International Journal of Primatology

, Volume 32, Issue 2, pp 491–510

Hand Preferences for Bimanual Coordination in 77 Bonobos (Pan paniscus): Replication and Extension

Authors

    • Department of Human SciencesLoughborough University
  • E. Hogervorst
    • Department of Human SciencesLoughborough University
  • P. Mbonzo
    • Sanctuaire des bonobosLola Ya Bonobo, Association ABC
  • W. D. Hopkins
    • Department of PsychologyAgnes Scott College
    • Division of PsychobiologyYerkes National Primate Research Center
Article

DOI: 10.1007/s10764-010-9484-5

Cite this article as:
Chapelain, A.S., Hogervorst, E., Mbonzo, P. et al. Int J Primatol (2011) 32: 491. doi:10.1007/s10764-010-9484-5

Abstract

The literature on manual laterality in nonhuman primates provides inconsistent and inconclusive findings and is plagued by methodological issues (e.g., small samples, inconsistency in methods, inappropriate measures) and gaps. Few data are available on bonobos and these are only from small samples and for relatively simple tasks. We examined laterality in a large sample of bonobos for a complex task. We tested 48 bonobos from Lola Ya Bonobo sanctuary (DR Congo) in an extension of our previous study of 29 bonobos from 3 European zoos. We assessed hand preferences using the tube task, which involves bimanual coordination: one hand extracts food from a tube that is held by the other hand. This task is a good measure of laterality and it has been used in other studies. We recorded events (frequency) and independent bouts of food extraction. We found significant manual laterality, which was not influenced by the settings or rearing history. We observed little effect of sex and found an influence of age, with greater right hand use in adults. The laterality was marked, with strong preferences and most individuals being lateralized (when analyzing frequency). We found individual preferences, with no group-level bias, even when we combined the data from the sanctuary and the zoos to enlarge the sample to 77. These first data, for a complex task and based on a large sample, are consistent with previous findings in bonobos and in other nonhuman primate species for a variety of tasks. They suggest that, despite particular features in terms of proximity to humans, language and bipedalism, bonobos do not display a laterality that is more marked or more similar to human handedness compared to that of other nonhuman primate species.

Keywords

Bimanual coordinationBonobosHand preferenceLateralityManipulationTube task

Introduction

Approximately 90% of humans use the right hand for complex actions (Annett 1985; Fagard 2004; Faurie 2004). This remarkable feature is referred to as right-handedness and is relatively constant between populations, although there is some cultural variation, with the percentage of right-handers ranging from 73% to 100% (Fagard 2004; Faurie 2004; Marchant et al.1995; Marchant and McGrew 1998; Raymond and Pontier 2004). Right-handedness is thought to be an ancient trait that was already present in early hominids (Cashmore et al. 2008; Coren and Porac 1977; Fagard 2004; Faurie 2004; Faurie and Raymond 2004; Uomini 2009). Neurologically, the preference for using the right hand is thought to be related to a specialization of the left hemisphere for manual functions (Corballis 1989; Fagard 2004). Despite extensive research, the origins and functions of human brain lateralization and handedness remain unresolved. There are several hypotheses (reviewed in Cashmore et al.2008; Chapelain 2010; McGrew and Marchant 1997; Papademetriou et al.2005) that propose different factors as possible selective pressure for the emergence of handedness, including: postural demands (McNeilage et al.1987), bipedalism, tool use (Kimura 1979), throwing (Calvin 1983), gestural communication and language (Corballis 2003; Hewes 1973; Vauclair 2004), precise actions, manipulations and bimanual actions, especially bimanual coordination (Byrne and Byrne 1991; Fagot and Vauclair 1991).

It is unlikely that handedness emerged de novo in humans (McNeilage et al.1987), so we can expect to find precursor forms in nonhuman species. Studying manual laterality, defined as a preference for using one hand over the other, in other species can provide clues to understanding the origins of human handedness. Nonhuman primates and especially great apes, are particularly valuable models for studying the evolution of human brain lateralization and handedness. Indeed, they are close to humans in the phylogeny, exhibit great similarities to humans in hand anatomy and skills (Byrne et al.2001) and display neuroanatomical brain asymmetries (Cantalupo and Hopkins 2001; Gannon et al.1998; Holloway and De La Coste-Lareymondie 1982; Hopkins et al.2000, 2007).

Many studies have examined hand preferences in nonhuman primates (review in Cashmore et al.2008; Fagard 2004; Hopkins 2006; Hopkins and Cantalupo 2005; McGrew and Marchant 1997; Papademetriou et al.2005). Previous studies have found evidence of manual preferences for a variety of actions, such as, reaching, feeding, carrying and manipulating. The proportion of nonlateralized subjects is relatively high in most cases. The preferences are generally present on an individual basis, with similar numbers of right-handers and left-handers, indicating no group-level bias. Group-level biases have occasionally been reported (e.g., in Hopkins 1994, 1995; Hopkins et al.2004; Vauclair et al.2005), but they are never as marked as the extreme bias that is observed in humans (90% of individuals of one kind). However, there is little consistency of findings between studies. Thus, this topic is a matter of considerable debate and inquiry (Fagot and Vauclair 1991; Hopkins 2006; Hopkins and Cantalupo 2005; Lehman 1993; McGrew and Marchant 1997; McNeilage et al.1987; Palmer 2002; Papademetriou et al.2005; Warren 1980).

Several major problems hinder research on hand preferences in nonhuman primates. First, the majority of studies have considered small groups of subjects (fewer than 10 individuals of the same species, Hopkins 2006; Marchant and McGrew 1991). This is problematic because a large sample (50 subjects) is required to reliably detect a group-level bias, particularly for a bias of the order of 65%, as found in nonhuman primates (Hopkins and Cantalupo 2005). Thus, small sample size is suspected to be responsible for the absence of group-level bias that is generally reported in the literature (Hopkins 2006; Hopkins and Cantalupo 2005; Marchant and McGrew 1991; McGrew and Marchant 1997).

The second central problem that hampers interpretation of the literature is methodological inconsistency between studies. A variety of tasks has been used to assess laterality, which raises problems because the strength and direction of hand preference vary according to the task (Chapelain et al.2006; Fragaszy and Mitchell 1990; Lilak and Phillips 2008; Marchant and McGrew 1996; Papademetriou et al.2005; Spinozzi et al.1998; Warren 1980). This makes it difficult to compare findings between studies and species.

Third, interpretation of the data is plagued by the use of methods that may not be appropriate. Most studies have used simple tasks to measure hand preferences (e.g., simple reaching), while laterality is more easily revealed in complex tasks (Fagot and Vauclair 1991). Thus, some of the negative findings in the literature may stem from the use of tasks that are not sufficiently complex (Fagot and Vauclair 1991; McGrew and Marchant 1997; McNeilage et al.1987). Task complexity is thus an important factor to consider when assessing hand preferences. Among complex tasks that are thought to be appropriate measures, bimanual manipulative coordinated actions with different but complementary roles (one hand manipulates an item that is held by the other hand) elicit particularly strong laterality (Byrne and Corp 2003; Hopkins 2006; Rogers and Kaplan 1996). Bimanual tasks are also less vulnerable to the influence of postural and situational factors (e.g., position of the object, Fagot et al.1991; Seltzer et al.1990; Vauclair and Fagot 1987), so hand preferences in such tasks are more likely to reflect brain lateralization (Hopkins 1994, 2006; Hopkins et al.2001). There is one particularly good measure, the tube task, which requires a precise bimanual coordination while manipulating a tube. The subject has to use one hand to extract food from a tube that is held by the opposite hand. Previous tube task studies revealed a marked laterality in nonhuman primates, with strong individual preferences and most individuals being lateralized (review in Chapelain 2010; Chapelain and Hogervorst 2009; Hopkins and Cantalupo 2005; Vauclair et al.2005) (Table I). Furthermore, group-level biases have been found: in chimpanzees (right bias, Hopkins 1995, 1999; Hopkins et al. 2001, 2004, 2005), orang-utans (left bias, Hopkins et al.2003), infant rhesus macaques (left bias, Westergaard et al.1997) and baboons (right bias, Vauclair et al.2005).
Table I

Studies that used the tube task to measure hand preferences (results for analyses based on frequency). Group-level biases are based on binomial tests on the number of right-handed versus left-handed subjects. % of right-handers: percentage of right-handers amongst lateralized subjects

Study

Species

N

Not lateralized

Right-handed

Left-handed

Group-level bias

% of right-handers

Vauclair et al. (2005)

Baboons (Papio anubis)

104

19

52

33

Right bias

61

Hopkins (1995)

Chimpanzees (Pan troglodytes)

110

19

59

32

Right bias

65

Hopkins (1999)

Chimpanzees (Pan troglodytes)

188

40

95

53

Right bias

64

Hopkins et al. (2001)

Chimpanzees (Pan troglodytes)

109

22

54

33

Right bias

62

Hopkins et al. (2004)

Chimpanzees, (Pan troglodytes)

467

33

272

162

Right bias

63

Schweitzer et al. (2007)

De Brazza's monkeys (Cercopithecus neglectus)

12

0

3

9

No bias

25

Hopkins et al. (2003)

Gorillas (Gorilla gorilla)

31

4

15

12

No bias

56

Begg-Reid and Schillaci (2008)

Gorillas (Gorilla gorilla)

6

2

3

1

NA

75

Chapelain and Fagard (submitted)

Humans (Homo sapiens sapiens)

52

6

42

4

Right bias

91

Hopkins et al. (2003)

Orangutans (Pongo pygmaeus)

19

0

4

15

Left bias

21

Westergaard et al. (1997)

Rhesus macaques (infants; Macaca mulatta)

19

4

3

12

Left bias

20

Westergaard and Suomi (1996)

Rhesus macaques (Macaca mulatta)

55

12

28

15

No bias

65

Bennett et al. (2008)

Rhesus macaques (Macaca mulatta)

124

25

49

50

No bias

49

Phillips and Sherwood (2005)

Tufted capuchins (Cebus apella)

7

1

3

3

No bias

50

Westergaard and Suomi (1996)

Tufted capuchins (Cebus apella)

45

6

19

20

No bias

49

Lilak and Phillips (2008)

Tufted capuchins (Cebus apella)

11

1

5

5

No bias

50

Meunier and Vauclair (2007)

White-faced capuchins (Cebus capucinus)

13

1

6

6

No bias

50

Fourth, many factors may influence hand preferences. For example, living conditions are suspected to affect the laterality of captive animals, with a possible influence of limited amount of space, little variety of external stimuli, interactions with right-handed humans, asymmetry in the environment and disturbed sociality (McGrew and Marchant 1997, 2001; Warren 1980). Being raised by humans during infancy has also been suggested to influence hand preferences (McGrew and Marchant 1997, 2001). Thus, studies should account for the influence of these factors, checking that rearing and settings do not affect the results. In addition to these external factors, sex and age should also be taken into account because they may influence laterality. For instance, several studies have found that males were more left-handed than females (e.g., Byrne and Corp 2003; Corp and Byrne 2004; Milliken et al.1991). Other studies have found that immature individuals exhibited weaker or less consistent preferences than adults, which indicates that laterality may increase with age, suggesting some maturation of hand preferences (e.g., Boesch 1991; Fletcher and Weghorst 2005; Hook and Rogers 2000; Hopkins 1994, 1995; Humle and Matsuzawa 2009; Milliken et al.1991; Vauclair and Fagot 1987; Ward et al.1990; Westergaard and Suomi 1993, 1994).

Finally, there are important gaps in the literature with respect to the species and tasks studied. For example, research has mainly focused on macaques and chimpanzees, while there has been relatively little investigation in bonobos. There are fewer than 10 published bonobo studies and these are based on small numbers of subjects (2–22 bonobos), which makes the findings difficult to interpret. Bonobos are an excellent model species for studying the evolution of handedness for several reasons. First, Pan is the closest taxon to humans in the phylogeny (Takahata and Satta 1997). Second, bonobos display linguistic abilities that may be greater than that of other ape species (Savage-Rumbaugh et al.1985, 1986) and they are thought to have a greater predisposition for bipedal gait and to use bipedal locomotion more frequently than other nonhuman primates (Susman 1984; Susman et al.1980). Bipedalism and language are traits that are proposed to have driven the evolution of handedness. Thus, hypotheses predict that bonobos should exhibit a pattern of laterality that is the closest to humans of all the nonhuman primates.

Previous studies on bonobos report evidence of manual preferences for various activities (e.g., reaching, feeding, carrying, hanging and gesturing, Christel et al.1998; Colell et al.1995; De Vleeschouwer et al.1995; Harrison and Nystrom 2008; Hopkins et al.1993; Hopkins and DeWaal 1995; Shafer 1997). A high proportion of individuals were nonlateralized for most of the actions studied. Moreover, only individual-level preferences were found (with the exception of carrying (group-level left bias) and initiating locomotion (group-level right bias), combining data from Hopkins et al. (1993) and Hopkins and DeWaal (1995)). It must be noted that these studies assessed hand preferences in spontaneous daily activities, including: feeding, carrying, leading limb, gesturing, reaching, manipulating, hanging and scratching (Harrison and Nystrom 2008; Hopkins et al.1993; Hopkins and DeWaal 1995; Shafer 1997) and for experiments that involved relatively simple tasks: reaching for food tasks (Christel et al.1998; Colell et al.1995; De Vleeschouwer et al.1995; Hopkins et al.1993). There are almost no data on complex tasks in bonobos. Particularly, there are virtually no data concerning bimanual manipulative coordination, while these actions are proposed to be involved in the emergence of handedness. Ingmanson (1998, 2005) studied hand use in wild bonobos for “the peeling of sugar cane, where one hand is used in power grip and the other for small manipulations” and showed that “individuals tended to be very consistent in the use of either the right or left hand” (Ingmanson 1998, p.125), but that no group-level bias occurred. However, these data were only published as abstracts and the sample size, methods and results are not available.

We aimed to provide data for a particularly relevant and complex task in a large sample of bonobos. We used the tube task, a bimanual manipulative coordinated task, to assess hand preferences in the bonobos of Lola Ya Bonobo sanctuary, the site that housed the largest captive bonobo group. This is an extension of our previous work in 29 bonobos housed in 3 zoos, using the same methods (Chapelain and Hogervorst 2009). When combining the new data from the sanctuary with the zoo data, the total sample analyzed included 77 bonobos, which is one third of the worldwide captive bonobo population. This large sample size allowed for reliable assessment of group-level laterality and enabled us to investigate the effects of sex, age, rearing history (mother-raised bonobos vs. bonobos that experienced various degrees of interactions with humans during infancy) and living conditions (4 conditions: Stuttgart zoo, Twycross zoo, Apenheul zoo and Lola Ya Bonobo sanctuary). The particular features of bonobos and the results of other species tested on this task lead to the prediction that bonobos should exhibit a marked laterality and a group-level right bias for the tube task.

Materials and Methods

Subjects:

We conducted this experiment between November 8 and December 20, 2007, on the bonobos of Lola Ya Bonobo sanctuary, Kinshasa (DR Congo). The sanctuary housed 58 bonobos, but we excluded individuals with finger mutilations or hand/arm injuries (current or old), as well as individuals that had insufficient data for analysis. We analyzed a sample of 48 individuals, which included 29 males and 19 females; 13 adults (10+ yr), 7 adolescents (7–9 yr), 25 juveniles (3–6 yr) and 3 infants (<3 yr) (Badrian and Badrian 1984). Because of the small number of infants, we analyzed infants and juveniles together.

All but 2 subjects that were born at the sanctuary, were orphans rescued from the bushmeat traffic and pet trade. They were separated from their mothers in early infancy (generally after 1 yr old) and then lived for a few months to several years in a human environment. When they arrived at the sanctuary, the infants lived in a nursery with other bonobo infants and were cared for by 4 human surrogate mothers. When they became independent, at ca. 5 yr, they were placed in a mixed age bonobo group in one of the 3 enclosures, where they had fewer interactions with human keepers (Table II). We refer to this rearing history as Lola reared.
Table II

Living conditions of the bonobos studied

 

N total

N tested

Settings

Interaction with the keepers

Visitors

Lola Ya Bonobo sanctuary, DR Congo

58

48

The enclosure included 30 ha of rainforest. It was divided into 3 separate enclosures (enclos1,enclos2, enclos3). Each enclosure hosted a group of ca. 15 bonobos.

Some interaction

Very few visitors.

Close to the bonobos

Twycross Zoo, Twycross, England

10

8

The cage included a grassy outdoor enclosure (25 × 16 m hexagon, area 800 m²) connected with an indoor part that was divided into 2 rooms (9.5 × 5.5 m and 9.5 × 6 m).

Very limited interaction

Very many visitors.

Close to the bonobos

Apenheul Zoo, Apeldoorn, Holland

9

8

The bonobos were housed on a large island with grass and bushes (area: 4.670 m2). The island was connected with a large indoor part that was divided into several rooms (total area: 175.2 m², largest room: 77.3 m² area with height: 8.2 m).

Some interaction

Very many visitors.

Far from the bonobos (and the zoo closes during winter)

Wilhelma Zoo, Stuttgart, Germany

16

13

The bonobos were separated into 2 groups. One group was housed in a room (9.32 × 5.25 m) connected with a small outdoor area (6.5 × 4.75 m); the other group was housed in a small room (4.12 × 2.75 m) connected with an outdoor area (4 × 9.5 m) (all concrete floor).

Some interaction

Very many visitors.

Close to the bonobos

N total = number of subjects in the group, N tested = number of subjects tested

The bonobos lived in a large area of rainforest that was divided into 3 enclosures (Table II). Each enclosure had a small enclosure used to isolate the individuals and a house where the bonobos slept at night. We tested the subjects in these isolation enclosures and houses to allow observations and avoid loss of the tubes.

We compared and combined the data from Lola Ya Bonobo sanctuary with those from our previous study (Chapelain and Hogervorst 2009) of 29 bonobos housed in 3 European zoos (Twycross, Apenheul and Stuttgart; Table II). This zoo group included 11 males and 18 females; 16 adults, 5 adolescents, 7 juveniles and 1 infant. Twenty-one bonobos were mother-reared and 8 bonobos were human hand-reared (removed from their mothers within the first weeks of life and reared by humans during infancy). The same observer (A. Chapelain) assessed hand preferences and she used the same methodology in the two studies. The settings varied from very unnatural settings at Stuttgart and Twycross (relatively small cages) via more natural at Apenheul (island), to natural-like at Lola Ya Bonobo (large forest enclosure) (Table II).

Finally, we compared the data from the combined bonobo sample (N = 77) to previously published data from a sample of chimpanzees tested with the same task (Hopkins 1995), which included 110 individuals from the Yerkes National Primate Research Center (Atlanta, GA, USA). The methodology used to record the data in chimpanzees was similar to that used here (for frequency).

Tube Task:

Given that hand preference varies according to the task, even small differences in the methods may yield to differences in the results. Therefore, we used strictly the same methodology here as in our previous study (Chapelain and Hogervorst 2009), which was similar to that used in other tube task studies (reviewed in Chapelain and Hogervorst 2009), to allow for reliable data comparisons. In the tube task, the individual holds a tube with one hand, while reaching for food inside with a finger of the other hand. The active hand studied is the one reaching for food; and the subordinate hand is the one holding the tube. The tubes were white plastic tubes (15 cm length, 32 mm diameter), baited with honey smeared on the inside edge at both ends. A. Chapelain conducted the experiment with the help of the keepers. We gave the baited tubes to the bonobo group by throwing them into the enclosure. We performed 10–12 test sessions for each of the 4 bonobo groups (nursery, enclos1, enclos2, enclos3), at the rate of 1 test session per day, on successive days. We tested each individual on a mean of 8 different days (range 3–12) to ensure a sufficiently large data set per individual to allow statistical detection of individual preferences (Marchant and McGrew 1991; McGrew and Marchant 1996, 1997). Several bonobos could use the tubes at the same time, but we observed only 1 randomly chosen individual at a time (focal animal sampling, Altmann 1974). We recorded data via direct observation of the bonobo group, using a Dictaphone.

Data Recorded:

We recorded the name of the individual, which hand held the tube, which hand was used to extract the food and which digit was inserted into the tube. We recorded data only when the bonobo held 1 tube in the subordinate hand. We excluded all other cases, e.g., when the bonobo held more than 1 tube, when it held a tube in the active hand, when it held the tube with a foot and when the tube was held by another individual. These requirements ensured that we analyzed data on bimanual coordination only and that the behavior was standardized between trials and across subjects.

We used 2 different recording techniques: frequency and bouts.

Frequency: We counted every time that the subject inserted its finger into the tube and brought it to the mouth. This variable has been used in most other studies, so we needed it for between-studies comparisons. However, this method has been criticized on grounds of lack of data independence, because the use of one hand could influence the following use of this hand in the subsequent trials of the sequence, so counting every trial could introduce biases in the sample (Marchant and McGrew 1991; McGrew and Marchant 1997; Palmer 2003). Most previous studies measured only frequency.

Bouts: To ensure that the data points were strictly independent of each others, we also recorded bouts for the action of inserting the finger into the tube and bringing it to the mouth. We counted 1 bout for 1 sequence of identical actions (Marchant and McGrew 1991; McGrew and Marchant 1996, 1997). We considered a sequence as terminated when the subject dropped the tube, changed the hand holding the tube, or manipulated the tube with both hands. After such an event, the hand used in the next bout was considered as independent of the one used previously (McGrew and Marchant 1997).

Statistical Analysis:

We calculated the commonly used handedness index (HI) for each individual, using the formula: HI = (R – L)/(R + L), where R and L are the numbers of times that the right and left hands were used to extract the food (Michel et al.1985). The HI gives the direction of preference from −1.0 to +1.0. Negative values indicate a left hand bias and positive values indicate a right hand bias. The absolute value of HI (ABSHI) gives the strength of preference from 0 to 1. We used the binomial test (B; Siegel and Castellan 1988) to evaluate the significance of differences between the use of the right and left hands for each individual. This allowed us to consider handedness on a discrete scale of measurement by classifying the subjects as right-handed, left-handed, or nonlateralized based on the z-score. We assessed group-level bias in the number of right-handed and left-handed individuals using the binomial test. We used the one-sample t-test (Siegel and Castellan 1988) to assess group-level bias in hand use. This test evaluated whether the mean HI value for the group differed from a chance distribution with a mean of 0. Finally, we investigated the effects of sex, age, rearing, settings and number of data points, using Mann–Whitney (MW), Kruskall-Wallis (KW) and Spearman correlation tests (Siegel and Castellan 1988). We used nonparametric tests because the data did not meet the criteria for using parametric statistics. We considered lateral biases as significant when p ≤ 0.05 (two-tailed). We used SPSS 16 for all analyses. To limit possible effects of small number of data points per individual, we excluded subjects with fewer than 15 data points, as done in our previous study (Chapelain and Hogervorst 2009). This reduced the sample to 40 individuals for analyses on bouts. We reanalyzed the chimpanzee data (Hopkins 1995) using the same statistical methods to allow for reliable comparison between the 2 species of Pan.

Results

Lola Ya Bonobo:

We provide descriptive statistics and analyses for Lola Ya Bonobo in Tables III, IV and V.
Table III

Descriptive statistics for laterality (frequency and bouts) for each sample

 

N

Number of data points

Not lateralized

Right-handed

Left-handed

Mean ABSHI

% preference

Mean HI

Lola Ya Bonobo

Frequency

48

Total: 7058

6 (12.5%)

22

20

0.458 (SE = ±0.006)

75.4% (SE = ±0.303, N = 42)

0.043 (SE = ±0.011)

Mean: 147.042 (SE = ±1.569, range = 17–332)

Bouts

40

Total: 1186

29 (72.5%)

6

5

0.335 (SE = ±0.007)

85.8% (SE = ±0.698, N = 11)

0.026 (SE = ±0.012)

Mean: 29.65 (SE = ±0.282, range = 15–56)

 

Zoos (Twycross, Stuttgart, Apenheul)

Frequency

29

Total: 7889

3 (10.3%)

11

15

0.569 (SE = ±0.011)

81.2% (SE = ±0.544, N = 26)

0.02 (SE = ±0.023)

Mean: 272 (SE = ±5.68, range = 47–656)

Bouts

29

Total: 1381

12 (41.4%)

8

9

0.492 (SE = ±0.01)

84% (SE = ±0.70, N = 17)

0.026 (SE = ±0.02)

Mean: 47.62 (SE = ±0.71, range = 15–98)

 

Lola Ya Bonobo + zoos

Frequency

77

 

9 (11.7%)

33

35

0.499 (SE = ±0.004)

77.6% (SE = ±0.198, N = 68)

0.034 (SE = ±0.008)

Bouts

69

 

41 (59.4%)

14

14

0.401 (SE = ±0.004)

84.7% (SE = ±0.37, N = 28)

0.026 (SE = ±0.007)

 

Chimpanzees (Yerkes Primate Research Center)

Frequency

110

Total: 11517

26 (23.6%)

54

30

0.497 (SE = ±0.003)

80.4% (SE = ±0.135, N = 84)

0.136 (SE = ±0.005)

Mean: 104.7 (SE = ± 0.765, range = 17–515)

% preference = mean percentage of use of the preferred hand.

Table IV

The effect of the number of data points per subject on laterality

 

Comparison of the number of data points between right-handed, left-handed and nonlateralized individuals, KW test

Correlation between the number of data points and the ABSHI values, Spearman test

Correlation between the number of data points and the HI values, Spearman test

Lola Ya Bonobo

Frequency

H = 0.047, df = 2, p = 0.977

p = –0.132, p = 0.371, N = 48

p = 0.006, p = 0.966, N = 48

Bouts

H = 7.304, df = 2, p= 0.026

p = –0.529, p= 0.0004, N = 40

p = –0.118, p = 0.423, N = 40

 

Lola Ya Bonobo + zoos

Frequency

H = 0.109, df = 2, p = 0.947

p = 0.023, p = 0.843, N = 77

p = 0.042, p = 0.716, N = 77

Bouts

H = 3.144, df = 2, p = 0.208

p = –0.194, p = 0.11, N = 69

p = –0.174, p = 0.153, N = 69

Significant results are in bold. There was no significant effect of the number of data points per subject (except in one case: a negative correlation between the number of data points and the ABSHI values for Lola Ya Bonobo (analyses based on bouts))

Table V

Effects of sex, age, settings and rearing on HI and ABSHI values (analyses not presented in the text)

 

Effect of

Analyses on HI values

Analyses on ABSHI values

Lola Ya Bonobo – frequency

Sex

MW test, U = 247.5, p = 0.555, N1 = 29, N2 = 19

MW test, U = 274, p = 0.975, N1 = 29, N2 = 19

Age

KW test, H = 1.665, p = 0.435

KW test, H = 0.17, p = 0.919

MW test, p ≥ 0.191

MW test, p ≥ 0.695

 

Lola Ya Bonobo – bouts

Sex

MW test, U = 130.5, p = 0.075, N1 = 23, N2 = 17

MW test, U = 190.5, p = 0.891, N1 = 23, N2 = 17

Age

KW test, H = 2.358, p = 0.308

KW test, H = 2.193, p = 0.334

MW test, p ≥ 0.126

MW test, p ≥ 0.184

 

Lola Ya Bonobo + zoos – bouts

Sex

MW test, U = 429.5, p = 0.047, N1 = 34, N2 = 35, higher HI values in males (mean = 0.138, SE = ±0.016) than females (mean = –0.083, SE = ±0.012)

MW test, U = 525.5, p = 0.404, N1 = 34, N2 = 35

Age

KW test, H = 2.117, p = 0.347

KW test, H = 0.298, p = 0.861

MW test, p ≥ 0.147

MW test, p ≥ 0.595

Settings

MW test, U = 514.5, p = 0.426, N1 = 40, N2 = 29

MW test, U = 391, p = 0.022, N1 = 40, N2 = 29, higher ABSHI in zoos (mean = 0.492, SE = ±0.01) than Lola (mean = 0.335, SE = ±0.007)

Rearing history

KW test, H = 0.736, p = 0.692

KW test, H = 5.292, p = 0.071

MW test, U = 472, p = 0.676, N1 = 21, N2 = 48

MW test, U = 372.5, p = 0.086, N1 = 21, N2 = 48

Means are given whenever the difference is significant. Results for Lola Ya Bonobo + zoos – frequency are presented in the text

When analyzing frequency (number of responses per subject), 42 bonobos (87.5%) were significantly lateralized and only 6 showed no preference. The mean HI value (0.043) was not significantly different from 0 (t(47) = 0.559, p = 0.579), indicating no bias in hand use. Twenty-two bonobos were classified as right-handed and 20 as left-handed, so there was no group-level bias in the number of right-handed and left-handed subjects (B test, z = 0.309, p = 0.878).

When analyzing bouts (number of bouts per subject), 11 bonobos (27.5%) were significantly lateralized and 29 showed no preference. The mean HI value (0.026) was not significantly different from 0 (t(39) = 0.382, p = 0.704), indicating no bias in hand use. Six bonobos were classified as right-handed and 5 were left-handed, so there was no group-level bias (B test, z = 0.302, p = 1).

Lola Ya Bonobo and the Zoos Combined:

Table III provides descriptive statistics for Lola Ya Bonobo and the zoos combined. Investigation of the effect of the number of data points per subject is provided in Table IV. The raw data and analyses for the zoo sample can be found in Chapelain and Hogervorst (2009) and these findings are summarized in Table III.

When analyzing frequency, 68 bonobos (88.3%) were significantly lateralized and only 9 showed no preference. The number of lateralized bonobos was greater than the number of nonlateralized individuals (B test, z = 6.724, p < 0.001). The mean HI value (0.034) was not significantly different from 0 (t(76) = 0.519, p = 0.605), indicating no bias in hand use. Thirty-three bonobos were classified as right-handed and 35 were left-handed, so there was no group-level bias in the number of right-handed and left-handed subjects (B test, z = 0.243, p = 0.904). The percentage of right-handers among lateralized subjects was 48.5% (42.9% of the whole group including nonlateralized subjects).

When analyzing bouts, 28 bonobos (40.6%) were significantly lateralized and 41 showed no preference. The number of lateralized subjects was not significantly different from the number of nonlateralized individuals (B test, z = 1.565, p = 0.148). The mean HI value (0.026) was not significantly different from 0 (t(68) = 0.434, p = 0.665), indicating no bias in hand use. Fourteen bonobos were classified as right-handed and 14 were left-handed, so there was no group-level bias (B test, z = 0, p = 1.149). The percentage of right-handers among lateralized subjects was 50% (20.3% of the whole group including nonlateralized subjects).

HI values for frequency and bouts were significantly positively correlated (Spearman test, p = 0.947, p < 0.001, N = 77), as were ABSHI values (Spearman test, p = 0.867, p < 0.001, N = 77). For the following analyses, we summarize the results of analyses based on bouts in Table V and present the results of analyses based on frequency in more detail in the text, because this is the measure used in all other studies.

There was no significant effect of sex on either HI (MW test, U = 622, p = 0.229, N1 = 40, N2 = 37) or ABSHI (MW test, U = 652.5, p = 0.372, N1 = 40, N2 = 37; Table VI). Comparing the 3 age groups (infants + juveniles N = 36, adolescents N = 12, adults N = 29) (Table VI, Fig. 1), we found no significant difference in HI (KW test, H = 4.469, df = 2, p = 0.107) or ABSHI (KW test, H = 0.247, df = 2, p = 0.884). However, when we compared each age group with each other group and with combined categories, using paired comparisons, adults displayed significantly higher HI values than infants + juveniles (MW test, U = 370.5, p = 0.046, N1 = 36, N2 = 29) and than nonadults (infants + juveniles + adolescents; MW test, U = 495, p = 0.035, N1 = 48, N2 = 29). In addition, there was a significant bias toward right hand use (right skewed HI values; t(28) = 2.059, p = 0.049) in adults. With regard to the strength of laterality, there was no significant effect of age on ABSHI (MW test, p ≥ 0.628).
Table VI

Laterality data for each category of subjects based on age and sex (analyses based on frequency)

 

Infants + juveniles

Adolescents

Adults

Males

Females

Lola Ya Bonobo

N

28

7

13

29

19

Mean HI

0.035 (SE = ±0.020)

–0.124 (SE = ±0.077)

0.152 (SE = ±0.036)

0.073 (SE = ±0.019)

–0.002 (SE = ±0.028)

Mean ABSHI

0.482 (SE = ±0.010)

0.425 (SE = ±0.045)

0.422 (SE = ±0.017)

0.466 (SE = ±0.010)

0.444 (SE = ±0.013)

 

Lola Ya Bonobo + zoos

N

36

12

29

40

37

Mean HI

–0.073 (SE = ±0.016)

–0.073 (SE = ±0.053)

0.212* (SE = ±0.019)

0.110 (SE = ±0.015)

–0.048 (SE = ±0.014)

Mean ABSHI

0.483 (SE = ±0.008)

0.527 (SE = ±0.028)

0.508 (SE = ±0.010)

0.533 (SE = ±0.008)

0.463 (SE = ±0.007)

 

chimpanzees

N

17

14

79

  

Mean HI

0.159 (SE = ±0.030)

0.014 (SE = ±0.037)

0.152* (SE = ±0.007)

  

Mean ABSHI

0.408 (SE = ±0.019)

0.433 (SE = ±0.018)

0.527 (SE = ±0.004)

  

Asterisks indicate significant biases based on t-tests

https://static-content.springer.com/image/art%3A10.1007%2Fs10764-010-9484-5/MediaObjects/10764_2010_9484_Fig1_HTML.gif
Fig. 1

Effect of age on HI values (analyses based on frequency).

There was no significant difference in either HI (MW test, U = 657, p = 0.682, N1 = 48, N2 = 29) or ABSHI (MW test, U = 554.5, p = 0.137, N1 = 48, N2 = 29) between the Lola Ya Bonobo sample and the zoo sample (Table III).

There was no significant difference in HI (KW test, H = 0.3, df = 2, p = 0.861) or ABSHI (KW test, H = 1.465, df = 2, p = 0.481) between bonobos with different rearing history: mother-reared (N = 23, HI = 0.003, SE = ±0.028, ABSHI = 0.565 SE = ±0.013), human hand-reared (N = 8, HI = 0.029 SE = ±0.079, ABSHI = 0.47 SE = ±0.048) and Lola reared (N = 46, HI = 0.051 SE = ±0.012, ABSHI = 0.472 SE = ±0.006). Finally, there was no difference in either HI (MW test, U = 572, p = 0.586, N1 = 23, N2 = 54) or ABSHI (MW test, U = 514, p = 0.234, N1 = 23, N2 = 54) between mother-reared bonobos and the other bonobos combined (human hand-reared + Lola reared).

Comparison with Chimpanzees:

Reanalyzing the data from Hopkins (1995), the number of lateralized chimpanzees (84) was greater than the number of nonlateralized subjects (26) (B test, z = 5.53, p < 0.001; Table III). The mean HI (0.136) was significantly different from 0 (t(109) = 2.552, p = 0.012) and was skewed toward the right, indicating a bias toward right hand use. Moreover, there was a group-level right bias in the distribution of the individuals, with significantly more right-handed (54) than left-handed subjects (30) (B test, z = 2.619, p = 0.012).

Using the same age categories as those used with bonobos (Badrian and Badrian 1984), there was no significant difference between the 3 age groups (infants + juveniles N = 17, adolescents N = 14, adults N = 79; Table VI, Fig. 1) in HI (KW test, H = 0.895, df = 2, p = 0.639) or ABSHI (KW test, H = 2.972, df = 2, p = 0.226). When we compared each age group with each other group and with combined categories, we also found no significant effect of age on HI (MW test, p ≥ 0.367) or ABSHI (MW test, p ≥ 0.087). There was a significant bias toward right hand use (right skewed HI values) in adults (t(78) = 2.335, p = 0.022) and in adults + adolescents (t(92) = 2.224, p = 0.029), but not in the other groups.

There was no significant between-species difference in HI (MW test, U = 3803.5, p = 0.236, N1 = 77, N2 = 110) or ABSHI (MW test, U = 4234.5, p = 0.999, N1 = 77, N2 = 110) between the chimpanzee sample and our combined bonobo sample.

Discussion

We assessed hand preferences in a large sample of bonobos for a bimanual manipulative coordinated task and found significant laterality, with individual preferences and no group-level bias. With regard to possible influential factors, our results suggest that neither housing nor rearing significantly influenced laterality. Indeed, there was no difference between the three zoos (Chapelain and Hogervorst 2009) or between the zoos and the sanctuary. We found only one difference between bonobos housed in different settings: the ABSHI values were higher in the zoos compared to the sanctuary (analyses based on bouts). However, this may be due to the difference in sample size (more data points per subject in the zoos), which can possibly influence ABSHI values (Hopkins 2006; Hopkins et al.2001, 2005; McGrew and Marchant 1997). Our findings match previous data that show no effect of settings on laterality in bonobos (Harrison and Nystrom 2008; Shafer 1997), as well as some data of other species (Hopkins et al.2004; Hopkins and Cantalupo 2005). We also found no significant difference in laterality between mother-reared, human hand-reared and Lola reared individuals, nor when we compared mother-reared bonobos with the other bonobos that were in close contact with humans during infancy. This suggests that human-rearing did not significantly influence hand preference. These are the first data on the effect of rearing on laterality in bonobos and they are consistent with several studies of other ape species (Fletcher and Weghorst 2005; Hopkins 1995; Hopkins et al.2003, 2004, 2005). Therefore, the observed laterality could not be an artificial product of biases related to captive settings or human-rearing and can be considered to be a natural phenomenon (Fletcher and Weghorst 2005; Hopkins 2006; Hopkins and Cantalupo 2005). It would be interesting to compare further captive subjects and wild subjects that live in their natural environment and have no close contact with humans. This is not yet possible, as there are almost no data on laterality in wild bonobos (only Ingmanson 1998; Ingmanson 2005 abstracts), so field studies are needed. The laterality that we observed may be related to brain lateralization (Corballis 1989; Fagard 2004; Fagot and Vauclair 1991; McNeilage et al.1987). In support of this idea, the preferences were very strong (exclusive in some cases) on this novel task, suggesting that it is unlikely that they were learned through practice on this task (Warren 1980).

We found no effect of sex on laterality in any of the 3 samples considered, with one exception. We found only one significant difference: a greater right hand use in males than females in the combined sample (Lola Ya Bonobo + zoos; analyses based on bouts). There was also a nonsignificant trend for males to be more strongly lateralized than females in the zoo-living bonobos (analyses based on bouts; Chapelain and Hogervorst 2009). Previous studies found that male bonobos were more right-handed than females in gesturing and carrying, while females were more right-handed than males for the leading limb in locomotion (Hopkins et al.1993; Hopkins and DeWaal 1995) and that females favored the right hand more than males for overall limb use (Harrison and Nystrom 2008). Thus, whilst our data and previous data suggest some influence of sex on hand preferences in bonobos for certain behaviors, this effect is variable. Sex has occasionally been shown to influence hand preferences in other species, but the results also vary between tasks, studies and species (Corp and Byrne 2004; Milliken et al.1991; Spinozzi et al.1998; Ward et al.1990).

We found no effect of age on the strength of laterality in any of the 3 samples considered. This suggests that laterality may not increase with age and is in accordance with previous data for overall limb use in bonobos (Harrison and Nystrom 2008). However, another study reported stronger laterality in old vs. young bonobos (Shafer 1997). Studies of other species have occasionally shown an increase in the strength of laterality with age (Fletcher and Weghorst 2005; Hook and Rogers 2000; Hopkins 1994, 1995; Humle and Matsuzawa 2009; Ward et al.1990; Westergaard and Suomi 1993). With regard to the direction of laterality, we found a significant effect of age in the combined sample (Lola Ya Bonobo + zoos; analyses based on frequency). Adults exhibited greater right hand use than both the youngest individuals (infants + juveniles) and the nonadults category. Moreover, there was a significant group-level bias toward right hand use (right skewed HI values) in adults. This age effect was also observed in the zoo-living bonobos, with adults displaying greater right hand use than the youngest individuals (Chapelain and Hogervorst 2009). This matches previous work on bonobos, which also found greater right hand use in adults compared to young subjects for several behaviors (feeding, reaching, bimanual feeding) (Hopkins et al.1993; Hopkins and DeWaal 1995). Thus, the data suggest an increase of right hand use with age in bonobos for certain behaviors. A similar age effect has been reported in several other species (e.g., lemurs, Ward et al.1990, macaques, Westergaard and Lussier 1999, capuchin monkeys, Westergaard and Suomi 1993, 1994). Taken together, these findings support the maturational hypothesis (Geschwind and Galaburda 1985) proposing that the left hemisphere (right hand) develops more slowly than the right hemisphere (left hand), which causes a greater use of the right hand with age. Longitudinal studies that follow the same individuals over several years are necessary to improve our understanding of age effects on laterality.

When considering the strength of laterality, bonobos showed pronounced individual hand preferences (up to 100% use of the preferred hand) and most individuals were lateralized, for analyses based on frequency. This marked laterality is consistent with the results of other species tested using the tube task (review in Chapelain and Hogervorst 2009) (Table I). It can be noted that laterality was generally weaker with bouts than with frequency (this study; Chapelain and Hogervorst 2009; Hopkins et al.2001). This effect is difficult to interpret because it is proposed to be related to the smaller sample size with bouts than frequency, as significant biases are more likely to appear with large than small samples (Hopkins 2006; Hopkins et al.2001, 2005; McGrew and Marchant 1997) (hypothesis tested and discussed in Chapelain and Hogervorst 2009). Our finding of strong laterality for bimanual manipulative coordination in bonobos is consistent with previous data on bimanual coordinated actions in bonobos and other species for the tube task and food-processing tasks (Byrne and Byrne 1991; Byrne and Corp 2003; Corp and Byrne 2004; Ingmanson 1998; Meguerditchian et al. 2010). This supports hypotheses proposing that complex tasks that are crucial for survival, such as food processing that involves bimanual coordination, manipulation and precise actions, elicit laterality; and suggests that these actions may have been selective pressures for the emergence of handedness.

When considering the direction of laterality, we found only individual-level preferences. No group-level bias occurred in the sample of 48 bonobos from Lola Ya Bonobo and in the enlarged sample combining these new data with those from 29 zoo-living bonobos. Thus, these results based on a larger sample confirm those of our previous study (Chapelain and Hogervorst 2009). Most previous works suffer from small sample size issues that hamper detection of group-level biases (Hopkins 2006; Marchant and McGrew 1991). Our sample of 77 bonobos was appropriate to detect a human-like extreme group-level bias (90%), as well as smaller biases (65%) such as those found in nonhuman primates. Therefore, our data allow us to reliably conclude that bonobos do not exhibit group-level laterality for the tube task. In the literature, the tasks used vary considerably between studies (notably regarding complexity), which hinders data interpretation. We used a complex task that is a good measure for revealing laterality. Our result is consistent with previous findings in bonobos for simpler tasks and smaller samples (Christel et al.1998; Colell et al.1995; De Vleeschouwer et al.1995; Harrison and Nystrom 2008; Hopkins et al.1993; Hopkins and DeWaal 1995; Ingmanson 1998; Ingmanson 2005; Shafer 1997). Thus, even when a large sample of subjects is tested using an appropriate measure, bonobos do not exhibit group-level laterality. When comparing with previous tube task studies in other species, our finding is consistent with several studies that report only individual-level preferences; in gorillas, white-faced capuchins, tufted capuchins, rhesus macaques and de Brazza’s monkeys. However, other studies found significant group-level biases; in orang-utans, infant rhesus macaques, baboons, chimpanzees and humans (Table I). The difference with chimpanzees is particularly surprising because the two species are so closely related (Takahata and Satta 1997). A large number of chimpanzees have been tested with the tube task (N = 467) and group-level right biases have been reported in different populations (Hopkins 1995, 1999; Hopkins et al.2001, 2004, 2005). When we reanalyzed and compared a sample of chimpanzees (Hopkins 1995) with our bonobo sample, we found no difference between bonobos and chimpanzees in HI and ABSHI values; but only the chimpanzees exhibited a group-level bias. This is a difference for which we have no explanation at present. There is also a striking difference between bonobos and humans, but in fact, humans differ from all nonhuman primate species, exhibiting an outstanding group-level bias for the tube task (Chapelain and Fagard submitted) (Table I).

In conclusion, we examined a large sample of bonobos using a complex task and found evidence of significant manual laterality. This laterality was not related to artificial biases due to captive settings or human-rearing and can possibly reflect a brain lateralization for manual functions. We found little effect of sex and observed an influence of age, with greater right hand use in adults. The laterality was very marked, indicating that bimanual manipulative coordination elicited laterality, suggesting that this could be a selective pressure for the emergence of handedness. However, the preferences were individual and no group-level bias occurred. Finally, the pattern of laterality was weaker than that observed in humans (Annett 1985; Fagard 2004; Faurie 2004), even when considering comparable data based on the same task (Chapelain and Fagard submitted). These findings are consistent with previous data in bonobos and with results in other nonhuman primate species for the same task and for different tasks. Our data indicate that, despite their proximity to humans and particular features in terms of language and bipedalism, bonobos display a laterality that is not particularly outstanding, being not more marked or more similar to human handedness than that of other nonhuman primate species.

Acknowledgments

We thank the keepers of Lola Ya Bonobo (Jean-Claude Nzumbi, Stany Mokando, Claude Paluku, Amos Kisungu, Henriette Lubondo, Yvonne Vela Tona, Micheline Nzonzi, Espérance N’Sona), all the staff of the sanctuary and especially the director, Claudine André and the research coordinator, Brian Hare. We also thank the editor, anonymous reviewers and Shan Cook for their advice on this article. This study was part of Amandine Chapelain Ph.D. research, funded by Loughborough University, UK. This research conducted at Lola Ya Bonobo was funded by NIH grant HD-56232 and NS-42867 to Dr. William Hopkins.

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