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Hand preference during unimanual and bimanual reaching actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana).

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American Journal of Primatology 70:500–504 (2008)
BRIEF REPORT
Hand Preference During Unimanual and Bimanual Reaching Actions in Sichuan
Snub-Nosed Monkeys (Rhinopithecus roxellana)
DA-PENG ZHAO1, WEI-HONG JI2, KUNIO WATANABE3, AND BAO-GUO LI1
1
College of Life Sciences, Northwest University, Xi’an, China
2
The Ecology and Conservation Group, Institute of Natural Resources, Massey University, Albany, Auckland, New Zealand
3
Field Research Center, Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
Hand preferences were investigated during one unimanual action (food-reaching) and one bimanual
action (mount-reaching) in a semi-free-ranging group of Sichuan snub-nosed monkeys (Rhinopithecus
roxellana) in Zhouzhi National Nature Reserve, Qinling Mountains of China. Nine of 14 individuals
tested on the unimanual food-reaching action and all six individuals tested on the bimanual mountreaching action exhibited a manual preference. Both significant right- and left-handed preferences were
observed in the two actions. Sex did not affect either direction or strength of hand preference in the
unimanual action. Hand preference for the bimanual action was stable over time, and the strength of
hand preference was significantly stronger in the bimanual action than in the unimanual action. Am. J.
c 2007 Wiley-Liss, Inc.
Primatol. 70:500–504, 2008.
Key words: Sichuan snub-nosed monkey (Rhinopithecus roxellana); hand preference; unimanual
food-reaching; bimanual mount-reaching
INTRODUCTION
Lateralized behavior has been studied as an
observable measure of cerebral functional asymmetry
for many years, and interest in the evolutionary
origins of lateralized behavior in humans has
prompted recent research into the study of manual
laterality in nonhuman primates [Bradshaw & Rogers, 1993; Porac & Coren, 1981]. Preference for
using one hand over the other has been studied in
a wide variety of primate species [see review,
Papademetriou et al., 2005]. The majority of studies
on lateralized hand use in Old World monkeys has
been conducted on cercopithecines [e.g. Blois-Heulin
et al., 2006; Harrison & Byrne, 2000; Hauser et al.,
1991; Tokuda, 1969; Warren et al., 1967; Watanabe &
Kawai, 1993]; much less is known about handedness
in colobines [e.g. Mittra et al., 1997; Neves &
Dolhinow, 1995; Wells, 2002]. Furthermore, although
captive settings offer a more controlled environment
for assessing hand preferences [e.g. Blois-Heulin
et al., 2006; Wells, 2002], studies of natural or semifree-ranging primate groups can provide further
important insights into the evolution of handedness.
This study of a colobine species, Rhinopithecus
roxellana, has three main aims. First, we explore the
laterality of manual function in unimanual foodreaching in a semi-free-ranging setting, consider the
influence of sex on hand preference, and compare
results with data on the same species in captivity.
Second, we investigate laterality during bimanual
r 2007 Wiley-Liss, Inc.
mount-reaching, i.e. an action in which the male
reaches with both hands from behind the solicited
female toward her hindquarters. Third, the degree of
hand preference shown in these two actions is
compared and discussed.
MATERIALS AND METHODS
Study Site and Species
The study site is located in Zhouzhi National
Nature Reserve (ZNNR) on the northern slopes of
the Qinling Mountains, China. The east ridge
troop and the west ridge troop of this species are
present in the study area [Zhao et al., 2008]. The
west ridge troop includes one all-male group
and our focal group, consisting of several one-male
units. A 15 30 m provisioning site is established at
Contract grant sponsor: Natural Science Foundation of China;
Contract grant number: 30770375; 30570312; 30630016; Contract grant sponsor: Cosmo Oil Eco Card Fund of Japan;
Contract grant number: 2005-2010; Contract grant sponsor:
Graduate Innovation Fund of Northwest University; Contract
grant numbers: 07YYB06.
Correspondence to: Baoguo Li, College of Life Sciences, Northwest University, Xi’an 710069, China.
E-mail: baoguoli@nwu.edu.cn
Received 9 May 2007; revised 30 October 2007; revision accepted
31 October 2007
DOI 10.1002/ajp.20509
Published online 13 December 2007 in Wiley InterScience (www.
interscience.wiley.com).
Hand Preference During Reaching Actions in R. roxellana / 501
Sanchakou (1,646 m above sea level), Gongnigou
valley (331480 6800 N, 1081160 1800 E), in ZNNR [Li &
Zhao, 2007]. The focal group was herded toward the
provisioning site where the research was conducted
at approximately 9:00 every day. Apples, radishes,
and corn were provided three times per day (10:00,
12:00, and 14:00). Approximately 200 g of feed were
provided per monkey per day. The data were
collected from a distance of between 0.5 and 50 m
from the target animal. All the monkeys have been
individually identified since 2001 based on their
prominent physical characteristics [Zhao et al., 2005,
2007]. During our observation period, we obtained
permission from ZNNR to conduct this research. Our
research complied strictly with animal care regulations and applicable national laws in China.
used binomial z-scores to determine whether the
frequency of left- or right-hand use exceeded that
expected by chance (50% right-hand use). A z-score
greater than 11.96 indicated significant left-handedness, whereas a z-score less than 1.96 indicates
a significant right-handedness. A z-score between
11.96 and 1.96 indicates no preference.
With respect to group-level handedness, we
performed Wilcoxon Signed ranks tests on the
paired percentages to evaluate whether this group
is ambipreferent or lateralized in hand use. Furthermore, sexual differences in manual laterality were
tested with a Mann–Whitney U-test and the strength
difference of hand preference (i.e. ABS-HI score)
with the paired samples test. All statistical tests
were two tailed and Po0.05 was chosen as the level
of significance.
Data Collection
Data were collected from July 8, 2003, to
January 17, 2004, with a video camera, by means of
focal animal behavioral sampling [Altmann, 1974;
Martin & Bateson, 1993]. Data on food-reaching and
mount-reaching were collected from 14 individuals
(nine adult males, five adult females) and six adult
males, respectively. Of these focal subjects, five adult
males were included in both food- and mountreaching observations. Hand preferences in the
unimanual reaching action were assessed by observing which hand was used first when reaching for
food (corn, or radish/apple pieces were scattered over
a wide area) in a quadrupedal posture. If the focal
animal sat in front of the food and repeatedly picked
it up without moving position, only the first reaching
action was recorded for hand preference. Hand
preferences in the bimanual reaching action were
assessed by observing which hand was extended first
when reaching for mounting, the second step of
copulation behavior as described in detail by Zhao
[2005] and Li and Zhao [2007]. Following the method
described by Fletcher [2006], the videotapes, totaling
5,786 min, were analyzed by two observers, using
careful cross-checking and obtaining complete agreement, to confirm the hand preference of each
individual performing each action.
Data Analysis
Hand preference for each focal individual
in each action was analyzed using two methods
described by Hopkins [1999]. First, to identify the
degree of individual lateral bias, we calculated
a handedness index (HI) for each animal by
subtracting the number of left-handed responses
(L) from the number of right-handed responses (R)
and dividing by the total number of responses, i.e.
HI 5 (RL)/(R1L). The HI varied between 1.0 and
1.0, indicating left and right hand bias, respectively.
The absolute value (ABS-HI) reflects the strength of
the individual-level hand preference. Second, we
RESULTS
Unimanual Food-reaching
A total of 1,314 unimanual food-reaching events
were recorded from 14 R. roxellana (nine adult males
and five adult females) for hand preference analysis
(mean 5 94, SE 5 32). On the basis of individual
z-scores, seven individuals were classified as lefthanded (50%), two as right-handed (14%), and five as
ambiguous-handed (36%) (Table I). There was no
hand preference for unimanual food-reaching at
group level in adult R.roxellana (z 5 1.852,
P 5 0.064, not significant).
The mean HI and ABS-HI scores in the unimanual reaching action were 0.22 (SD 5 0.35) and
0.33 (SD 5 0.24), respectively. No difference was
found for unimanual food-reaching action between
sexes, either in direction of hand preference (U 5 20;
N1 5 9; N2 5 5; P 5 0.739; the mean HI score per
subject was 0.26, SD 5 0.27 for males and 0.14,
SD 5 0.48 for females), or in the strength of hand
preference (U 5 18; N1 5 9; N2 5 5; P 5 0.549; the
mean ABS-HI score per subject was 0.30, SE 5 0.22
for males and 0.38, SE 5 0.28 for females).
Bimanual Mount Reaching
We recorded a total of 497 bimanual mountreaching events from six male individuals for hand
preference analysis in R. roxellana (mean 5 83,
SE 5 13). The mean HI and ABS-HI scores for all
focal animals in the bimanual reaching action were
0.28 (SD 5 0.65) and 0.64 (SD 5 0.11), respectively.
All subjects exhibited significant individual-level
hand preference during mount-reaching based on
the z-scores. Four animals showed a left-hand
preference and the remainder showed a right-hand
preference at the individual level (Table I). No
group-level preference for mount reaching was
found in male R. roxellana (z 5 1.363, P 5 0.173,
not significant). For testing whether individual
Am. J. Primatol.
502 / Zhao et al.
TABLE I. Lateralized Hand Use During Unimanual and Bimanual Reaching Actions in Rhinopithecus roxellana
The unimanual reaching action
No. Animal ID Animal gender
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
BZT
CM
DB
HR
JB
JT
JZT
LP
PK
XN
BT
HTP
XC
YL
YZM
Male
Male
Male
Male
Male
Male
Male
Male
Male
Male
Female
Female
Female
Female
Female
L
R
HI
343 132 0.44
31 32
0.02
49 39 0.11
55 35 0.22
53 28 0.31
29
4 0.76
27 16 0.26
85 113
0.14
— —
—
33 13 0.43
62 22 0.48
6 22
0.57
20
4 0.67
15 16
0.03
17 13 0.13
The bimanual reaching action
ABS-HI z-score Preference L
0.44
0.02
0.11
0.22
0.31
0.76
0.26
0.14
—
0.43
0.48
0.57
0.67
0.03
0.13
9.59
0.16
1.03
2.09
2.79
4.37
1.70
1.98
—
2.91
4.40
3.02
3.28
0.17
0.71
Left
Ambi
Ambi
Left
Left
Left
Ambi
Right
—
Left
Left
Right
Left
Ambi
Ambi
58
—
82
—
79
—
75
34
5
—
—
—
—
—
—
R
HI
14
—
15
—
10
—
13
89
23
—
—
—
—
—
—
0.61
—
0.69
—
0.78
—
0.70
0.47
0.64
—
—
—
—
—
—
ABS-HI z-score Preference
0.61
—
0.69
—
0.78
—
0.70
0.47
0.64
—
—
—
—
—
—
5.18
—
6.80
—
7.36
—
6.57
5.21
3.39
—
—
—
—
—
—
Left
—
Left
—
Left
—
Left
Right
Right
—
—
—
—
—
—
L, left-handed responses; R, right-handed responses; HI 5 (#R#L)/(#R1#L); ABS-HI, absolute value.
preferences are consistent across time, we calculated
the Pearson correlation coefficient between HI scores
in the first and second halves of the observation
period. There was a significant positive correlation
(r 5 0.771, P 5 0.072), meaning that hand preferences in this bimanual reaching action were stable
over time in this species.
Among those five subjects tested on both the
unimanual and bimanual actions, all displayed the
same direction of hand preference according to the
HI score. The HI scores for the unimanual action
(mean 5 0.18, SE 5 0.20) were not significantly
different from the HI scores for the bimanual action
(mean 5 0.46, SE 5 0.52) (t(4) 5 1.754, P 5 0.154).
Three exhibited the same hand preference based on
the z-score; the other two moved from ambiguous
(slightly, but not significantly, left-handed) in the
unimanual action to significantly left-handed in the
bimanual action based on the z-score. Manual
preference strength (i.e. the ABS-HI score) of these
five individuals was significantly greater in the
bimanual action (mean ABS-HI 5 0.65, SD 5 0.12)
than the unimanual action (mean ABS-HI 5 0.23,
SD 5 0.11) (t(4) 5 7.464, P 5 0.002).
DISCUSSION
To our knowledge, this is the first study of
hand preference in both unimanual and bimanual
reaching actions in Sichuan snub-nosed monkeys.
Our results suggest that hand preference during
unimanual food-reaching and bimanual mountreaching in R. roxellana is specific to the individual
rather than the group. Sex did not affect the
direction or strength of hand preference in the
unimanual action. These results agree with earlier
studies of handedness in other colobines [e.g.
Am. J. Primatol.
Harrison & Byrne, 2000; Mittra et al., 1997; Neves
& Dolhinow, 1995; Warren et al., 1967; Wells, 2002]
and some great apes [e.g. Rogers & Kaplan, 1996].
Under the lateralization model of McGrew and
Marchant [1997] on the presence, strength, and
direction of lateralized primate hand use, we classify
R. roxellana into level 2.
For the unimanual reaching action, our results
differed from those of earlier captive studies which
showed that male monkeys exhibit only right-hand
preference at the individual level [Liang & Zhang,
1998; Ma et al., 1988]. The discrepancy in the results
may be related to two differences in methodology
between the studies. First, the settings are different:
it has been shown that housing conditions and
environmental stress may influence manual laterality in primates [e.g. MacNeilage et al., 1987].
Second, different statistical procedures may influence results. In our study, z-scores were used,
whereas in others, P-values [Ma et al., 1988] and w2
values [Liang & Zhang, 1998] were used. A combination of differences in study environments and
methods used to analyze hand preferences may
partly account for the discrepant results between
our study and some earlier ones.
Studies on arboreal primates are crucial for
understanding the role of posture and postural
instability on handedness. This notion is central to
the postural origin hypothesis proposed by MacNeilage et al. [1987] and MacNeilage [1991] that
arboreal primates should preferentially use their left
hand for manual actions like grasping food; such a
postural effect is observable both in prosimians and
in Old World monkeys [Papademetriou et al., 2005].
Although only half of the individuals in our study
were significantly left-handed according to the
z-score value, based on the HI, 71% of focal
Hand Preference During Reaching Actions in R. roxellana / 503
R. roxellana showed a trend for left-hand preference
during unimanual food-reaching action; this
is in partial agreement with the postural origin
hypothesis. Even though the bimanual reaching
action did not reveal a group-level preference
for one hand, all subjects tested displayed manual
laterality at the individual level, and hand preferences were stable over time. Furthermore, we found
stronger hand preferences for this action compared
to unimanual reaching. This reflects the postural
effect on hand preference during reaching actions
in R. roxellana, also found in other primates
[Bradshaw & Rogers, 1993; Frost, 1980; Westergaard
et al., 1998].
In conclusion, although the size of our sample
does not allow us to make strong generalizations
concerning lateral preferences in Sichuan snubnosed monkeys, the R. roxellana studied appeared
lateralized in unimanual and bimanual actions.
Furthermore, hand preferences were stronger
for a bimanual action than a unimanual action,
supporting the view that posture could be a crucial
factor influencing manual laterality in this species.
It should be noted that the behaviors studied
here, although performed by an arboreal species,
took place on the ground. Future research should
focus on the arboreal behaviors to reach further
and more robust conclusions about the laterality
of this species.
ACKNOWLEDGMENTS
Cordial thanks to Dr. William D. Hopkins and
Prof. Colin Groves for their helpful comments on
an earlier version of this study. Prof. Lesley Rogers,
Dr. Susan G. Larson, Dr. Hélène Meunier and
Dr. George F. Michel who kindly supplied relevant
references. The constructive comments of Editor
James R. Anderson and two anonymous reviewers
are greatly appreciated. Dapeng Zhao expresses his
special thank to Miss Yisha Ha.
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