Hand preference in a captive island group of chimpanzees (Pan troglodytes)

Morphological cerebral asymmetries in chimpanzee brains, similar to those found in humans, in whom they are associated with speech and handedness, suggest the possibility of functional lateralization in the chimpanzee. This possibility was investigated by examining hand preferences in an island group of five chimpanzees on a series of unimanual and bimanual tasks that are diagnostic of human hand and cerebral dominance. Each subject was tested in a double compartment cage on three unimanual nonsequential, three unimanual sequential, and three bimanual coordination tasks. One of the three unimanual sequential tasks was a bar-press task that is analogous to the commonly used human finger-tapping task. For the unimanual tasks, exclusive of the bar-press, the chimpanzees showed a highly individualistic pattern of hand preference that did not change as a function of task complexity. On the bar-press task, four of five subjects produced higher rates with one hand compared to the other; however, relative hand performance on this task was unrelated to hand preference on the other unimanual tasks. For the group of subjects, performance rates did not differ between the left and right hands; however, a practice effect was observed for the right hand in all subjects. The bimanual tasks also revealed a complex pattern of individual handedness, with no trends apparent for the group as a whole. Consistent with previous findings, the results from these tests on this group of five chimpanzees suggest that cerebral morphological asymmetries in the chimpanzee are not associated with motor dominance as reflected in handedness.     

Manual Laterality for Simple Reaching and Bimanual Coordinated Task in Naturalistic Housed <Emphasis Type="Italic">Pan troglodytes</Emphasis>

Researchers have shown renewed interest in the study of manual lateralization in chimpanzees. Currently there is no consensus confirming the presence or absence of manual dominance at a species level, mainly for populations in the wild and in semicaptivity. We aimed to evaluate the manual laterality in a group of chimpanzees in an intermediate setting (semicaptivity) via 2 tasks: one simple and unimanual (simple reaching) and the other complex and bimanual (tube task). We replicated the same experiments from Hopkins in a new and different sample of chimpanzees. In simple reaching, the hand is used to gather food and the type of grip and the posture are evaluated. The tube task assesses the hand used to extract food from the tube and the method of extraction (digital or instrumental). Through the handedness index we observed that the subjects show clear and strong individual preferences for both tasks (100% lateralized subjects in the tube task; 86% in simple reaching), although we did not detect population preferences for any of the tasks. However, considering both tasks jointly (multiple evaluation), it was possible to detect, for the first time, skilled manual dominance at a group level in semicaptive chimpanzees in one multitask index and borderline significance in a second multitask index.     

Hand Preference for a Novel Bimanual Coordinated Task During Termite Feeding in Wild Western Gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>)

Although the level of handedness in humans varies cross-culturally, humans are generally described as right-handed, which has been considered a uniquely human trait. Recently, captive chimpanzees (Pan troglodytes) have been shown to exhibit right-hand preference when performing bimanual but not unimanual tasks. Less clear is whether this pattern also occurs in wild chimpanzees and other African apes. Using videos (N = 49) of six wild western gorillas (Gorilla gorilla gorilla) feeding on termites at the Mondika Research Center (Republic of Congo), we tested whether they exhibit hand preference when performing unimanual, i.e., reaching for termite mound pieces; bimanual, i.e., “termite tapping”: rhythmically shaking a piece of termite mound with the dominant hand and collecting the termites in the other hand tasks; or hand transfer prior to bimanual tasks, i.e., transferring a piece of termite mound from one hand to the other. All individuals exhibited exclusive hand preference when performing the bimanual tasks, with five of six gorillas preferring the right hand. Conversely, most individuals did not show any manual preference during the unimanual task. In addition, hand preference during hand transfer revealed clear hand dominance of similar strength and direction of those shown for the bimanual task, suggesting that this measure is as sensitive as the bimanual task itself. Thus, we propose “termite feeding” as a novel task to be considered in future hand-preference studies in wild western gorillas. Our results are in concordance with those for chimpanzees and captive gorillas showing hemispheric specialization for bimanual actions in apes.     

Hand preferences on unimanual and bimanual tasks in Tonkean macaques (Macaca tonkeana)

This is the first study to examine hand preferences in Tonkean macaques on a bimanual task. One of our objectives was to continue the move toward greater task standardization, in order to facilitate comparisons between species and studies on handedness. The main aim was to test and determine task robustness, by varying intra‐task complexity. To this end, we administered several different tasks to the subjects: two unimanual tasks (grasping task featuring items of different sizes) and three coordinated bimanual tasks (tube task involving different materials, weights, and diameters). Although we found no significant hand preference in either task at the group level, the macaques were more strongly lateralized for small items than for large ones in the unimanual grasping task. Moreover, the absence of a correlation between these two versions of the unimanual task confirmed the weakness of this grasping task for assessing handedness. Regarding the bimanual tube task, no difference was found between the three versions in either the direction or the strength of hand preference. Moreover, the highly correlated hand preferences between these three versions suggest that the tube task provides a more robust means of measuring manual preferences. Am J Phys Anthropol 152:315–321, 2013. © 2013 Wiley Periodicals, Inc.     

Laterality in hand use across four tool-use behaviors among the wild chimpanzees of Bossou, Guinea, West Africa

Population-level right handedness is a human universal, whose evolutionary origins are the source of considerable empirical and theoretical debate. Although our closest neighbor, the chimpanzee, shows some evidence for population-level handedness in captivity, there is little evidence from the wild. Tool-use measures of hand use in chimpanzees have yielded a great deal of variation in directionality and strength in hand preference, which still remains largely unexplored and unexplained. Data on five measures of hand use across four tool-use skills--ant-dipping, algae-scooping, pestle-pounding and nut-cracking--among the wild chimpanzees of Bossou, Guinea, West Africa, are presented here. This study aims to explore age- and sex-class effects, as well as the influence of task motor, cognitive and haptic demands, on the strength and directionality of hand preference within and across all five measures of hand use. Although there was no age- or sex-class effect on the directionality of hand preference, immature 相似文献   

Hand preferences on unimanual and bimanual tasks in white-faced capuchins (Cebus capucinus)

This study examined hand preference in white-faced capuchins on a unimanual task and on a coordinated bimanual task. For the unimanual task, handedness was assessed by observing simple reaching for small grains. For the bimanual task, tubes lined with chocolate paste inside were presented to the capuchins. The hand and the finger(s) used to remove chocolate paste were recorded. Seven individuals out of eight in the reaching task and 12 out of 13 in the tube task exhibited a hand preference. Moreover, test-retest correlations showed stability in hand use across time for the coordinated bimanual task. We found no significant differences in strength of hand preference between sexes. Finally, as noted in other primate species, the capuchins were more lateralized in the bimanual task compared to the unimanual task.     

Can the Patterns of Sexual Swelling Cycles in Female Taï Chimpanzees be Explained by the Cost-of-Sexual-Attraction Hypothesis?

Chimpanzee females of East and West African populations differ in the average number of cycles per interbirth interval. Whereas females in Gombe, Mahale, and Kibale (eastern chimpanzees, Pan troglodytes schweinfurthii) average <9 cycles before they conceive, females at Taï (western chimpanzees; Pan troglodytes verus) average 29 cycles. We examined data from 2 different study groups (North and South) at Taï. By showing that Taï females interrupt cyclic activity for, on average, 7.4 mo between the end of the postpartum amenorrhea period (PPA) and the subsequent conception, and by calculating the number of cycles to conception based on a probability distribution of cycles over the interbirth interval, we show that Taï females average 19.4 cycles (North Group) and 11.7 cycles (South Group) to conception; therefore, the earlier calculation of 29 cycles was an overestimate. Further, at Taï young parous females have a significantly shorter PPA than those of older females, but the number of cycles to conception does not differ significantly between primiparous and nulliparous females. Some of our results are therefore not in line with the predictions of the cost-of-sexual-attraction hypothesis, which proposes that the factor ultimately responsible for the intensity of female sexual attractiveness is female intragroup scramble competition. We discuss an alternative hypothesis—the social passport hypothesis—which is compatible with the results of the study.     

Stable nitrogen isotope analysis of dentine serial sections elucidate sex differences in weaning patterns of wild chimpanzees (Pan troglodytes)

Offspring provisioning is one of the most energetically demanding aspects of reproduction for female mammals. Variation in lactation length and weaning strategies between chimpanzees (Pan troglodytes), our closest living relative, and modern human societies have been reported. When and why these changes occurred is frequently debated. Our study used stable nitrogen isotope data of tooth root dentine from wild Western chimpanzees (Pan troglodytes verus) in Taï National Park, Côte d'Ivoire, to quantify weaning in these chimpanzees and explore if infant sex plays a role in maternal investment. We analyzed serial sections of deciduous lateral incisor root dentine from four Taï chimpanzees to establish the δ¹⁵N signal of nursing infants; we then analyzed serial sections of first permanent mandibular molar root dentine from 12 Taï chimpanzees to provide quantitative δ¹⁵N data on weaning in this population. Up to 2 years of age both sexes exhibited dentine δ¹⁵N values ≈2–3‰ higher than adult female Taï chimpanzees, consistent with a nursing signal. Thereafter a steady decrease in δ¹⁵N values consistent with the onset, and progression, of weaning, was visible. Sex differences were also evident, where male δ¹⁵N values decreased at a significantly slower rate compared to females. Confirmation of sex differences in maternal investment among Taï chimpanzees, demonstrates the viability of using isotope analysis to investigate weaning in non‐human primates. Additionally, assuming that behaviors observed in the Taï chimpanzees are illustrative of the ancestral pattern, our results provide a platform to enable the trajectory of weaning in human evolution to be further explored. Am J Phys Anthropol 153:635–642, 2014. © 2013 Wiley Periodicals, Inc.     

Sex difference in chimpanzee handedness

Chimpanzees at Mahale, Tanzania, show strong individual hand preferences when they use bimanual actions in processing the fruit of Saba florida and Citrus lemon. The direction of hand preference differs between the sexes: most males are left-handed, whereas most females are right-handed. Monkeys and apes are considered to lack "handedness," in the sense of a population mode of left- or right-hand preference; they are normally ambidextrous. Indeed, strong individual preferences were previously seldom found in natural tasks. We propose that lateralization of manual actions becomes advantageous in bimanual tasks, which involve role differentiation between the hands and a need to combine power and precision. If the pattern of lateralization found here reflects the ancestral state, common to chimpanzees and humans, this may explain why, in modern humans, women tend more strongly to be right-handed than men, who include a larger minority of left-handers.     

How similar are nut-cracking and stone-flaking? A functional approach to percussive technology

Various authors have suggested similarities between tool use in early hominins and chimpanzees. This has been particularly evident in studies of nut-cracking which is considered to be the most complex skill exhibited by wild apes, and has also been interpreted as a precursor of more complex stone-flaking abilities. It has been argued that there is no major qualitative difference between what the chimpanzee does when he cracks a nut and what early hominins did when they detached a flake from a core. In this paper, similarities and differences between skills involved in stone-flaking and nut-cracking are explored through an experimental protocol with human subjects performing both tasks. We suggest that a ‘functional’ approach to percussive action, based on the distinction between functional parameters that characterize each task and parameters that characterize the agent''s actions and movements, is a fruitful method for understanding those constraints which need to be mastered to perform each task successfully, and subsequently, the nature of skill involved in both tasks.     

Laterality of hand use pays off in foraging success for wild chimpanzees

The aim of this study was to see if behavioral lateralization in hand use benefits a lateralized organism in nature. We recorded wild chimpanzees (Pan troglodytes schweinfurthii) at Gombe, Tanzania, fishing for termites (Macrotermes spp.), an extractive foraging task using elementary technology. We compared individual apes who were completely lateralized, using only one hand or the other for the task, versus those who were incompletely lateralized, using either hand. Exclusively lateralized individuals were more efficient, that is, gathered more prey per unit effort, but were no different in success or error rate from incompletely lateralized apes. This is the first demonstration of a payoff to laterality of behavioral function in primates in conditions of ecological validity.     

Lateralization of hand skill in bipolar affective disorder

Diverse strands of evidence suggest that schizophrenia is associated with an excess of left and mixed handedness, reflecting anomalous cerebral lateralization. Genetic studies have indicated a degree of overlap between bipolar disorder (BPD) and schizophrenia. Nevertheless, pattern of handedness and degree of lateralization have not been explicitly tested in BPD. We measured handedness, footedness and relative manual dexterity in a sample of 47 families comprising BPD probands and their bipolar-spectrum and unaffected relatives (N = 240). The BPD I sample (N = 55) was significantly more lateralized on handedness, footedness and relative manual dexterity than their unaffected relatives (N = 66). They were also more lateralized than their relatives with other psychiatric diagnoses. No evidence of excess mixed handedness or footedness was observed in the BPD I sample. We raise the possibility that schizophrenia and BPD I differ in that disproportionate left-hemisphere dominance in BPD I is associated with right-hemisphere dysfunction leading to deficits in emotional regulation. Given our results, we hypothesized that degree of lateralization may be a phenotypic marker or endophenotype for BPD I. We therefore conducted a family-based genetic association analysis with this quantitative trait. Relative hand skill was significantly associated with a functional variant in the catechol-O-methyltransferase gene. We speculate that this polymorphism may influence brain lateralization.     

Handedness and Grooming in Pan troglodytes: Comparative Analysis Between Findings in Captive and Wild Individuals

Grooming is a complex set of motor actions, common in highly social primates. We tested for asymmetries in hand use during unimanual and bimanual allogrooming in 215 captive chimpanzees. In addition to hand use, we coded in the ethogram whether the manual grooming action co-occurred with the use of the mouth. Overall, grooming did not elicit strong handedness at the individual level, but there is a small yet significant population-level right-hand bias for bimanual grooming. Mouth use during grooming had no influence on hand use. A comparison of the findings with previously published data on handedness for grooming in wild chimpanzees suggests that wild apes are more right-handed than captive individuals are for allogrooming. Collectively, the results suggest that role differentiation of the hands is an important factor in the assessment of handedness for grooming, and perhaps additional manual actions of chimpanzees and other primates.     

Lateralized behaviour of a non-social cichlid fish (Amatitlania nigrofasciata) in a social and a non-social environment

Cerebral lateralization, the partitioning of cognitive function preferentially into one hemisphere of the brain, is a trait ubiquitous among vertebrates. Some species exhibit population level lateralization, where the pattern of cerebral lateralization is the same for most members of that species; however, other species show only individual level lateralization, where each member of the species has a unique pattern of lateralized brain function. The pattern of cerebral lateralization within a population and an individual has been shown to differ based on the stimulus being processed. It has been hypothesized that sociality within a species, such as shoaling behaviour in fish, may have led to the development and persistence of population level lateralization. Here we assessed cerebral lateralization in convict cichlids (Amatitlania nigrofasciata), a species that does not shoal as adults but that shoals briefly as juveniles. We show that both male and female convict cichlids display population level lateralization when in a solitary environment but only females show population level lateralization when in a perceived social environment. We also show that the pattern of lateralization differs between these two tasks and that strength of lateralization in one task is not predictive of strength of lateralization in the other task.     

Assessment of Cerebral Lateralization in Children using Functional Transcranial Doppler Ultrasound (fTCD)

There are many unanswered questions about cerebral lateralization. In particular, it remains unclear which aspects of language and nonverbal ability are lateralized, whether there are any disadvantages associated with atypical patterns of cerebral lateralization, and whether cerebral lateralization develops with age. In the past, researchers interested in these questions tended to use handedness as a proxy measure for cerebral lateralization, but this is unsatisfactory because handedness is only a weak and indirect indicator of laterality of cognitive functions¹. Other methods, such as fMRI, are expensive for large-scale studies, and not always feasible with children².Here we will describe the use of functional transcranial Doppler ultrasound (fTCD) as a cost-effective, non-invasive and reliable method for assessing cerebral lateralization. The procedure involves measuring blood flow in the middle cerebral artery via an ultrasound probe placed just in front of the ear. Our work builds on work by Rune Aaslid, who co-introduced TCD in 1982, and Stefan Knecht, Michael Deppe and their colleagues at the University of Münster, who pioneered the use of simultaneous measurements of left- and right middle cerebral artery blood flow, and devised a method of correcting for heart beat activity. This made it possible to see a clear increase in left-sided blood flow during language generation, with lateralization agreeing well with that obtained using other methods³.The middle cerebral artery has a very wide vascular territory (see Figure 1) and the method does not provide useful information about localization within a hemisphere. Our experience suggests it is particularly sensitive to tasks that involve explicit or implicit speech production. The ''gold standard'' task is a word generation task (e.g. think of as many words as you can that begin with the letter ''B'') ⁴, but this is not suitable for young children and others with limited literacy skills. Compared with other brain imaging methods, fTCD is relatively unaffected by movement artefacts from speaking, and so we are able to get a reliable result from tasks that involve describing pictures aloud^5,6. Accordingly, we have developed a child-friendly task that involves looking at video-clips that tell a story, and then describing what was seen.     

Passive acoustic monitoring reveals group ranging and territory use: a case study of wild chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Background

Assessing the range and territories of wild mammals traditionally requires years of data collection and often involves directly following individuals or using tracking devices. Indirect and non-invasive methods of monitoring wildlife have therefore emerged as attractive alternatives due to their ability to collect data at large spatiotemporal scales using standardized remote sensing technologies. Here, we investigate the use of two novel passive acoustic monitoring (PAM) systems used to capture long-distance sounds produced by the same species, wild chimpanzees (Pan troglodytes), living in two different habitats: forest (Taï, Côte d’Ivoire) and savanna-woodland (Issa valley, Tanzania).

Results

Using data collected independently at two field sites, we show that detections of chimpanzee sounds on autonomous recording devices were predicted by direct and indirect indices of chimpanzee presence. At Taï, the number of chimpanzee buttress drums detected on recording devices was positively influenced by the number of hours chimpanzees were seen ranging within a 1 km radius of a device. We observed a similar but weaker relationship within a 500 m radius. At Issa, the number of indirect chimpanzee observations positively predicted detections of chimpanzee loud calls on a recording device within a 500 m but not a 1 km radius. Moreover, using just seven months of PAM data, we could locate two known chimpanzee communities in Taï and observed monthly spatial variation in the center of activity for each group.

Conclusions

Our work shows PAM is a promising new tool for gathering information about the ranging behavior and habitat use of chimpanzees and can be easily adopted for other large territorial mammals, provided they produce long-distance acoustic signals that can be captured by autonomous recording devices (e.g., lions and wolves). With this study we hope to promote more interdisciplinary research in PAM to help overcome its challenges, particularly in data processing, to improve its wider application.

     

Buttress drumming by wild chimpanzees: Temporal patterning, phrase integration into loud calls, and preliminary evidence for individual distinctiveness

Wild chimpanzees (Pan troglodytes) generate low-frequency sounds that are audible to humans from a distance of at least 1 km away by hitting the buttresses of trees with their hands and feet. This buttress drumming occurs in discrete bouts of rapidly delivered beats that usually accompany “pant hoots,” the species-specific long-distance vocalization. Individual differences in male chimpanzee (P.t. verus) drumming were investigated during a 6-month field study in the Taï National Park, Ivory Coast. Analysis of drumming bouts recorded from six adult males revealed significant differences between individuals in three acoustic features: (1) mean duration of inter-beat interval; (2) mean number of beats per bout; and (3) mean bout duration. Preliminary analysis indicated that individuals differ in their tendency to deliver drum beats in temporally close pairs separated by longer interbeat intervals. Qualitative examination also suggested that individuals may differ in the temporal integration of drumming into the pant hoot vocalization. These results suggest that there may be acoustic cues available for chimpanzees to recognize unseen males by their drumming performances alone. Drumming by Taï chimpanzees was also compared to drumming by chimpanzees (P.t. schweinfurthii) from the Kanyawara study group in Kibale National Park. Uganda. The Kanyawara chimpanzees appeared to drum more often without vocalizing than did the Taï chimpanzees. When they did drum and vocalize together, the Kanyawara chimpanzees appeared to integrate their drumming later into the associated pant hoots than did the Taï chimpanzees. These results suggest the possibility that interpopulation variation exists in chimpanzee buttress drumming.     

Clapping in chimpanzees: evidence of exclusive hand preference in a spontaneous, bimanual gesture

An increased understanding of spontaneous bimanual tasks performed by chimpanzees would enhance the ongoing debate on population handedness in this species, and thus shed light on the evolution of hemispheric lateralization in humans. However, documentation of such bimanual activities has been largely absent in the literature because such behavior is infrequently observed in the natural repertoire of this species. This study presents data on a simple, spontaneous bimanual gesture-"clap"-that was investigated in a naturalistic group of 26 chimpanzees (Pan troglodytes). Sixteen individuals exhibited a total of 657 bouts of clapping directed toward humans, usually in the context of food availability. Most individuals were exclusive in their dominant hand preference, but since there was no population bias to the right or the left, the population is placed at level 3 of McGrew and Marchant's [Yearbook of Physical Anthropology 40:201-232, 1997] laterality framework. This is the first reported evidence of level 3 laterality in a non-tool-using task. Clapping increased in frequency with age, being common in adults, present at lower rates in adolescents, and absent in infants and juveniles. There was no effect of rearing or sex. The lack of population bias to the left or right for this bimanual gesture has implications for the debate on the evolution of language.     

Factor Analysis of Multiple Measures of Hand Use in Captive Chimpanzees: An Alternative Approach to the Assessment of Handedness in Nonhuman Primates

We tested whether chimpanzee handedness could be characterized as either unidimensional or multidimensional when considered across multiple measures of hand use. We determined for each of 6 different tasks in a sample of 105 captive chimpanzees hand preferences, and subjected the individual hand preference scores to a factor analysis. Five of the 6 tasks loaded on two separate factors that accounted for 54% of the variance. To assess population-level handedness, we calculated handedness indices for the loadings on each factor, for the item loadings across all factors, and for all tasks including ones that did not load on any factor. There is significant population-level right handedness for all 4 indices, which suggests that chimpanzee handedness is multidimensional and not task specific.