Effects of upright posture on hand preference for reaching vs. the use of probing tools by tufted capuchins (Cebus apella)

This research examined the effects of task (reaching vs. Tool use) and posture (quadrupedal vs. bipedal) on hand preference in tufted capuchins (Cebus apella). Regarding direction of hand preference, we found a significant main effect of posture, as the bipedal stance elicited greater use of the right hand than did the quadrupedal stance, and a significant posture × task interaction, as bipedal reaching elicited greater use of the right hand than did other postural and task conditions. Further, we found a significant main effect of task on strength of hand preference, as tool use elicited more consistent use of one hand over the other than did reaching. Our findings indicate that bipedal reaching facilitates a mild right-hand bias in intensely manipulative primates. We speculate that this moderate bias may have been pushed in the direction of nearly exclusive right-hand preference in most humans with the development of complex tool use. Am. J. Primatol. 44:147–153, 1998. © 1998 Wiley-Liss, Inc. This article is a US Government work and, as such, is in the public domain in the United States of America.     

Carrying, Sharing, and Hand Preference in Tufted Capuchins (Cebus apella)

We examined the relationship among carrying, food-sharing, and hand preference in tufted capuchins (Cebus apella). The rationale was to evaluate further the use of Cebus as an alternative primate model to Pan for behavior relevant to early hominid evolution. We first examined bipedalism and food-sharing within an established social group, and then examined the direction and strength of hand preference for food carrying in an expanded sample. Several aspects of capuchin behavior warrant discussion. First, bipedal carrying and food-sharing occurred more frequently when we provided bulky foods than when we provided smaller foods. Second, food-sharing was characterized by passive tolerance, rather than active giving, between subjects. Third, subjects shared food primarily with immatures and followed a pattern of reciprocal exchange. Finally, we found no evidence for population-level hand preference for carrying. We posit that an array of behavioral similarities among Cebus, Pan, and Homo evolved through convergent processes, and in this regard capuchins can be seen as an alternative primate model to chimpanzees for the evolution of early hominid behavior.     

First evidence on foot preference during locomotion in Old World monkeys: a study of quadrupedal and bipedal actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

This is the first report of foot preference during locomotion in Old World monkeys. Foot preferences during the quadrupedal walking action and the bipedal shifting action of a naturalistic group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Zhouzhi National Nature Reserve in the Qinling Mountains of China were investigated. Twelve of 21 individuals tested on quadrupedal action and all 21 individuals tested on bipedal action exhibited a significant foot preference. Both significant right- and left-footed preferences were observed; sex affected neither direction nor strength of foot preference in both actions. The finding that 61.90% of focal R. roxellana showed a right-foot preference, both in quadrupedal action based on the footed index and in bipedal action based on the z-score, is in partial agreement with the postural origin hypothesis on footedness. Foot preference was significantly stronger in bipedal action than in quadrupedal action, supporting the view that posture could be a crucial factor influencing foot preference as well as hand preference in this species.     

Hand preference in capuchin monkeys varies with age

The purpose of this research was to examine the influence of age on hand preference in capuchin monkeys (Cebus apella). Twenty-two capuchins, aged 6 months to 30 years, were presented with a task that involved reaching for food and a task that involved using sponging tools to absorb juice. Adults exhibited a greater percentage of right-handed actions in each task than did immature subjects. Adults also exhibited a stronger lateral bias than did immature subjects in the sponging task. These results are consistent with hypotheses: a) adult capuchin monkeys are biased toward use of their right hand for reaching; b) adult capuchins exhibit a greater incidence of right-hand preference than do immature capuchins; and c) primates exhibit age-related differences in the strength and direction of hand preference in tasks that involve the use of tools.     

Hand Preferences in Different Tasks by Tufted Capuchins (Cebus apella)

We examined hand preferences in 25 tufted capuchins (Cebus apella) in three tasks. The hole task involved a single action of reaching for food in a hole. The horizontal panel and the vertical panel tasks required the alignment of two apertures, by moving or lifting a panel, to reach for food in a hole. We found a significant group-level right-hand preference for reaching actions in the hole and in the horizontal panel tasks, but not in the vertical panel task, in which the food retrieval implied the complementary use of both hands. No significant hand bias emerged for moving or lifting actions with high visuospatial components. There is a stronger hand preference in more complex manual activity—coordinated bimanual hand use for food retrieval—than in other unimanual measures. We discuss the results in the context of previous reports on primate laterality.     

Ant-Gathering with Tools by Captive Tufted Capuchins (Cebus apella)

We examined ant-gathering with tools by captive tufted capuchins (Cebus apella) via two experiments. In Experiment 1, we provided groups of subjects with sticks and small branches and an apparatus that accommodated the use of tools to gather ants. In Experiment 2, we sealed the apparatus with acetate and provided the same subjects with sticks and stones. Seven of 14 subjects used sticks and leaves as probes to extract ants from the apparatus. Six of them modified probes by detaching sticks from larger branches, breaking sticks into two or more pieces, and subtracting leaves and bark. Three subjects later used a stone and stick tool-set to penetrate acetate barriers and to extract ants. These results demonstrate the use of tools by Cebus to capture moving prey and are consistent with the idea that sensorimotor skills associated with the production and use of tools in primates evolved convergently in capuchins and great apes.     

Modification of Clay Forms by Tufted Capuchins (Cebus apella)

We examined modification of clay forms by tufted capuchins (Cebus apella) by presenting groups of subjects with clay, paint, stones, leaves, and sticks. In Experiment 1, 7 of 10 subjects reshaped portable forms with their hands and with stones, and decorated them with leaves and paint. In Experiment 2, 9 subjects marked clay slabs manually and with stick and stone tools. The manipulative propensities of Cebus can help us to understand psychological processes that underlie artistic expression in Homo and Pan.     

Pestle use and modification by tufted capuchins (Cebus apella)

We examined the use and modification of pestles by tufted capuchins (Cebus apella). In each of two experiments we presented 18 subjects with an apparatus that held sugarcane along with materials that the animals could use as tools. In Experiment 1 we presented the subjects with sticks, and in Experiment 2 we presented them with sticks, stones, paper towels, and food biscuits. Seven subjects used sticks as pestles to break down fiber to and squeeze sap from sugarcane in Experiment 1. Five of them modified sticks for this purpose. In Experiment 2, 10 animals used pestles and sponges, combined tools, and used pestles to mix together different kinds of food. These results provide further evidence of functional convergence for the use and modification of tools byCebus andPan and are consistent with the view that extractive foraging is associated with the tool-using and toolmaking behavior of primates.     

Problem-Solving Strategies and Hand Preferences for a Multicomponent Task by Tufted Capuchins (Cebus apella)

We examined hand preferences in 23 tufted capuchins (Cebus apella) in 2 tasks requiring the lid of a box to be lifted before taking out a peanut. The first task, Box 1, could entail either 2 or 3 problem-solving acts, with the 3-act solution involving bimanual coordination for food retrieval. The second task, Box 2, involved only the 3-act solution. The results indicated that the types of solution employed to perform the task influenced capuchin hand preferences. In the 2-act solution, capuchins exhibited a significant right-hand bias for the final one-handed reaching action, but not for the initial lid lifting action. In contrast, in the 3-act solution, no significant asymmetry emerged for any act. We noted a significant effect of subject's sex on the strength of laterality, with males being more strongly lateralized than females. We discuss results in the light of recent models of primate laterality.     

The use of probing tools by tufted capuchins (cebus apella): evidence for increased right-hand preference with age

We examined hand preference in the use of tools by tufted capuchins (Cebus apella). We presented a colony of monkeys with an enclosed container designed to accommodate the use of probing tools. Over an 8-month period, 13 monkeys used probes to extract sweet syrup from the narrow opening of the apparatus. Five monkeys exhibited bias toward use of their right hand and eight monkeys exhibited bias toward use of their left hand. Adult monkeys exhibited a greater percentage of right-hand preferent probing sequences than did juveniles. These results are consistent with hypotheses that in tasks that involve the use of tools, nonhuman primates exhibit strong lateral asymmetries at the individual level, a moderate left-hand bias at the population level, and increased bias with age toward use of the right hand.     

Canine Dimorphism and Interspecific Canine Form in Cebus

I investigated canine dimorphism and interspecific canine form in adult specimens from 4 capuchin species (Cebus albifrons, C. apella, C. capucinus, and C. olivaceus). I used various univariate and multivariate statistics, which are based on 6 variables, to test several hypotheses that are based upon the finding that canine dimorphism is strongly associated with intermale competition in platyrrhines (Kay et al., 1988), Greenfield (1992a), Plavcan and van Schaik (1992, 1994). Results from the indices of canine dimorphism and the unpaired t-tests corroborate the prediction that males of each species possess significantly larger canines than those of females. Large male canines are especially prominent in 2 variables, maxillary and mandibular canine height. Greene's t-test (1989) does not support the prediction that Cebus apella and C. olivaceus possess a larger degree of canine dimorphism relative to C. albifrons and C. capucinus. No interspecific differences in degree of canine dimorphism are indicated by this test. Results of the discriminant function analyses (DFA) do not find that Cebus apella and C. olivaceus possess different canine form relative to C. albifrons and C. capucinus as predicted. However, Cebus apella is differentiated from the untufted capuchins (C. albifrons, C. capucinus, and C. olivaceus) by the DFA. I suggest that intermale competition is the primary selective force underlying the observed morphological patterns; however, it does not explain all the variation associated with canine dimorphism in Cebus.     

Hand preferences for a haptic searching task by tufted capuchins (Cebus apella)

We tested the effects of a haptic search task on hand preferences in capuchins(Cebus apella) and compare this situation to a visual by guided reaching task. In the haptic task, 21 monkeys searched for sunflower seeds on the top or side surfaces of 12 objects. A left-hand preference emerged at the group level, suggesting a greater involvement of the right hemisphere. The percentage of preferred hand usage and the direction of the preference were influenced by both sex and age of the subjects: adult males tended to be less lateralized than the other groups of subjects were. Shape had an insignificant effect on the direction of hand preferences or on the percentage of preferred hand use. No lateral bias emerge in the visually guided reaching task, and the percentage of left-hand usage fell significantly across tasks, demonstrating that the haptic demands of the task enhance the use of the left hand at the group level. We discuss these results with regard to current theories on manual lateralization in nonhuman primates.     

Kinematic analysis of bipedal locomotion of a Japanese macaque that lost its forearms due to congenital malformation

Spontaneously acquired bipedal locomotion of an untrained Japanese monkey (Macaca fuscata) is measured and compared with the elaborated bipedal locomotion of highly trained monkeys to assess the natural ability of a quadrupedal primate to walk bipedally. The subject acquired bipedalism by himself because of the loss of his forearms and hands due to congenital malformation. Two other subjects are performing monkeys that have been extensively trained for bipedal posture and locomotion. We videotaped their bipedal locomotion with two cameras in a lateral view and calculated joint angles (hip, knee, and ankle) and inertial angle of the trunk from the digitized joint positions. The results show that all joints are relatively more flexed in the untrained monkey. Moreover, it is noted that the ankle is less plantar flexed and the knee is more flexed in mid-to-late stance phase in the untrained monkey, suggesting that the trunk is not lifted up to store potential energy. In the trained monkeys, the joints are extended to bring the trunk as high as possible in the stance phase, and then stored potential energy is exchanged for kinetic energy to move forward. The efficient inverted pendulum mechanism seems to be absent in the untrained monkeys locomotion, implying that acquisition of such efficient bipedal locomotion is not a spontaneous ability for a Japanese monkey. Rather, it is probably a special skill that can only be acquired through artificial training for an inherently quadrupedal primate.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Transfer of tools and food between groups of tufted capuchins (Cebus apella)

This research examined tool and food transfer between two groups of tufted capcuhin monkeys (Cebus apella). Subjects in one group transferred stones to subjects in a second group who in turn used the stones as cutting tools and then transferred food to subjects in the first group. Aspects of the capuchins' behavior are similar to those described for food-sharing in Cebus, cooperative tool use in Papio, and tool and food exchange in Pan. We propose that tool use and food-sharing facilitate tool and food transfer between captive groups of Cebus apella. Am. J. Primatol. 43:33–41, 1997. © 1997 Wiley-Liss, Inc.     

Locomotion in ornithischian dinosaurs: an assessment using three‐dimensional computational modelling

Ornithischian dinosaurs were primitively bipedal with forelimbs modified for grasping, but quadrupedalism evolved in the clade on at least three occasions independently. Outside of Ornithischia, quadrupedality from bipedal ancestors has only evolved on two other occasions, making this one of the rarest locomotory transitions in tetrapod evolutionary history. The osteological and myological changes associated with these transitions have only recently been documented, and the biomechanical consequences of these changes remain to be examined. Here, we review previous approaches to understanding locomotion in extinct animals, which can be broadly split into form–function approaches using analogy based on extant animals, limb‐bone scaling, and computational approaches. We then carry out the first systematic attempt to quantify changes in locomotor muscle function in bipedal and quadrupedal ornithischian dinosaurs. Using three‐dimensional computational modelling of the major pelvic locomotor muscle moment arms, we examine similarities and differences among individual taxa, between quadrupedal and bipedal taxa, and among taxa representing the three major ornithischian lineages (Thyreophora, Ornithopoda, Marginocephalia). Our results suggest that the ceratopsid Chasmosaurus and the ornithopod Hypsilophodon have relatively low moment arms for most muscles and most functions, perhaps suggesting poor locomotor performance in these taxa. Quadrupeds have higher abductor moment arms than bipeds, which we suggest is due to the overall wider bodies of the quadrupeds modelled. A peak in extensor moment arms at more extended hip angles and lower medial rotator moment arms in quadrupeds than in bipeds may be due to a more columnar hindlimb and loss of medial rotation as a form of lateral limb support in quadrupeds. We are not able to identify trends in moment arm evolution across Ornithischia as a whole, suggesting that the bipedal ancestry of ornithischians did not constrain the development of quadrupedal locomotion via a limited number of functional pathways. Functional anatomy appears to have had a greater effect on moment arms than phylogeny, and the differences identified between individual taxa and individual clades may relate to differences in locomotor performance required for living in different environments or for clade‐specific behaviours.     

Energetic costs of bipedal and quadrupedal walking in Japanese macaques

We investigated the energetic costs of quadrupedal and bipedal walking in two Japanese macaques. The subjects were engaged in traditional bipedal performance for years, and are extremely adept bipeds. The experiment was conducted in an airtight chamber with a gas analyzer. The subjects walked quadrupedally and bipedally at fixed velocities (<5 km/hr) on a treadmill in the chamber for 2.5-6 min. We estimated energy consumption from carbon dioxide (CO2) production. While walking bipedally, energetic expenditure increased by 30% relative to quadrupedalism in one subject, and by 20% in another younger subject. Energetic costs increased linearly with velocity in quadrupedalism and bipedalism, with bipedal/quadrupedal ratios remaining almost constant. Our experiments were relatively short in duration, and thus the observed locomotor costs may include presteady-state high values. However, there was no difference in experimental duration between bipedal and quadrupedal trials. Thus, the issue of steady state cannot cancel the difference in energetic costs. Furthermore, we observed that switching of locomotor mode (quadrupedalism to bipedalism) during a session resulted in a significant increase of CO2 production. Taylor and Rowntree ([1973] Science 179:186-187) noted that the energetic costs for bipedal and quadrupedal walking were the same in chimpanzees and capuchin monkeys. Although the reason for this inconsistency is not clear, species-specific differences should be considered regarding bipedal locomotor energetics among nonhuman primates. Extra costs for bipedalism may not be great in these macaques. Indeed, it is known that suspensory locomotion in Ateles consumes 1.3-1.4 times as much energy relative to quadrupedal progression. This excess ratio surpasses the bipedal/quadrupedal energetic ratios in these macaques.     

Kinematics and energetics of nut-cracking in wild capuchin monkeys (Cebus libidinosus) in Piauí, Brazil

Wild bearded capuchins (Cebus libidinosus, quadrupedal, medium-sized monkeys) crack nuts using large stones. We examined the kinematics and energetics of the nut-cracking action of two adult males and two adult females. From a bipedal stance, the monkeys raised a heavy hammer stone (1.46 and 1.32 kg, from 33 to 77% of their body weight) to an average height of 0.33 m, 60% of body length. Then, they rapidly lowered the stone by flexing the lower extremities and the trunk until the stone contacted the nut. A hit consisting of an upward phase and a downward phase averaged 0.74 s in duration. The upward phase lasted 69% of hit duration. All subjects added discernable energy to the stone in the downward phase. The monkeys exhibited individualized kinematic strategies, similar to those of human weight lifters. Capuchins illustrate that human-like bipedal stance and large body size are unnecessary to break tough objects from a bipedal position. The phenomenon of bipedal nut-cracking by capuchins provides a new comparative reference point for discussions of percussive tool use and bipedality in primates.     

Laterality of Hand Function in Tufted Capuchin Monkeys (Cebus apella): Comparison between Tool Use Actions and Spontaneous Non-tool Actions

This study examined hand preference for tool use and spontaneous non-tool actions in tufted capuchin monkeys (Cebus apella). We noted a lack of lateral bias across measures, and greater strength of hand preference for tool use than for self-directed or feeding activities. Animals that used tools exhibited a population-level right-hand bias for self-touching whereas animals that did not use tools exhibited a lack of lateral bias for this measure. Our findings are consistent with views that hand preference is expressed more strongly for tool use than for non-tool activities, and that lateral bias for self-directed behavior is related to problem-solving skills in primates.     

Using the Tools at Hand: Manual Laterality and Elementary Technology in Cebus spp. and Pan spp.

Cebus and Pan appear to be a remarkable example of evolutionary convergence in behavioral ecology. We examine their apparently analogous solutions to problems posed by laterality of hand function and elementary technology. We scrutinize appropriate published data in a meta-analysis, focusing on Cebus apella and C. capucinus and on Pan paniscus and P. troglodytes. We compare behavioral data in terms of captive versus wild, and tool use versus non-tool use, but notable gaps exist in the data, especially for bonobos. Cebus and Pan spp. are equivalent tool users in captivity, but chimpanzees are notably more extensively so in nature. For hand preference, captive bonobos and wild and captive chimpanzees show ambipreference for non-tool-use patterns. For both Cebus spp. and Pan spp., there is a tendency for individuals to be committed exclusively to one hand or the other for tool use. The data for laterality of hand function fit consistently into the five-level model proposed by McGrew and Marchant (1996).     

The advantage of standing up to fight and the evolution of habitual bipedalism in hominins

Background

Many quadrupedal species stand bipedally on their hindlimbs to fight. This posture may provide a performance advantage by allowing the forelimbs to strike an opponent with the range of motion that is intrinsic to high-speed running, jumping, rapid braking and turning; the range of motion over which peak force and power can be produced.

Methodology/Principal Findings

To test the hypothesis that bipedal (i.e., orthograde) posture provides a performance advantage when striking with the forelimbs, I measured the force and energy produced when human subjects struck from “quadrupedal” (i.e., pronograde) and bipedal postures. Downward and upward directed striking energy was measured with a custom designed pendulum transducer. Side and forward strikes were measured with a punching bag instrumented with an accelerometer. When subjects struck downward from a bipedal posture the work was 43.70±12.59% (mean ± S.E.) greater than when they struck from a quadrupedal posture. Similarly, 47.49±17.95% more work was produced when subjects struck upward from a bipedal stance compared to a quadrupedal stance. Importantly, subjects did 229.69±44.19% more work in downward than upward directed strikes. During side and forward strikes the force impulses were 30.12±3.68 and 43.04±9.00% greater from a bipedal posture than a quadrupedal posture, respectively.

Conclusions/Significance

These results indicate that bipedal posture does provide a performance advantage for striking with the forelimbs. The mating systems of great apes are characterized by intense male-male competition in which conflict is resolved through force or the threat of force. Great apes often fight from bipedal posture, striking with both the fore- and hindlimbs. These observations, plus the findings of this study, suggest that sexual selection contributed to the evolution of habitual bipedalism in hominins.