaches per monkey as well as the total number ofbouts observed per day. Figure 3.3 Alpha male Fang eating corn. A splinter troop Imown as the Pelka troop had split from the main troop in 1990. This troop was usually separated frorn the main troop by at least 50 yards and had about 70 22

PAGE 29

members. The Pelka troop did not suffer the same degree ofloss as the main troop and was somewhat more socially stable during the end portion of the research. The third group of monkeys consisted mainly of peripheral males: adult and sub-adult males who maintained a distance of at least 20 yards from the main and Pelka troops at most times. Occasionally, a female would be observed with one or more members of this group of males. For the most part, this subset of monkeys seemed to be a loosely organized coalition which might be spread out over great distances. Monkeys migrated out of this group with regularity (presumably intending to migrate to other troops as they would in their native environment); these would be caught and kept in cages to prevent their trying to leave again, since there are no other troops in Texas for these monkeys to migrate to. One way in which this study differs from the majority of other laterality studies is that the subjects are free ranging. The vast majority oflaterality studies have been conducted with captive animals. There are a variety of reasons for this, including the greater ease of creating demanding tasks-which have been shown to bring out lateral bias-in a captive environment. Notably, however, there have been a nwnber of previous laterality studies on free ranging Japanese macaques. The Arashiyama West troop is free ranging, provisioned, and heretofore unstudied for hand preference and is well suited to being used as a comparison group to the aforementioned studies. Sample Observations were taken after the monkeys had been fed, generally mid-to late morning. Feeding usually took several hours with monkeys dispersing in the late afternoon. 23

PAGE 30

The area where the monkeys were fed was flat and dry with vegetation consisting mainly of sagebrush and mesquite. Daytime temperatures remained within the 70s and 80s (Fahrenheit). Access to the facility was poor during wet weather, so nearly all observation periods were initiated when the weather was warm and dry. For data collection and subsequent hand preference analysis, observed monkeys were categorized by age and sex. Tattoo identifications (see Appendix A) of individuals were noted whenever possible to afford checks for accuracy of age and sex categories. Young monkeys were difficult to sex and occasionally sex could not be identified. Thus, three codes were used: male, female, and unknown, the last for animals whose sex was not determined (infants and some juveniles). Adult males and females were readily distinguished; fully adult males are generally larger than females and had obvious genitalia and a full muscular shoulder girdle which extends armmd the shoulder and neck area of the animal. Adult females were most easily identified when they had infants or juvenile offspring or when there were obvious signs of estrus or lactation. Sub-adult males and females were difficult to differentiate; these animals, typically not mature in appearance, were not as strongly marked by the secondary sex characteristics described above. Sub-adult males tended to associate in a peripheral same-sex group, which helped in identifYing sex, but the only conclusive diagnosis was provided by sighting genitalia or tattoo identification. Infants and juveniles by and large were not tattooed so there was no secondary method to check for correct sex identification. Very young animals, then, were not distinguished by sex, only by age. Monkeys were categorized as old, adult, sub-adult, juvenile, or infant. Old animals were those monkeys which were born before 1972 and had been brought over to the U.S. from Japan. Old females were generally very gray and decrepit-looking and past reproductive age (though some would still exhibit signs of estrus). There were fewer old males than old females 24

PAGE 31

and they tended to be fairly robust in appearance with a very pronounced shoulder girdle of muscle. Adult animals were those monkeys of reproductive age born in Texas after 1972, but before 1984. Adult females were detected by body size, appearance of nipples, signs of estrus, having offspring, or by individual identification (Figure 3.4). There were considerably fewer adult males than adult females due to the high death rate among males in this age group. Adult males were distinguished by a muscular shoulder girdle and by being generally larger than females and subadults, but without the robustness of old males. Figure 3.4 Lactating adult female macaque. 25

PAGE 32

Sub-adult monkeys were generally pre-reproductive and lacked obvious secondary sex characteristics. They were larger than juveniles and infants and had been born between 1984 and 1988. Sub-adult females were recognized as having smaller than adult body size, undeveloped nipples, and no signs of estrus, with confumation when possible by identification of the individual. Sub-adult females stayed close to females of their maniline and were not often seen outside the troop. Sub-adult males tended to be smaller and had an overall lighter body frame than fully adult males. They were usually found on the periphery of the main or Pelka troops and roamed together in a troop consisting mainly of males of this age. Figure 3.5 Infant macaque, born in 1992. Infants and juveniles were newborn to approximately five years of age (Figure 3. 5). Sex was coded as unknown for animals in this age group. Initially monkeys were placed in separate categories if they were under one year in age, one to two years, two to three years, and four or five years. Later, these four categories were combined in the single category 'infanttjuvenile' for the purpose of analysis. The reason for combining these groups was twofold: first, when broken into four groups, there were very few bouts within some of these categories (for example, there were a total of only 12 bouts with infants as focal animals), secondly, since all animals with unknown sex were within these categories, they made a natural category which could be compared with the adult population of both sexes. 26

PAGE 33

Monkeys at the Arashiyama West site are identified by facial tattoos which were developed from a coding system used in Japan for monkey identification. They also have a number tattooed on the inside of the right thigh. Very few adult animals did not have tattoos; however, a great number of infants and juveniles had not been so marked. Unfortunately tattoos are often hard to read without disturbing the animal enough to end the observation session. Visible tattoos were transcribed onto observation sheets and later decoded using the decoding monkey face (see appendix A). Tattoo identifications showed a near perfect correlation with sex and age assessments, leading to a high degree of confidence that assignments of sex and of age were correct. Data Collection Monkeys were only selected for observation while sitting and eating grain. Grain was poured out of the back of a truck along a dirt road that was approximately one mile long. Daily observations usually began at the end of this feeding area, furthest from the grain storage area. This furthest point generally attracted the largest number of monkeys, those more socially dominant and able to compete in a more densely populated feeding area. Focal subjects were selected on the basis of proximity while moving back toward the grain storage area. Each day efforts were made to sample individuals from the largest number of age and sex categories possible. Observations were conducted until the monkeys left the area, until observer fatigue set in, or until the weather precluded further observations. As a result of how focal animals were 27

PAGE 34

chosen, members of the main troop were more heavily sampled than those of the Pelka troop or of the peripheral group. Once a focal animal was selected for sampling, an observation sheet was started (Figure 3.6) and the animal's sex, age, and tattoos were recorded. Monkeys were observed while picking grains up and eating grains from the ground; the hand used by the monkey to pick up grains during 10-110 sequential reaches was recorded. Additionally, information about the type of grain being eaten and the position of the monkey throughout the bout were recorded (each observation sheet equaled one bout). Each monkey was observed until one of two terminating acts occurred: I) the animal moved to a location that made continued observation impossible, or 2) the end ofthe data recording sheet was reached. In a few cases, the 100 reach limit ofthe observation sheet was extended by using a single square for two entries, but observation of an individual was usually stopped after 100 entries to prevent any single monkey from contributing a disproportionate fraction of the total data collected. When the observation sheet was completed, another monkey was chosen and the process began again. 28

PAGE 35

Age Sex # Stress Feed Notes Figure 3.6 Sample observation sheet used in the field for recording monkey hand usage. The grid was used to record each instance of hand use as either R or L; color codes (using a 4 color pen) were used to distinguish between sitting and standing and between com and milo. The face was used to record information about the monkey's facial tattoos; thigh tattoos were recorded if readable. Sampling Limitations Due to limited observation time and resmrrces, monkeys were not identified on an individual basis (except to verifY age and sex assessments made in the field). Every attempt was made to samole as many individuals as possible. To accomplish this, no single individual was 29

PAGE 36

ever observed twice in one day. Data were taken by moving from one section of the troop to another in a methodical manner, observing monkeys who were ever more distant from the starting point. Whenever there was some doubt as to whether the animal had already been observed, no further sample was taken and that bout was not included in the analysis. An observation period in which a monkey made less than 10 reaches or in which the age or sex categorization was undetermined or in doubt was discarded from analysis. 30

PAGE 37

CHAPTER4 RESULTS A total of20,283 reaches for grain by monkeys over 314 behavioral bouts recorded dwing 22 days of observation were analyzed. The majority of animals observed were sub adults, adults, or old animals (72%) with about 28% of the bouts representing infant or juvenile monkeys. About 54% ofthe observations were offemales, about 37% were of males with the remaining g<>fo being of unknown gender. The age and sex breakdown of the sample is shown in table 4.1. Sex Female Male Unknown Total Infant 0 1 11 12 (.04) Juvenile 24 32 17 73 (.23) Age Sub-adult 47 55 0 102 (.32) Adult 80 23 0 103 (.33) Old 19 5 0 24 (.08) Total 170 (.54) 116 (.37) 28 (.09) 314 (1.00) Table 4.1 Number of monkeys in each age/sex category (n=314). 31

PAGE 38

Figure 4.1 describes the nwnber of reaches made by monkeys per bout. There were no bouts with less than 10 reaches, nor were there any bouts with more than 11 0 reaches. There were more bouts within the 90-100 reaches per bout range than within any other range. 0 0 0 CD Ill .... = Q 0 lrl
PAGE 39

portion of the population at any given point which deviates from the expected density. 1.0 on the vertical axis represents the expected value for the population. Each number vertically is the number of monkeys with an observed degree of hand preference compared to or divided by the expected number from pure chance. Each of the small circles lined above the horizontal axis represents one bout in the described sample. The line above the circles describes the density of bouts (circles) at any given point and how that density deviates from the expected value. The density plot (Figure 4.2) shows the placement of each bout on the horizontal left to right continuum. Notice that the distribution of the population is skewed toward the left, indicating a tendency for left hand preference. There are notable spikes at both the left and right side of the plot which indicate that some bouts were entirely left or right handed. 33

PAGE 40

2.0 .... 1.5 Ill = Gl = 1.0 Cl -= ell "3 .::1. Cl Po! 0.5 0.0 Q!:(J!:t(l*'* .. 0.0 0.2 0.4 0.6 0.8 1.0 Degree of Lateral Preference Figure 4.2 approximate density function for ratio of reaches in the entire sample population, N=314 bouts. Across the horizontal axis 0 represents all reaches with the left hand, 1 represents all reaches with the right hand. The vertical axis represents the approximate density function for the population (average= 1 ). Infant and juvenile monkeys have been split out from adults and combined into one group in the density plot shown in figure 4.3. Combining these groups seemed appropriate because a significant proportion of the bouts recorded for infants and juveniles were of monkeys whose sex was unknown, and there were only 12 infant observations, none of which contained more than 60 reaches. The monkeys in this group were spread out nearly evenly along the 34

PAGE 41

horizontal axis indicated a lack of strong preference for either hand for this group, although clearly a few individuals were strongly biased to either the right or the left. 2.5 2.0 t> 1.5 .... = Qj A = Q 1.0 "+:I "' '"3 c. Q 0.5 0.0 0.0 0.2 0.4 0.6 0.8 1.0 Degree of Lateral Preference Figure 4.3 approximate density function for ratio of reaches in the infantjuvenile population, N=85 bouts. Across the horizontal axis 0 represents all reaches with the left hand, 1 represents all reaches with the right hand. The vertical axis represents the approximate density function for the population (average= 1 ). The next density plot (Figure 4. 4) shows hand preference for the entire sample of adults without regard to sex. This plot shows a substantial skew in the population toward the left. It is especially noticeable how few of this sample prefer the right hand. 35

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2.5 2.0 to .... Ill -... 1.5 Q,) = Q .c 1.0 Cll "3 Cl. Q Pol 0.5 0.0 0.0 0.2 0.4 0.6 0.8 1.0 Degree of Lateral Preference Figure 4.4 approximate density function for ratio of reaches in the adult population, (both male and female) N=229 bouts. Across the horizontal axis 0 represents all reaches with the left hand, I represents all reaches with the right hand. The vertical axis represents the approximate density function for the population (average = 1 ). Differences between the density plots of the ymmg monkeys (infants and juveniles) and adult monkeys ( subadults, adults and old animals) are striking, showing a much greater trend toward left hand use in the adult population. When compared using at-test, a p value of.03333 was found, indicating a statistically significant tendency toward left hand usage in the adult monkey portion of the sample when compared to the young monkey portion of the sample. Next, the adult population was broken down by sex of monkey. The adult female density plot (Figure 4 5), shows a fairly even distribution of hand preference across this sub-36

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population. Adult females were most often in the middle of the plot without substantial obvious hand preference, although there were a few individual bouts which showed very strong preference to either the left or the right. 3.0 .....---'-------'-------'--------'------'--------J'---,.._ 2.5 2.0 t> .... 1.5 = G) A 8 1.0 .c ell ::1 g. 0.5 0.0 ''''""'' rrooo 0.0 0.2 0.4 0.6 0.8 1.0 Degree of Lateral Preference Figure 4.5 approximate density function for ratio of reaches in the adult female population, N= 146 bouts. Across the horizontal axis 0 represents all reaches with the left hand, 1 represents all reaches with the right hand. The vertical axis represents the approximate density function for the population (average= 1). 37

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When a density plot was run for adult males (Figure 4.6), they showed a very significant skew to the left, with a majority of monkeys falling between the exclusively left side of the plot and the center. 2.5 2.0 to .... 11'1 = Cl) 1.5 A = 0 .c 1.0 n:t "3 0.5 0.0 0.0 0.2 0.4 0.6 0.8 1.0 Degree of Lateral Preference Figure 4.6 approximate density function for ratio of reaches in the adult male population, N=83 bouts. Across the horizontal axis 0 represents all reaches with the left hand, 1 represents all reaches with the right hand. The vertical axis represents the approximate density function for the population (average = 1 ). When compared to the adult female density plot the adult male density plot showed an extremely obvious tendency to use the left hand, while females were distributed more evenly between left and right hand preference. These two groups were analyzed using a t test which 38

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yielded a p value of.0003. This test demonstrates that in this sample adult males have a significant left hand preference when compared to adult females who showed no significant hand bias. Thus, the sample analyzed indicates that males are significantly more left handed than females and that adults are generally more left handed than infants and juveniles. 39

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CHAPTERS DISCUSSION AND CONCLUSION Significant differences were found between the young monkeys and the adult monkeys (ofboth sexes) when reaching for grain. This finding is consistent with other research on Japanese macaques (ltani 1963, Takeda 1994). The finding that adult males in this troop are significantly more lateralized to the left than are adult females is unexpected and suggests that there may be a sexual component to the determination ofhand preference among these monkeys. Kubota (1990) found that adults as a group tended to have stronger preferences than younger monkeys. This is in agreement with Itani ( 1957), who noted a greater left hand bias in the adult population of the monkeys at Takasakiyarna, but is at odds with Watanabe ( 1993 ), who found no correlation between age and manual laterality for the Kashima population but did find a slight left hand bias at the population level. Hand preference in the Arashiyama West troop was consistent with Itani's and Kubota's findings in that there was a greater tendency toward manual lateralization in adult animals, along with a tendency toward left hand bias. 40

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Unlike any of the previous studies with Japanese macaques, the Arashiyama West troop showed that adult males as a group have a distinct preference for using the left hand for eating. 1bat sex differences in hand preference have not been correlated in the literature is in part due to the infrequency of analysis based on sex differences (Kawai 1967, Tokuda 1969, Watanabe et al. 1993). In the study by Takeda (1994) differences in sex were looked for, but not found. Harigel ( 1994) found that males were likely to prefer either hand whereas females had a slight majority ofright-handers (though not enough more to be statistically significant). Kubota ( 1990) found that male monkeys did not show any significant preference for either hand whereas adult female monkeys had a greater frequency ofleft hand preference. It is unclear why the adult males of the Arashiyama West troop would be significantly different from the subjects studied in other research. It is certainly possible that it is the result of a dramatically different environment and/or related to some physiological process (possibly hormonal) or due to the small genetic pool from which this population is derived (150 animals, some related). It is also possible that the observed bias is the result of some type of arousal process. Future researchers might do well to investigate correlation of hand preference with dominance and states of arousal or activity. These types of emotional environmental indicators have been little studied, though Haringel ( 1994) has found preliminary evidence that such a relationship may exist in a captive environment. In the last decade researchers have begun to question earlier assumptions about hand preference. T rad.itionally, hand preference in nonhuman primates has been assessed by observing an individual eating. That is, the monkey picks up a food item and places it in its mouth. The number of times a monkey uses one hand in preference to the other is tallied and the monkey is assigned the label of either being ambidextrous or preferring either the right or left 41

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hand. My analysis has avoided categorizing the animals themselves as either left, right or ambidextrous, based upon a single bout (I 0-II 0 reaches), instead considering bouts of reaches on a continuum. This technique follows McGrew and Marchant ( I996) and allows detection of variations which might not be apparent using a simple trichotomy. Recently, McGrew and Marchant ( I996) added a new dimension to the issue of handedness, stating that there are five levels oflaterality. While I think that the word 'levels' in this context is a misstatement since they seem to be describing patterns ofbehavior, their framework is useful for the analysis of population level laterality. They state: Level I is the simplest, in which virtually all members of a population show no hand preferences, that is, when the norm for individuals is ambilaterality.... Level 2 is when a significant proportion of individuals are significantly lateralized to either side, but overall the distribution remains symmetrical. Level 3 is when a significant proportion of a population show not only laterality, but exclusive use of one hand or the other while still retaining synunetry. Through this level the overall distribution is still one ofhand preference, as there is no sign of skew to the left or right. Level4 is when the distribution oflateralized individual is asynunetrical; that is, there are significantly more right-than left-preferent members of a population or vice-versa. Finally, LevelS is Level 4 carried a step further, in which the distribution of exclusive users is asymmetrical, either biased to left or right. (McGrew and Marchant, I996:266) Although the use of the word level seems inappropriate, thinking of these as patterns is a useful framework for looking at laterality in groups. Using this method ofinterpretation, the Arashiyama West monkeys as a population showed only the first pattern oflaterality for simple reaching for grain. When adults are considered separately from young monkeys, the older monkeys approached the second pattern of hand preference. When adults are further subdivided by sex the male sub-population reached the second pattern oflaterality while the females, although somewhat skewed towards the second pattern, remained most closely described by the first pattern. Thus, the Arashiyama West monkey troop does not reach a 42

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population pattern of manual laterality that is significant when using this method of interpretation. The literature would lead one to expect mild left hand bias in at least some segments of the target population, and this study fulfills that expectation. Most literature on old world monkeys shows that monkeys have varying degrees ofhandedness at the individual level. ''We believe that most monkeys have some general tendency to use either the left or right hand which may become more apparent according to the situation and/or just by chance in continued examinations. However, these preferences are reflected as a matter of degree rather than exclusive right-or left -handedness" (Watanabe, 1993: 190). The monkeys at the Arashiyama West do show significant but nonexclusive hand biases at the individual leveL further supporting the conclusions ofWatanabe and others. This study highlights potentially fruitful directions for further research. It would be interesting to design tests that could be used to detect hand preference in the naturalistic experimentation is entirely missing in field studies oflaterality and could provide information about whether feral monkeys will display the same degree oflaterality recorded among captive primates. Further, gathering data which would correlate hand preference with dominance and arousal state may also prove illuminating. Finally, Rawlins (1989) and McGrew and Marchant (1992) conducted studies in which data on spontaneous hand use in free ranging primates (rhesus macaques and chimpanzees respectively) were collected and analyzed. This type of study would be especially interesting with Japanese macaques, since they show a fairly consistent level of hand preference across studies which measure simple reaching. 43

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50 l---2 30 20 3 10 -4 5 Appendix A 60 ----9 8 7 -6 The original Japanese system of numbering used a facial dot system and an inner thigh tattoo. The animal's number is written out on the inner tight thigh and then repeated in code on the animal's face. The location of the dot indicates a numerical value. The dots are then summed to find the tattoo number. Thus, an animal with a dot over each eye and under the left eye would be number 118. Numbers greater than 200 are indicated by placing two dots on the sites indicated. An animal with dot under his nose and two dots under the right eye would be 210. Each troop member has a unique name which consists of its mother's family name, the birth years of its matriline and the last two digits of its birth year. Thus Matsu 586374 is of the family Matsu, her grandmother was born in 1958, her mother was born in 1963, and she was born in 197 4. Many animals also receive a nickname such as Rocky ll, F atsu Matsu, or Kleenex. 44

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Appendix A (continued) This is a sample matriline chart from the Matsu matriline. Ma6069F Ma606978F #46 Maudie Mae. ___ #283 Cataract Ma60697883F Ma606986F #634 Magrite Ma6069788389M No tattoo Ma60697R85M #542 l\1a606987F No tattoo Ma6069788390M No tattoo Ma60697887F #835 Ma606990M No tattoo Ma6069788391F No tattoo Ma60697889M No tattoo #583 Ma60697891F #No tattoo If monkey number 283 was observed in the field, this chart could be used to learn that that monkey is named Cataract, that she is an adult female of the Matsu lineage who was born in 1978. This information in this appendix was taken from a worksheet given to me while conducting research. 45

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BIBLIOGRAPHY Altman, J. (1974). Observational study ofbehavior: Sampling methods. Behavior 49, 227-267. Anderson, JR., Degiorgio, C., Lamarque, C., and Fagot, J. (1996). A Multi-task assessment of hand lateralization in capuchin monkeys (Cebus ape /Ia). Primates 37(1), 97-103. Annett, M. ( 1985). Left, Right, Hand, and Brain: The right shift theory. Erlbalm, Hillsdale, N.J. Annett, M., and Annett, J. (1991). Handedness of eating in gorillas. Cortex 27, 269-275. Bard, K.A., Hopkins, W.D., and Fort, C.L. (1990). Lateral bias in infant chimpanzees (Pan troglodytes). J Comp. Psycho/. 104, 309-321. Bernstein, I.S. (1991). An empirical comparison offocal and ad libitum scoring with commentary on instantaneous scans, all occurrence and one-zero techniques. Anim. Behav. 42, 721-728. Bisazza, A., Cantalupo, C., Robins, A, Rogers, L.J., and Vallortigara, G. (1996). Right-pawedness in toads. Nature 3 79(65641 ), 408. Bisazza, A, Pignatti, R., and Vallortigara, G. (1997). Detour tests reveal task and stimulus specific neurallateraliztion in mosquito fish (Gambusia holbrooki). Behav. Brain Res (in press). Bisazza, A, Rogers, L.J., and Vallortigara, G. (in review). The origins of cerebral asymmetry: A review of evidence ofbehavioura1 and brain lateralization in fishes, reptiles, and amphibians. Neurosci. Biobehav. Rev. 46

PAGE 53

Bisazza, A, Cantalupo, C., Rogers, L.J., and Vallortigara, G. (in press). Lateral asymmetries during escape behaviour in a species of teleost fish (Jenynsia lineata). Physiol. Behav. Boesch, C. (1991). Handedness in wild chimpanzees. Int. J. Primatol. 12,541-558. Bradshaw, J., and Rogers, L. ( 1993). The evolution of lateral asymmetries, language, tool use, and imellect. Academic Press, San Diego. Bresard, B., and Bresson, F. (1987). Reaching or manipulation: Left or right? Behavioral Brain Sci. 10, 265-266. Bryden, M. (1982). Laterality: Functional asymmetry in the intact brain. Academic Press, New York. Byrne, R.W., and Byrne, J.M. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas. Cortex 27, 521-546. Cantalupo, C., Bisazza, A, and Vallortigara, G. ( 1995). Lateralization of predator evasion response in teleost fish (Girardinusfalcatus). Neurop5ychologia 33(12), 1637-1646. Chow, S.L. (1987). Meta-analysis of pragmatic and theoretical research: A critique. J. Psycho!. 121, 259-271. Cole, J. (1957). Laterality in the use ofthe hand, foot, and eye in monkeys. J. Camp. Physiol. Psycho!. 50, 296-299. Corballis, M.C. (1989). Laterality and human evolution. Psycho!. Rev. 96, 492-505. Corballis, M.C. (1991). The lopsided ape: Evolution of the generative mind. University Press, Oxford. Dimond, S., and Harris, R. (1984). Face touching in monkeys, apes, and man: Evolutionary origins and cerebral asymmetry. Neuropsychologia 22, 227-233. Dodson, D.L., Stafford, D., Forsythe, C., Seltzer, C.P., and Ward, J.P. (1992). Laterality in quadrupedal and bipedal prosimians: Reach and whole-body turn in the mouse lemur (Microcebus murinus) and the Galago (Galago moholi). Amer. J. Primal. 26, 191-202. 47

PAGE 54

Dreckel, A.W. (1995). Laterality of aggressive responses in Anolis. J Exp. Zoo!. 272, 194-200. Durden-Smith, J., and Desimone, D. (1983). Sex and the Brain. Arbor House, New York. Ettlinger, G. ( 1988). Hand preference, ability, and hemispheric specialization: In how far are these factors related in the monkey? Cortex 24, 389-398. Fedigan, L.M. (1991). History of the Arashiyama West Japanese macaques in Texas. In The Monkeys of Arashiyama: Thirty-five Years of Research in Japan and the West (pp. 54-73), Fedigan, L.M., and Asquith, P.J. (eds.). State University ofNew York Press, New York. Fagot, J., and Vauclair, 1. (1987). Spontaneous hand usage and handedness in a troop ofbaboons. Cortex 23, 265-274. Fagot, 1., and Vauclair, 1. (1988). Handedness and manual specialization in the baboon. Neuropsychologia 26, 795-804. Fagot, J,. and Vauclair, 1. (1991). Manual laterality in nonhuman primates: A distinction between handedness and manual specialization. Psychological Bulletin 109, 76-89. Falk, D. (1987). Brain lateralization in primates and its evolution in hominids. Yearbook Phys. Anthrop. 30, 107-125. Fleagle, J.G. (1988). Primate adaptation and evolution. Academic Press, New York Forrester, A., and Quiatt, D. ( 1994). Rhesus monkey hand preferences in lifting lids and reaching for food. In Current Primatology Vol. /1/: Behavioural Neuroscience, Physiology, and Reproduction (pp. 17-21 ). Anderson, J.R., Roeder, 1.1., Thierry, B., and Herrenschmidt, N. (eds.). University Louis Pasteur, Strasbourg. Forsythe, C., and Ward, J.P. (1988). Black lemur (Lemur macaco) hand preference in food reaching. Primates 29 (3), 369-374. 48

PAGE 55

Forsythe, C., Milliken, G.W., and Ward, J.P. (1988). Posturally related variations in the hand preferences ofthe ruffed lemur (Varencia variegata varigata). J. Camp. Psycho/. 102, 248-250. Fragaszy, D.M., and Mitchell, S.R. (1990). Hand preference and performance on unimanual and bimanual tasks in capuchin monkeys (Cebus apella). J. Camp. Psycho/. 104, 275-282, Galaburda, A.M., Lemay, M., Kemper, T.L., and Geschwind, N. (1978). Right-left asymmetries in the brain. Science 199, 852-856. Geschwind, N., and Behan, P. (1982). Left-handedness: association with immune disease, migraine, and developmental learning disorder. Proceedings of the National Academy of Sciences, USA 79, 5097-5100. Glick, S.D., and Shapiro, R.M. (1985). Functional and neurochemical mechanisms of cerebrallateralization in rats. In Cerebral Lateralization in Nonhuman Species (pp. 158-184), Glick, S.D. (ed.). Academic press, New York. Glick, S.D. (1993). Rotational behavior in children and adults. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries (pp. 307-317), Ward, J.P., and Hopkins, W.O. (eds.). Springer-Verlag, New York. Harigel, E.R. (1994). Hand preference injuvenile Japanese macaques (Macaca fuscata) as a function of sex, age, and rank. In Current Primato/ogy Vol. Ill: Behavioural Neuroscience, Physiology, and Reproduction (pp. 23-30). Anderson, J.R., Roeder, J.J., Thierry, B., and Herrenschmidt, N. (eds.). University Louis Pasteur, Strasbourg. Harris, L.J., and Carlson D.F. (1993). Hand preference for visually guided reaching in human infants and adults. In Primate Laterality: Current Behavioral Evidence of Primate (pp. 285-305), Ward, J.P., and Hopkins, W.O. (eds.). Springer Verlag, New York. Hatta, T., and Koikke, M., (1991 ). Left-hand preference in frightened mother monkeys in taking up their babies. Neuropsychologia 29, 207-209. Hewes, G.W. (1973). Primate communication and the gestural origin oflanguage. Curr. Anthrop. 14, 5-29. 49

PAGE 56

Holloway, R.L., and de Ia Coste-Lareymondie, M.C. (I982). Brain endocast asymmetry in pongids and hominids: Some preliminary findings on the paleontology of cerebral dominance. Am. J. Phys. Anthrop. 58, 10 I-II 0. Hopkins, W.D. (199I). Handedness and laterality in apes and monkeys. Primatology Today 27I-274 Hopkins, W.D., and Morris, R. (I989). Laterality for visual-spatial processing in two language trained chimpanzees (Pan troglodytes). Behav. Neurosci. I03, 227-239. Hopkins, W.D., Washburn, D.A., and Rumbaugh, D.M. (I989). Note on hand use in the manipulation of joysticks by rhesus monkeys (Macac.:a mulatta) and chimpanzees (Pan troglodytes). J. Camp. Psycho!. I03, 9I-94. Hopkins, W.D., Washburn, D.A., and Rumbaugh, D.M. (I990). Processing of form stimuli presented unilaterally in humans, chimpanzees (Pan troglodytes), and monkeys (Macaca mulatta). Behav. Neurosci. 104, 577-582 Hopkins, W.D., and de Waal, F.B. (1995). Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension. International .Journal of Primatology I6(2), 26I-276. lhobe, H. (I989). How social relationships influence a monkey's choice of feeding sites in the troop of Japanese macaques (Macacajuscata) in Kashima Islet. Primates 30(1), I7-25. ltakura, S. (I992). Task-specific hand preferences oftwo Japanese macaques on mirror -guided reaching. The Psychological Record 42, I73-I78. ltani, J. (I957). Personality of Japanese monkeys. Primates II, 29-33 (in Japanese, summary in Kubota, I990). Itani, J., Tokuda, K., Furuya, Y., Kano, K., and Shin, Y. (1963). The social construction of natural troops of Japanese monkeys in Takasakiyama. Primates 4, 242. Kawai, M. (I967). Catching behavior observed in the Kashima troop: A case of newly acquired behavior. Primates 8, I8I-I86. 50

PAGE 57

King, J.E., and Landau, V.I. (1993). Manual preference in varieties ofreaching in squirrel monkeys. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries (pp. 107-124), Ward, J.P., and Hopkins, W.D. (eds.). Springer-Verlag, New York. Kubota, K. ( 1990). Preferred hand use in the Japanese macaque troop, Arashiyama-R, during visually guided reaching for food pellets. Primates 31 (3), 393-406. MacNeilage, P.F. (1991). The "postural origins" theory ofprimate neurobiological asymmetries. In The Biological Foundations of Language Development (pp. 319341 ), Krasnegor, N., Rumbaugh, D. M., Studdert-Kennedy, M.G., and Schiefelbusch, T. (eds.). Academic Press, New York. MacNeilage, P.F. (1993). Implications of primate functional asymmetries for the evolution of cerebral hemispheric specializations. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries (pp. 319-341 ), Ward, J.P., and Hopkins, W.D. (eds.). Springer-Verlag, New York. MacNeilage, P.F., Studdert-Kennedy, M.G., and Lindblom, B. (1987). Primate handedness reconsidered. Behavioral and Brain Sciences 10, 247-303. Marchant, L.F., and McGrew, W.C. (1991). Laterality offunction in apes: A meta analysis of methods. J. Human Evol. 21, 425-438. Marchant, L.F., and McGrew, W.C. (1992). Laterality oflimb function in wild chimpanzees of Gombe National Park: Comprehensive study of spontaneous activities. J. Human Evol. 30, 427-443. Masataka, N. (1989). Population-level asymmetry ofhand preference in lemurs. Behavior 110, 245. Mason, A.M., Wolfe, L.D., and Johnson, J.C. (1995). Hand preference in the Sifaka (Propithecus verreauxi coquereli) during feeding in captivity. Primates 36(2), 275280. Matoba, M., Masataka, N., and Tanioka, Y. (1991). Cross-generational continuity of hand-use preferences in marmosets. Behavior 117(3-4), 281-286. McGrew, W.C., and Marchant, L.F. (1992). Chimpanzees, tools, and termites: Hand preference or handedness? Curr. Anthro. 33, 114-119. 51

PAGE 58

McGrew, W.C., and Marchant, L.F. (1994). Primate ethology: A perspective on human and nonhuman handedness. In Handbook of psychological anthropology (pp. 171-184), Bock, P.K. (ed.). Greenwood Press, Westport, CT. McGrew, W.C., and Marchant, L.F. (1996). Laterality of hand use in great apes. In Great Ape Societies (pp. 255-274), McGrew, W.C., Marchant, L.F., and Nishida, T. ( eds. ). University Press, Cambridge. Megirian, D., Weller, L., Martin, G.F., and Watson, C.R.R. (1977). Aspects of laterality in the marsupial Trichosurus vulpecula (brush tailed possum). Annals of the New York Academy of Sciences 299, 197-212 Milliken, G. W., Forsythe, C., and Ward, J.P. (1989). Multiple measures of hand-use lateralization in the ring tailed lemur (Lemur catta). J. Camp. Psycho/. 103, 262268. Morell, V. (1991). A hand on the bird and one in the bush. Science 254,33-34. Preilowski, B. (1993). Cerebral asymmetry, interhemispheric interaction and handedness: Second thoughts about comparative laterality research with nonhuman primates about a theory and some preliminary results. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries (pp. 125-148), Ward, J.P., and Hopkins, W.D. (eds.). Springer-Verlag, New York. Quiatt, D., Dudgeon, D., and Quiatt, S. (1991). Rhesus monkeys prefer right hand for lifting feeder bin lids. A mer. J. Phys. A nth, Supplement 13 (abstract only). Rawlins, R.G. (1993). Locomotive and manipulative use ofthe hand in the Cayo Santiago macaques (Macaca mulatta). In The primate hand(pp. 21-30), Preuschoft, H., and Chivers, D.J. (eds.). Springer-Verlag, New York. Rogers, L.J. (1989). Laterality in animals. Int. J. Camp. P!;}'chol. 3, 5-25. Seltzer, C., Forsythe, C., and Ward, J.P. (1990). Multiple measures of motor lateralization in human primates (Homo sapiens). J. Camp. Psycho/. 104, 159-166. Stafford, D.K., Milliken, G. W., and Ward, J.P. (1990). Lateral bias in feeding and brachiation in Hylobates. Primates 31 (3 ), 407-414. 52

PAGE 59

Takeda, S. (1994). Hand specialization in social grooming behavior in Japanese macaques (Macacafuscata). In Current Primatology Vol. Ill: Behavioural Neuroscience, Physiology, and Reproduction (pp. 31-55). Anderson, J.R., Roeder, J.J., Thierry, B., and Herrenschrnidt, N. (eds.). University Louis Pasteur, Strasbourg. Tan, U. (1987). Paw preference in dogs. International J. of Neuroscience 32, 325329. Tan, U., and Kutlu, N. (1991 ). The distribution of paw preference in right-, left-, and mixed-pawed male and female cats: The role of a female right-shift factor in handedness. International J. of Neuroscience 59,219-229. Tokuda, K. (1969). On the handedness of Japanese monkeys. Primates 10,41-46. Toth, N. (1985). Archaeological evidence for preferential right-handedness in the lower and middle Pleistocene and its possible implications. J. Hum. Evol. 14, 607614. Vallortigara, G., Regolin, L., Bortolomiol, G., and Tommasi, L. (1996). Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behavioural Brain Research 74, 135-143. Ward, J.P., Milliken, G.W., Dodson, D.L., Stafford, O.K., and Wallace, M. (1990). Handedness as a function of sex and age in a large population of lemur. J. Comp. 104, 167-173. Ward, J.P, Milliken, G. W., and Stafford, D.K.,( 1993). Patterns of lateralized behavior in prosimians. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries (pp. 43-74), Ward, J.P., and Hopkins, W.O. (eds.). Springer Verlag, New York. Warren, J.M. (1980). Handedness and laterality in human and other animals. Physiol. Psycho!. 8, 351-359. Watanabe, K., and Kawai, M. (1993). Lateralized hand use in the precultural behavior of the Koshima Monkeys (Macacafuscata) In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries (pp. 183-192), Ward, J.P., and Hopkins, W.O. (eds.). Springer-Verlag, New York. 53

PAGE 60

WeiJes, J.F. (1975). The anthropoid hand: A comparative study of prehension. In Contemporary Primatology (pp. 30-33), Kondo, S., Kawai, N., and Ebara, A (eds.). S. Karger, Basel. Welles, J.F. (1976). A comparative study of manual prehension in anthropoids. Saugetierkundliche Mitteilungen 24,26-37 Westergaard, G.C. (1991). Hand preference in the use and manufacture of tools by tufted capuchin (Cebus appella) and lion-tailed macaque (Macaca silenus) monkeys. J. Camp. Psycho/. 105, 172-176. Westergaard, G.C., and Suomi, S.J. (1993). Hand preference in capuchin monkeys varies with age. Primates 34(3), 295-299. Westergaard, G. C., and Suomi, S.J. (1996). Hand preference for stone artifact production and tool-use by monkeys: Possible implications for the evolution of right handedness in hominid.s. J. Camp. Psycho/. 30, 291-298. Yeni-Komshian, G.H., and Benson, D.A (1976). Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys. Science I 92, 387-389. 54