Handedness in Nature: First Evidence on Manual Laterality on Bimanual Coordinated Tube Task in Wild Primates

Abstract

Handedness is a defining feature of human manual skill and understanding the origin of manual specialization remains a central topic of inquiry in anthropology and other sciences. In this study, we examined hand preference in a sample of wild primates on a task that requires bimanual coordinated actions (tube task) that has been widely used in captive primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an arboreal Old World monkey species that is endemic to China, and 24 adult individuals from the Qinling Mountains of China were included for the analysis of hand preference in the tube task. All subjects showed strong individual hand preferences and significant group-level left-handedness was found. There were no significant differences between males and females for either direction or strength of hand preference. Strength of hand preferences of adults was significantly greater than juveniles. Use of the index finger to extract the food was the dominant extractive-act. Our findings represent the first evidence of population-level left-handedness in wild Old World monkeys, and broaden our knowledge on evaluating primate hand preference via experimental manipulation in natural conditions.

Approximately 90% of humans are right-handed (Porac and Coren, 1981; Annett, 2002). Such an overwhelming right-hand preference at the population level is generally considered a unique evolutionary characteristic of human beings across a variety of cultures and many believe it is associated with the evolution of left cerebral lateralization for manual control and language (Porac and Coren, 1981; Corballis, 1983; Marchant and McGrew, 1998; Corballis, 2002; Raymond and Pontier, 2004). Research on hand preference in nonhuman primates brings essential light to evolutionary origins of human cerebral lateralization and its adaptive value (Fagot and Vauclair, 1991; Bradshaw and Rogers, 1993; Annett, 2002; Vallortigara and Bisazza, 2002; Cashmore et al., 2008). Though evidence of group-level limb biases is weak in nonhuman animals, including primates, there is increasing evidence of population-level handedness in some primate species (e.g., Byrne and Byrne, 1991; see review by Ward and Hopkins, 1993; Rogers and Andrew, 2002; Vallortigara and Rogers, 2005; Hopkins, 2007a).

There are two continuing issues in the comparative assessment of primate hand preference that require further study. One issue is the matter of methodological inconsistencies across studies. In other words, various tasks are used to assess hand use of nonhuman primates. Most studies on hand preference in wild and captive primates have used relatively simple measures of hand use such as simple reaching (Lehman, 1993; Papademetriou et al., 2005). It is becoming increasingly clear that unimanual tasks, such as simple reaching, may not be the most sensitive for eliciting consistent preferential hand use compared to tasks that require coordinated bimanual actions (Byrne and Byrne, 1991; Vauclair et al., 2005; Hopkins, 2007b). The task complexity theory proposes that strong preferences and group-level biases of manual laterality would be more likely to appear in complex tasks, such as bimanual coordinated tasks compared to less demanding, unimanual tasks (Fagot and Vauclair, 1991). Studies in a number of primate species have provided evidence in support of the task complexity view of primate hand preference (Cebus apella: Westergaard and Suomi, 1996; Spinozzi et al., 1998; Lilak and Phillips, 2008; Cercocebus torquatus: Blois-Heulin et al., 2006; Laurence et al. 2011; Cercopithecus c. campbelli: Chapelain et al. 2006; Cercopithecus neglectus: Trouillard and Blois-Heulin, 2005; Schweitzer et al. 2007; Chlorocebus aethiops: Harrison and Byrne, 2000; Gorilla gorilla: Byrne and Byrne, 1991; Pan troglodytes: Colell et al., 1995; Rhinopithecus roxellana: Zhao et al. 2010).

Moreover, increasingly, studies are now investigating manual laterality for bimanual coordinated actions in different contexts such as spontaneous or natural behaviors (e.g., bimanual feeding: Hopkins, 1994; Meguerditchian et al., 2010; bimanual grooming: Hopkins et al., 2007; Zhao et al., 2010; bimanual stone handling: Leca et al., 2010) or using experimental tasks (e.g., tube task: Hopkins, 1995; Westergaard and Suomi, 1996; Vauclair et al., 2005; ball task: Schweitzer et al., 2007; box task: Blois-Heulin et al., 2006). It is generally believed that experimental tasks elicit a greater strength of manual laterality than spontaneous tasks (e.g., Cercopithecus campbelli: Chapelain et al., 2006; Cercopithecus neglectus: Schweitzer et al., 2007). Therefore, considering that the diversity of tasks could cause potential inconsistency of results, choosing more standardized measure of hand use that can be used across different settings is crucial to reliably assess and compare hand preference in nonhuman primate species.

The second critical issue on the comparative assessment of hand preference is the imbalance of data between captive and wild populations of nonhuman primates. The majority of studies on hand preference in nonhuman primates have been conducted in captive living individuals (e.g., Fagot and Vauclair, 1991; Marchant and McGrew, 1991; Hopkins et al., 2011) and some have suggested that being raised by humans during infancy, captive housing conditions and environmental stress may, in essence, influence manual laterality in primates (McGrew and Marchant, 1997, 2001; Palmer, 2003). Since the initial report of population-level handedness in mountain gorillas for bimanual feeding by Byrne and Byrne (1991), there is growing body of evidence reporting population-level handedness in wild nonhuman primates, notably apes (Boesch, 1991; Corp and Byrne, 2004; Lonsdorf and Hopkins, 2005; Peters and Rogers, 2007; Humle and Matsuzawa, 2009). However, in contrast, there are very few studies reporting handedness in wild populations of monkeys (Panger, 1998; Garber et al., 2008; Zhao et al., 2010). Further complicating this issue is the fact that most studies on hand preference in wild primates use different measures (e.g., nut-cracking: Humle and Matsuzawa, 2009; manipulating a dowel: Garber et al. 2008; stone handling: Leca et al., 2010; termite-fishing: Lonsdorf and Hopkins, 2005) than those employed by scientists working in captive settings, though again, this is beginning to change (e.g., simple reaching: Lilak and Phillips, 2008; bimanual feeding: Hopkins, 1994; Meguerditchian et al. 2010; grooming: Hopkins et al., 2007; tool-use: Hopkins et al., 2009). This makes comparing findings between the two settings very difficult if not impossible.

Hopkins (1995) first introduced “the tube task”, an experimental task that assesses hand use for coordinated bimanual actions. In the tube task, the primate needs to hold a baited tube with one hand and extract the food inside the tube with a finger on the opposite hand (Hopkins, 1995). In contrast to other common measures of hand use, the tube task is a kind of complex task involving bimanual coordination (Hopkins, 1995). The tube task elicits consistent and reliable hand preference at the individual level because it removes the potential influence of situational factors that might influence hand use (Hopkins and Cantalupo, 2005). Moreover, it is relatively simple to administer and therefore can be used with many different primate species. Therefore the tube task is ideally suited as a standard measure of hand preference.

To date, the tube task has been used with a number of primate species including great apes (Gorilla gorilla: Hopkins et al., 2003a; Begg-Reid and Schillaci, 2008; Hopkins et al., 2011; Pan paniscus: Chapelain and Hogervorst, 2009; Chapelain et al., 2011; Pan troglodytes: Hopkins, 1995; Hopkins, 1999a; Hopkins et al., 2001; Hopkins et al., 2003a,b; Hopkins and Cantalupo, 2003; Hopkins et al., 2004; Hopkins et al., 2005; Llorente et al., 2009; Llorente et al., 2011; Pongo pygmaeus: Hopkins et al., 2003a), Old World monkeys (Cercopithecus neglectus: Schweitzer et al., 2007; Macaca mulatta: Westergaard and Suomi, 1996; Westergaard et al., 1997; Papio anubis: Vauclair et al., 2005) as well as New World monkeys (Cebus apella: Westergaard and Suomi, 1996; Spinozzi et al., 1998; Phillips and Sherwood 2005; Spinozzi et al., 2007; Lilak and Phillips 2008; Cebus capucinus: Meunier and Vauclair, 2007). The group-level handedness has been reported in seven nonhuman primates species to date (right-handedness: Cebus apella: Spinozzi et al., 1998; Gorillas gorilla: Hopkins et al., 2011; Pan troglodytes: Hopkins, 1995, 1999a; Hopkins et al., 2001, 2003a,b; 2004, 2005; Llorente et al., 2009, 2011; Hopkins et al., 2011; Papio anubis: Vauclair et al., 2005; left-handedness: Cercopithecus neglectus: Schweitzer et al., 2007; Macaca mulatta: Westergaard et al., 1997, Bennet et al., 2008; Pongo pygmaeus: Hopkins et al., 2003a; Hopkins et al., 2011).

One limitation of these studies is that all research on the tube task has been conducted in captive- or semi-naturally living primates (see review by Chapelain and Hogervorst, 2009). Though such settings can offer a more controlled environment for assessing limb preferences in non-human primates, studies of wild or naturalistic populations can potentially provide important insights into how manual laterality is potentially influenced by natural environmental conditions (Hopkins, 2007a). To address this issue, we examined hand preferences for the tube task in a sample of wild primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an arboreal Old World monkey species that is endemic to China, and has, until recently, rarely been studied in laterality research (Zhao et al., 2008a,b,c, Zhao et al., 2010). With regard to bimanual coordination, there are no data to date on the experimental tube task but there is one report on spontaneous bimanual grooming that reported group-level left-handedness in wild R. roxellana (Zhao et al., 2010).

There were three main aims of this study in wild R. roxellana. First, we sought to examine whether wild R. roxellana would show population-level handedness for the tube task. Based on the previous report of group-level left handedness for bimanual grooming in this species (Zhao et al. 2010), we hypothesized that left hand biases would similarly be evident for the tube task.

Second, we aimed to test another prediction that hand preference for the experimental tube task were more biased than that for spontaneous bimanual grooming task based on the hypothetic statement mentioned above, “experimental tasks elicit a greater strength of manual laterality than spontaneous tasks (Chapelain et al., 2006; Schweitzer et al., 2007)”. Third, we aimed to compare the tube task results in this species with previous data from other species on the tube task in order to make an integrated assessment of primate hand preference for bimanual coordinated actions and discuss their differences and similarities from a broad comparative primate perspective.

METHODS

Study site and study species

This study was conducted at the Zhouzhi National Nature Reserve (ZNNR) on the northern slope of the Qinling Mountains, in the Shaanxi province of China. There were two troops of Sichuan snub-nosed monkeys, the East Ridge troop (ERT) and the West Ridge troop (WRT), at the study site. The focal population consists of one-male groups within the WRT, as described in detail by Zhao et al. (2010). Permission of the Zhouzhi National Nature Reserve to conduct this research was obtained before the onset of the study.

We set up one provisioning site at Sanchakou (1646 m above sea level) in Gongnigou valley (33°48′68″N, 108°16′18″E). The field assistants searched for monkeys of the focal population and attracted them to the provisioning site at approximately 9:00 a.m. every day when research was being conducted. Approximately 200g of feed were provided per monkey per day on three occasions (10:00 a.m., 12:00 p.m., and 14:00 p.m. respectively). Compared with the daily total diet of R. roxellana, the energy intake of provisioned food is very limited and thus its influence on their natural behavior was minimal. On the whole, the focal group was well-habituated to the presence of observers and had many years of experience as subjects in other naturalistic observational studies. We identified all focal individuals via their physical characteristics and kept a distance of 5–50m from the focal animals during observations.

Data collection

We collected data from September 2010 to January 2011 based on a comprehensive study on asymmetry of limb use in R. roxellana (Zhao et al., 2008a,b,c; Zhao et al., 2010). Following the method described by Hopkins (1995), an opaque polyvinyl-chloride (PVC) tube was used in the assessment of hand preferences (Fig.1). In this study, the (PVC) tube was 3 cm in diameter and 10 cm in length. Honey mixed with corn kernels were smeared inside, approximately 2 cm from both ends of the tube. Four PVC tubes were placed on the ground simultaneously so as to minimize individual competition during each test.

Fig. 1.

An adult female R. roxellana performing the tube task on a branch (A color version of this figure may be viewed in the online issue, which is available at http://onlinelibrary.wiley.com/.)

We initially chose some individuals as focal subjects only because they performed the tube task on one's own initiative at the earlier stage of the test. If multiple individuals performed the tube task at the same time, we selected the individual with the nearest visible distance from the observer. If more than one individual were the same visible distance from the observer, we selected the individual who had the fewest number of responses. Every effort was made to balance the sampling responses among all subjects, although some of them performed many more responses than others. During our observation, most of data were recorded when monkeys performed the tube task on the ground. Occasionally some subjects took the tube, departed from the place where the tube was placed on, climbed a tree nearby, and then performed the tube task on a branch. All subjects kept the posture of squat when they performed the tube task, either on the ground or on a branch.

We recorded both the frequency and bouts in hand use in the present study. For the frequency in hand use, as described by Hopkins (1995) and Hopkins et al. (2011), we recorded the finger and hand use each time the subject inserted its finger(s) of one hand into the PVC tube and brought corn kernels with honey to its mouth (Fig. 1). The hand used to extract the food was considered as the dominant hand. Data were collected until the subject either dropped the tube or stopped extracting corn kernels for at least 10 seconds. For recording bouts in hand use, as described by Hopkins et al. (2001) and Chapelain and Hogervorst (2009), we defined one bout as each sequence of identical actions and recorded only the first extraction of such sequences. The identification of dominant hand was as same as the frequency recording technology. The new bout in hand use was noted when the subject either dropped the tube, changed the hand grasping the tube, held the tube with both hands or moved to another area to continue feeding. In addition, the digit used (thumb, index finger, middle finger, ring finger, little finger) to extract the food from the tube each time was also recorded. Feeding attempts while using the feet to hold the tube were not considered as responses, based on the method described by Meunier and Vauclair (2007). In order to assess consistency of hand preference on this experimental task, we divided the whole observation period into two periods (the first period: 20 September to 12 November 2010, the second period: 15 November 2010 to January 10 2010). Individuals who performed the tube task a minimum of 15 responses, based on frequency in hand use at each observation period, were included in the analysis of consistency in hand use. A minimum of 30 responses (frequency) was obtained from each subject.

Data analysis

Individual hand preferences were characterized using two methods (Hopkins, 1999b). First, to identify the degree of individual lateral bias, the handedness index (HI), one commonly used index, was calculated for each focal subject following the formula: (right-hand use − left-hand use) / (right-hand use + left-hand use) (Hopkins, 1999b). The HI varied between −1.0 and 1.0. Positive values indicate a bias toward right hand use and negative values indicate a bias toward left hand use. The absolute value (ABS-HI) reflects the strength of the individual-level hand preference. Secondly, z-scores were calculated based on the frequency of right and left hand use. The subjects were then categorized as right-handed (z ≥ 1.96), left-handed (z ≤ −1.96), or ambipreferent (1.96 > z > −1.96) based on their individual score. Group-level hand preference was analyzed via one-sample tests with individual HI scores and chi-square tests of independence (Hopkins, 1999b, Hopkins et al., 2011).

We used the Spearman correlation test to evaluate the relationship between the number of data points per subject and the HI and ABS-HI as well as the relationship between the HI and ABS-HI when calculated on the basis of bouts and frequencies. We used the Mann-Whitney U-test to evaluate sex/age/task differences in manual laterality. We adopted the Pearson correlation coefficient test to evaluate whether individual preferences were consistent across our two observation periods. Finally, we used analysis of variance (ANOVA) to evaluate the difference of digit use within subjects (Spinozzi et al., 2007). SPSS 16.0 was used to conduct the analyses and a two-tailed test with a level of significance of p ≤ 0.05 was adopted for all analyses.

RESULTS

Observations in hand use for the tube task were obtained in twenty-four individuals including 8 males and 16 females. The individual data on left and right hand use are shown in Table 1 and Table 2. For frequency in hand use, the mean number of data points per subject was 62.42 ± 5.74 (range: 31–144) and the mean HI and ABS-HI scores were −0.32 ± 0.15 (range: −1.00-0.97) and 0.73 ± 0.05 (range: 0.27–1.00) respectively. For bouts of hand use, the mean number of data points per subject was 15.21 ± 1.14 (range: 8–30) and the mean HI and ABS-HI scores were −0.31 ± 0.14 (range: −1.00-0.88) and 0.67 ± 0.05 (range: 0.20–1.00) respectively.

Table 1.

Frequency data on hand preference for the tube task in wild R. roxellana

No	Animal ID	Age class	Gender	L1	R2	Percentage3	HI	ABS-HI
1	bbe	Adult	male	23	47	67.14	0.34	0.34
2	bb-j140	Juvenile	female	28	13	68.29	−0.37	0.37
3	bb-j40	Juvenile	female	33	13	71.74	−0.43	0.43
4	bzt-j250	Juvenile	female	14	27	65.85	0.32	0.32
5	eq	Adult	male	39	0	100.00	−1.00	1.00
6	ff	Adult	female	129	2	98.47	−0.97	0.97
7	fg-j30	Juvenile	female	118	26	81.94	−0.64	0.64
8	fhtp	Adult	female	27	4	87.10	−0.74	0.74
9	fp-j20	Juvenile	female	43	12	78.18	−0.56	0.56
10	hm-3	Juvenile	female	23	10	69.70	−0.39	0.39
11	hto	Adult	male	66	3	95.65	−0.91	0.91
12	huj-4	Juvenile	male	47	27	63.51	−0.27	0.27
13	jba	Adult	male	65	0	100.00	−1.00	1.00
14	jb-j20	Juvenile	female	54	4	93.10	−0.86	0.86
15	jdi	Adult	female	10	43	81.13	0.62	0.62
16	jgu	Adult	female	82	0	100.00	−1.00	1.00
17	lm-3	Juvenile	male	6	80	93.02	0.86	0.86
18	rx-j30	Juvenile	female	36	0	100.00	−1.00	1.00
19	rx-j41	Juvenile	male	34	5	87.18	−0.74	0.74
20	sd	Adult	female	66	12	84.62	−0.69	0.69
21	thu	Adult	female	2	56	96.55	0.93	0.93
22	wxf2	Adult	female	3	46	93.88	0.88	0.88
23	xh	Adult	male	1	69	98.57	0.97	0.97
24	yli	Adult	female	50	0	100.00	−1.00	1.00

¹L: The number of responses made with the left hand

²R: The number of responses made with the right hand

³Percentage: The percentage of use of the preferred hand

Table 2.

Bout data on hand preference for the tube task in wild R. roxellana

No	Animal ID	Age class	Gender	L1	R2	Percentage3	HI	ABS-HI	z-score	Category4
1	bbe	Adult	male	5	10	66.67	0.33	0.33	1.29	Ambiguous-handed
2	bb-j140	Juvenile	female	11	3	78.57	−0.57	0.57	−2.14	Left-handed
3	bb-j40	Juvenile	female	8	4	66.67	−0.33	0.33	−1.15	Ambiguous-handed
4	bzt-j250	Juvenile	female	4	6	60.00	0.20	0.20	0.63	Ambiguous-handed
5	eq	Adult	male	8	0	100.00	−1.00	1.00	−2.83	Left-handed
6	ff	Adult	female	25	1	96.15	−0.92	0.92	−4.71	Left-handed
7	fg-j30	Juvenile	female	25	5	83.33	−0.67	0.67	−3.65	Left-handed
8	fhtp	Adult	female	7	1	87.50	−0.75	0.75	−2.12	Left-handed
9	fp-j20	Juvenile	female	14	5	73.68	−0.47	0.47	−2.06	Left-handed
10	hm-3	Juvenile	female	9	4	69.23	−0.38	0.38	−1.39	Ambiguous-handed
11	hto	Adult	male	11	2	84.62	−0.69	0.69	−2.50	Left-handed
12	huj-4	Juvenile	male	11	7	61.11	−0.22	0.22	−0.94	Ambiguous-handed
13	jba	Adult	male	16	0	100.00	−1.00	1.00	−4.00	Left-handed
14	jb-j20	Juvenile	female	14	2	88.00	−0.75	0.75	−3.00	Left-handed
15	jdi	Adult	female	3	8	73.00	0.45	0.45	1.51	Ambiguous-handed
16	jgu	Adult	female	18	0	100.00	−1.00	1.00	−4.24	Left-handed
17	lm-3	Juvenile	male	2	22	92.00	0.83	0.83	4.08	Right-handed
18	rx-j30	Juvenile	female	8	0	100.00	−1.00	1.00	−2.83	Left-handed
19	rx-j41	Juvenile	male	7	2	78.00	−0.56	0.56	−1.67	Ambiguous-handed
20	sd	Adult	female	12	4	75.00	−0.50	0.50	−2.00	Left-handed
21	thu	Adult	female	2	15	88.00	0.76	0.76	3.15	Right-handed
22	wxf2	Adult	female	1	12	92.00	0.85	0.85	3.05	Right-handed
23	xh	Adult	male	1	16	94.00	0.88	0.88	3.64	Right-handed
24	yli	Adult	female	14	0	100.00	−1.00	1.00	−3.74	Left-handed

¹L: The number of responses made with the left hand

²R: The number of responses made with the right hand

³Percentage: The percentage of use of the preferred hand

⁴Category of hand preference based on the index of the z-score

The number of observations per individual was not significantly correlated with the HI values for frequency (r = 0.099 p = 0.644) or bouts (r = 0.084, p = 0.695) in hand use. Similarly, the number of observations was not significantly associated with the ABS-HI scores when calculated on the basis of frequency (r = 0.084, p = 0.697) or bouts (r = 0.104, p = 0.628) in hand use. Thus, as has been reported in many other studies, individual differences in the total number of responses did not skew the distribution of handedness values.

Data consistency

There was a significant positive correlation between the HI score of bouts and that of frequencies (r = 0.991, p < 0.001), as well as between the ABS-HI score of bouts and that of frequencies (r = 0.938, p < 0.001). This indicates that handedness indices based on bouts and frequencies are sensitive to the same degree of lateral bias in hand use, a finding consistent with many other studies (e.g., Hopkins et al. 2001). Fifteen individuals met the criterion of having at least 15 frequency responses at each observation period in hand use and there was a significant positive correlation (frequency: r = 0.986, p < 0.001; bout: r = 0.959, p < 0.001) between HI scores in the two halves of our observation period. In short, individual hand preferences were stable over the observational time periods.

Individual and group-level hand preference

Based on the sign of the HI scores when calculated on the basis of frequency and bouts of hand use, there were 17 left-handed (70.83%) and 7 right-handed (29.71%) individuals (see Table 1, 2). One sample t-tests (frequency: t₂₃ = −2.177, p = 0.040; bout: t₂₃ = −2.317, p = 0.030) as well as a chi-square goodness-of-fit test (both frequency and bout: X²_{(1, N = 24)} = 4.167, p = 0.041) revealed a significant group-level left-hand preferences for the tube task. When using z scores as the index for hand preference classification, there were 13 left-handed (54.17%), 4 right-handed (16.67%) and 7 ambiguous handed (29.16%) individuals for the bout data (Table 2). A chi-square goodness-of-fit test showed that there was significantly more left-handed individuals than right-handed individuals for the bout data (X²_{(1, N = 17)} = 4.765, p = 0.029).

Digit use

Generally there are five extractive-act categories involved in the tube task. We performed an analysis of variance (ANOVA) on the percentages of responses of each category for each individual, and found a significant difference across categories (F_{[4, 115]} = 148.414, p<0.001). The mean percentage for each extractive act were 80.29 ± 4.16% (mean ± SE) with the index digit, 11.70 ± 4.12% with the thumb, 6.20 ± 1.82% with the index + the thumb, 1.79 ± 1.14% with the index + the middle, and 0.03 ± 0.03% with others. A post-hoc analysis using the least significant difference test revealed a significantly higher percentage of responses made with the index finger compared to all other extractive-act categories (all p<0.001).

Age and sex effects

We found no significant difference between adults and juveniles in the direction of hand preference (frequency: U = 62.50; N₁ = 13; N₂ = 11; p = 0.600; the mean HI score per subject was −0.27, SE = 0.24 for adults and −0.37, SE = 0.17 for juveniles; bout: U = 63.50; N₁ = 13; N₂ = 11; p = 0.641; the mean HI score per subject was −0.28, SE = 0.22 for adults and −0.36, SE = 0.15 for juveniles). However, we found the strength of manual laterality in adults was significantly higher than that in juveniles (frequency: U = 28.50; N₁ = 13; N₂ = 11; p = 0.012; the mean ABS-HI score per subject was 0.85, SE = 0.06 for adults and 0.59, SE = 0.08 for juveniles; bout: U = 34.00; N₁ = 13; N₂ = 11; p = 0.029; the mean ABS-HI score per subject was 0.78, SE = 0.06 for adults and 0.44, SE = 0.13 for juveniles) (Fig.2). Thus, adults showed stronger hand preferences than juveniles.

Fig. 2.

Age differences of hand preference in R. roxellana

a. based on frequency data

b. based on bout data

* indicates significant difference between adults and juveniles (p < 0.05)

We found no significant sex difference either in direction of hand preference (frequency: U = 60.50; N₁ = 8; N₂ = 16; p = 0.830; the mean HI score per subject was −0.22, SE = 0.29 for males and −0.37, SE = 0.17 for females; bout: U = 55.00; N₁ = 8; N₂ = 16; p = 0.580; the mean HI score per subject was −0.18, SE = 0.27 for males and −0.38, SE = 0.15 for females) or in the strength of hand preference (frequency: U = 56.50; N₁ = 8; N₂ = 16; p = 0.644; the mean ABS-HI score per subject was 0.76, SE = 0.10 for males and 0.71, SE = 0.06 for females; bout: U = 59.50; N₁ = 8; N₂ = 16; p = 0.782; the mean ABS-HI score per subject was 0.69, SE = 0.10 for males and 0.66, SE = 0.06 for females).

Comparison with bimanual grooming task in the same species

Finally, we compared the HI scores for the tube task recorded here with previously published data on hand preference for bimanual grooming in another sample group (Zhao et al., 2010). We found hand preference for the experimental tube task was more biased toward left hand use compared to spontaneous bimanual grooming task for both the direction (frequency: U = 191.50; N₁ = 24; N₂ = 26; p = 0.019; the mean HI score was −0.32, SE = 0.15 for the tube task and −0.13, SE = 0.04 for the bimanual grooming; bout: U = 183.00; N₁ = 24; N₂ = 26; p = 0.012; the mean HI score was −0.31, SE = 0.14 for the tube task and −0.13, SE = 0.04 for the bimanual grooming) and the strength (frequency: U = 13.50; N₁ = 24; N₂ = 26; p < 0.001; the mean ABS-HI score per subject was 0.73, SE = 0.05 for the tube task and 0.21, SE = 0.02 for the bimanual grooming; bout: U = 5.50; N₁ = 24; N₂ = 26; p < 0.001; the mean ABS-HI score per subject was 0.67, SE = 0.05 for the tube task and 0.21, SE = 0.02 for the bimanual grooming).

DISCUSSION

This is the first study to present data on hand preference for the tube task in a wild primate species. Our study in R. roxellana, an arboreal Old World monkey species, revealed several interesting findings. First, group-level left-handedness was found in hand use for the tube task. Second, no significant differences were found between sexes, either in the direction or in the strength of hand preference. Third, the strength of manual laterality for the tube task was significantly stronger in adults than juveniles. Finally, the tube task elicits a stronger degree of hand preference than bimanual grooming.

We recorded both the frequency and bouts in hand use in this study and found that the correlation between the HI measures based on frequency and bouts of hand use was nearly 1.0. This affirms that the two measures quantify the same hand preference and, more importantly, demonstrates that frequency in hand use does not result in skewed distributions of hand preference, as has been suggested by some researchers (McGrew and Marchant, 1997; Cashmore et al., 2008; Cashmore, 2009). Of course, there were more ambiguously-handed subjects when considering hand preference classifications based on bouts of hand use; however, this is not unexpected because of the reduced number of observations for each subject, which makes it more difficult for the z-score to exceed 1.96 or −1.96.

It has been hypothesized that a) bimanual tasks elicit stronger hand preferences than unimanual tasks and b) that experimental tasks elicit stronger hand preferences than spontaneous tasks. In this study, we compared the hand preferences in R. roxellana for an experimental (tube) and spontaneous task (bimanual grooming) task that had the same motor demands (i.e., both required bimanual actions). As others have reported (Chapelain et al., 2006; Schweitzer et al., 2007), we found that the experimental tube task elicited stronger hand preferences than the spontaneous task. The most parsimonious explanation for this finding is that situational factors likely have little influence in hand use for the tube task compared to grooming. In the case of grooming, the position of the individual being groomed as well as the location of the body part being groomed may influence the hand use by the groomer. These factors are removed in the case of the tube task and likely allow the subjects to more overtly express endogenous preferences for use of the hands.

As a means of placing the results found here within a larger comparative primate perspective, we have plotted the mean HI scores based on frequency data for the snub-nose monkeys with the published HI scores of 9 other species. The results in wild R. roxellana are somewhat consistent with those findings in other Old and New World monkeys who are mostly arboreal species, with the exception of capuchin monkeys (Fig.3). It is found that, within apes, orangutans are the most left-handed and gorillas are the most right-handed and these two species are correspondingly the most arboreal and terrestrial ape species (Hopkins et al., 2011). In contrast, chimpanzees and bonobos show more intermediate patterns of hand use and their positional behaviors are more transient than those of the other great apes (Hopkins et al., 2011). Independent of the potential theoretical explanations for the findings reported in Figure 3, we believe the most important aspect of this and other studies is that species can be compared for the same task of evaluating hand preference. As additional data of hand preference accumulate in other species, this will provide an empirical framework for testing more comprehensive theories of the evolution of handedness which are difficult to conduct on a species by species basis.

Fig. 3.

The mean HI score based on frequency data for 10 nonhuman primate species that has been tested on the tube task

* indicates significant population-level handedness based on combined published data from each species.

Handedness data for each species came from the following sources: Great apes from Hopkins et al. (2011) and Llorente et al. (2011), rhesus monkeys from Bennett et al (2008), Barbary macaques from Schmitt et al. (2008), baboons from Vauclair et al. (2005), De Brazza monkeys from Schweitzer et al. (2007), and capuchin monkeys from Lilak and Phillips (2008), Meunier and Vauclair (2007) and Spinozzi et al. (1998).

Samples sizes for each species were: chimpanzees (n = 536), bonobos (n = 118), gorillas (n = 76), orangutans (n = 44), De Brazza (n =12), rhesus (n =74), Barbary (n = 28), baboon (n = 104) and capuchins (n = 54).

Note: The tube task has been administered in several other studies within the rhesus and capuchin monkey species but individual data were not available in the published papers, so they were not included in these analyses.

Current evidence on sex differences in primates hand preference is relatively weak (Fagot and Vauclair, 1993; Springer and Deutsch, 1993; Kimura, 1999; Hopkins, 2007a), and studies reporting sex difference vary between tasks and species (Milliken et al., 1991; Ward and Hopkins, 1993; Spinozzi et al., 1998; Corp and Byrne, 2004; Chapelain et al. 2011). For the tube task, the obvious sex difference is found in one study in Cebus apella (Spinozzi et al., 1998, but Spinozzi et al., 2007; Lilak and Phillips, 2008) and one study in Pan paniscus (Chapelain et al. 2011, but Chapelain and Hogervorst, 2009) respectively. Wild R. roxellana on the tube task did not present significant sex difference, which accords with previous studies on the tube task in other Old World monkeys. In addition, hand preference in R. roxellana does not differ between males and females on any spontaneous action in previous reports (Zhao et al., 2008a, 2010). Collectively, the results suggest that the absence of sex difference is one stable characteristic of hand preference in this species, without reference to spontaneous actions or experimental actions.

Increasing evidence has shown that primate manual laterality may increase with age (McGrew and Marchant, 1997). Immature individuals exhibit weaker or less consistent preferences than adults (Vauclair and Fagot, 1987; Milliken et al., 1991; Hopkins, 1994, 1995; Hook and Rogers, 2000; Teixeira, 2008). As the first study examining age differences of hand preference in R. roxellana, we found a significant effect of age on the strength of hand preference, but not on the direction of hand preference. Younger individuals were less lateralized than older individuals and these findings partly support the notion that individual hand preference of primates develops with age.

The wild R. roxellana preferred to use the index finger on the tube task, which accord with other primate species when performing the same action (e.g. Cebus apella: Spinozzi et al., 2007; Cebus capucinus: Meunier and Vauclair, 2007; Cercopithecus neglectus: Schweitzer et al., 2007; Pan paniscus: Chapelain and Hogervorst, 2009; Chapelain et al., 2011; Pan troglodytes: Hopkins, 1995; Papio anubis: Vauclair et al., 2005). It supports the viewpoint of Hopkins (1995) that the tube task requires refined movements of distal digits and hands rather than gross or ballistic movements. Distal movements have been shown to require a greater participation of the contralateral hemisphere (Brinkman and Kuypers 1972, in Hopkins 1995).

CONCLUSIONS

We demonstrate the first evidence of left-handedness in Old World monkey species under natural conditions. Our results in R. roxellana lend further support to task complexity theory raised by Fagot and Vauclair (1991). Our findings highlight the importance of applying the tube task as a standard measure of primate manual laterality, and warrant further investigation with more samples in this species as well as in other primate species under wild conditions. In addition, this study broadens our knowledge on evaluating primate hand preference via experimental manipulation in natural conditions.