A COMPARISON OF DYNAMIC HAND MOVEMENTS IN CHIMPANZEES (PAN TROGLODYTES) AND CAPUCHIN MONKEYS (CEBUS APELLA) JESSICA L. CRAST

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1 A COMPARISON OF DYNAMIC HAND MOVEMENTS IN CHIMPANZEES (PAN TROGLODYTES) AND CAPUCHIN MONKEYS (CEBUS APELLA) by JESSICA L. CRAST (Under the Direction of Dorothy M. Fragaszy) ABSTRACT The ability to manipulate objects within the hand has been fully described in humans but remains to be documented and described in non-human primates. Studies suggest that several non-human primates are capable of such movements, evidenced by the dexterity of precision handling seen in the foraging and grooming behaviors of Old World primates and Cebus monkeys. Laboratory studies looking at individual control of the digits and neuroanatomy have supported this implication. This study presented a task to elicit in-hand movements in three adult chimpanzees (Pan troglodytes) and six adult capuchin monkeys (Cebus apella). All of the chimpanzees and two of the capuchins performed in-hand movements; the chimpanzees performed a wider variety of these movements and at a higher rate. The chimpanzees thus demonstrated more sophisticated control and coordination of the digits than the capuchins. The findings suggest behavioral consequences of the muscular, skeletal, and neuroanatomical features of each species. INDEX WORDS: manual dexterity, manual function, hand movements, non-human primates, chimpanzee, capuchin, precision handling, dynamic movements

2 A COMPARISON OF DYNAMIC HAND MOVEMENTS IN CHIMPANZEES (PAN TROGLODYTES) AND CAPUCHIN MONKEYS (CEBUS APELLA) by JESSICA L. CRAST BA, Alfred University, 2003 A Thesis Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree MASTER OF SCIENCE ATHENS, GEORGIA 2006

3 2006 Jessica L. Crast All Rights Reserved

4 A COMPARISON OF DYNAMIC HAND MOVEMENTS IN CHIMPANZEES (PAN TROGLODYTES) AND CAPUCHIN MONKEYS (CEBUS APELLA) by JESSICA L. CRAST Major Professor: Committee: Dorothy M. Fragaszy Irwin Bernstein Kathy Simpson Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia May 2006

5 iv ACKNOWLEDGEMENTS First, I would like to thank my advisor, Dr. Dorothy Fragaszy, for her guidance, patience, and expertise on this project. I have gained so much from her instruction and support in my graduate career thus far. I would also like to thank my committee members, Dr. Irwin Bernstein and Dr. Kathy Simpson for their assistance in the development and completion of my Masters thesis, it is much improved by their suggestions. I thank my family for their constant moral support, encouragement and praise throughout my entire education: my parents Larry and Patty Crast; my brother Tom Crast; my grandparents Bill and Nancy Parody, Bruce and Shirley Crast, I love all of you very much. Finally, I thank my friends and colleagues in graduate school for their advice, help, and friendship: Lisa Renzi, Carrie Rosengart, Erica Hoy Kennedy, Tannia Gutierrez, Tephillah Jeyaraj, Qing Liu, Katie Leighty, Michael Gumert, Michael Engles, Jenny Reiss, and Sarah Eisenstein.

6 v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS...v LIST OF TABLES... vii LIST OF FIGURES... viii CHAPTER 1 INTRODUCTION...1 The Primate Hand...1 Primate Hand Anatomy...2 Primate Hand Function...6 Conclusions and Predictions METHODS...15 Subjects...15 Materials...15 Experimental Setting and Procedure...16 Coding Hand Movements...19 Data Analysis RESULTS...25 Frequency and Percent of Total movements...25 Surface-brace and Assistance...26 In-depth Analysis of Movement DISCUSSION...32

7 vi General Discussion...32 Digital Independence and Hand Coordination...34 Classifying Chimpanzee and Capuchin Hand Movements...36 Encountered Problems...36 Next Steps...38 REFERENCES...41

8 vii LIST OF TABLES Page Table 1: Synonymous Terminology Used to Describe Static Grasping Patterns in Humans...44 Table 2: Synonymous Terminology Used to Describe Static Grasping Patterns in Great Apes...45 Table 3: Number of Trials Each Subject Performed With Each Object (Condition)...46 Table 4: The Number of Trials of Each Condition that were Scored for All Subjects...47 Table 5: Categories of Hand Movements, Coded Behaviors, and their Definitions...48 Table 6: Number of Trials, the Summed Trial Durations (in Seconds), the Average Trial Length (in Seconds), and the Total Number of Movements Performed Across All Trials for Each Subject...49 Table 7: Average Rate of Movements per Minute (Original Data and Transformed Data); Variance in the Original and Transformed Data for Each Species...50 Table 8: Frequency and Percent of Movements (in Parentheses) Performed Within Each Category...51 Table 9: Ways in Which Object was Braced Against the Surface of the Panel...52

9 viii LIST OF FIGURES Page Figure 1: Posterior View of the Human Hand Skeleton...53 Figure 2a: Relative Sizes of the Panels and Objects Used by the Chimpanzees...54 Figure 2b: Relative Sizes of the Panels and Objects Used by the Capuchins...54 Figure 3a: Chimpanzee Holding Circle Object in a Tripod Grasp...55 Figure 3b: Capuchin Holding Circle Object in a Pinch Grasp...55 Figure 4a: Chimpanzee Ai Inserting the Circle Object Toward the Tester...56 Figure 4b: Capuchin Monkey Chris Holding the Circle Object...56 Figure 5: Examples of Simultaneous Convergent Movements...57 Figure 6: Illustration of a Roll...58 Figure 7: Illustration of a Turnover...59 Figure 8: Frequency of In-hand Movements: Simultaneous Divergent Movements (SDV) and Sequential Movements (SQM)...60 Figure 9: Diagram of Human Hand...61

10 1 CHAPTER 1 INTRODUCTION The Primate Hand Hands, unique to the Primate Order, are our primary tools for manipulating and interacting with the environment and it is speculated that such enhanced manipulative abilities are linked with the evolution of bipedalism, brain enlargement, and language in humans (Wilson, 1999). The primate hand possess five digits (with the exception of the genera Ateles and Colobus, which have vestigial thumbs due to locomotor adaptations), at least one fingernail, and papillary ridges, or fingerprints, which enhance grip and facilitate unique foraging and locomotion styles in primates. Primates are able to grasp and manipulate objects at a distance from the body (Fragaszy, 1998), affording safer manipulation of prey and increased visual and sensory information. Primates achieve these daily tasks through the use of a variety of grips and hand movements. In the 1950 s, Napier and Napier first described two main prehensile grip types used by human and non-human primates, the power grips and precision grips, which are achieved by thumb opposition (Napier and Napier, 1985). Napier and Napier (1985) define thumb opposition as pad-to-pad contact of the thumb with one or all of the remaining digits. Humans display a large repertoire of grip types and static hand postures that have been named and categorized by a multitude of researchers in the fields of biomechanics, comparative anatomy, and occupational therapy. Humans frequently use skilled finger movements to accomplish delicate tasks, such as manipulating small objects within the hand to reorient their position for better grip or alignment. Elliott and Connolly (1984) defined such in-hand movements as intrinsic movements of the

11 2 hand. Elliott and Connolly are among the few scientists who have systematically looked at dynamic movement in human hand function. A richer understanding of dynamic hand movements will undoubtedly assist those in the above-mentioned fields, especially occupational therapy. To gain a comprehensive knowledge of dynamic hand movements, such as how these movements are coordinated, intrinsic movements of the hand must also be investigated in human counterparts the non-human primates. Field and laboratory studies have revealed that many non-human primates are capable of a wide variety of static grips, most notably in great apes, Old World monkeys and Cebus monkeys (Marzke and Wullstein, 1996; Byrne and Corp, 2001; Maier, 1993; Tanaka, 1998; Costello and Fragaszy, 1988). Their variability and flexibility in grasping and manipulative actions in foraging, grooming, and tool-using behaviors imply that these primates may have much richer manual repertoires than previously attributed. Until this point, their ability to perform intrinsic movements of the hand has not been systematically explored. The current study investigates this capability in two non-human primates: chimpanzees (Pan troglodytes) and capuchin monkeys (Cebus apella). These two species are distantly related, yet share several characteristics that indicate that both species are capable of in-hand movements. The following overview of primate hand anatomy, function, and neuroanatomical specializations illustrates both similarities and differences in the two species and provides the basis for this prediction. Primate Hand Anatomy Skeletal and Joint Anatomy The basic skeletal and joint anatomy of the hand is relatively consistent across the Primate Order, thus the human hand provides a good descriptive reference. As shown in Figure

12 3 1, the human hand is comprised of 27 bones: eight carpal, or wrist bones; five metacarpal, or palm bones; and 14 phalanges, or finger bones (Napier, 1993 Rev. Ed). Each digit contains three phalanges, except the first digit (thumb), which contains two. The bones of the hand articulate with one another through synovial joints, which are enclosed in capsules of lubricating and nourishing fluid and controlled by muscles and ligaments (Napier, 1993 Rev. Ed). Between the carpals and metacarpals are the carpometacarpal joints. The articulations between the metacarpals and phalanges are the metacarpalphalangeal (MP) joints. Between the phalanges are the proximal and distal interphalangeal (PIP and DIP) joints (Behnke, 2001). Apes and Old World monkeys, like humans, possess a saddle joint at the first metacarpal joint of the thumb, which functions like a ball and socket (Napier and Napier, 1985) allowing it to rotate, though certain joint motions are constrained. New world monkeys, such as Cebus monkeys, possess a hinge joint which does not permit the same degree of rotation or types of movement of the thumb (Christel and Fragaszy, 2000). However, because New World monkeys have relatively long thumbs and short fingers, comparable to the proportions of the human hand (Napier and Napier, 1967), and the abductor pollicis brevis muscle (Rose, 1992 as cited by Fragaszy, Visalberghi, and Fedigan, 2004), they are capable of achieving a pseudo-opposable precision grip (Napier and Napier, 1985). In the capuchin, the pseudo-opposable grip is functionally equivalent to several precision grips achieved by humans, apes and Old World monkeys. It is achieved between the distal pad of the index finger and the side or nail of the thumb (Fragaszy, 1998), whereas primates with a saddle joint can achieve a relatively large area of pad-to-pad contact between the pulp surfaces of the thumb and index finger.

13 4 Muscular Anatomy The muscles that control the primate hand originate in the arm (extrinsic muscles) and within the hand (intrinsic muscles). Most of the muscles that control the human hand have correlates in non-human primate hands, with differences primarily being the locations and extent to which the muscles split to insert on metacarpal and phalangeal bones. Major extrinsic muscles (originating from the epicondyle of the humerus, the ulna, and the radius) include the common flexor tendon four muscles that stretch across the anterior surface of the forearm, and the common extensor tendon four muscles that stretch across the posterior surface of the forearm (Behnke, 2001). In Cebus monkeys, the flexor musculature splits into the tendons of phalanges 1-5 below the carpal bones, whereas the chimpanzee flexor musculature separates into two muscles in the forearm above the carpal bones, one that extends to and inserts on phalanges 1 and 2, and the other that extends to and inserts on phalanges 3-5 (Lewis, 1989). The muscles that extend to phalanges 1 and 2 in Pan are the flexor pollicis longus, important for flexion of the thumb, and a portion of the flexor digitorum profundus, important for flexion of the index digit. These two muscles separate below the carpal bones in Pan. The flexor pollicis longus is more slender in both Cebus and Pan than in humans. However, in Cebus, it is completely part of the common flexor muscle sheet, whereas in Pan it deviates with a portion of the flexor digitorum profundus, as described above (Lewis, 1989). In humans, the flexor pollicis longus is completely split from the common flexor muscle sheet and the index portion of the flexor digitorum profundus above the carpal bones; the two muscles extend independently to insert on phalanges 1 and 2. The increased deviation and elaboration implies greater muscular control of digits 1 and 2 in chimpanzees, and even further control in humans (Lewis, 1989), indicating that chimpanzees and humans have a greater ability to individually control these digits than Cebus monkeys. Thus,

14 5 it is possible that chimpanzees and humans have more in common with each other, in terms of hand movements and object manipulation, than they do with capuchin monkeys. In humans, extrinsic muscles that are also important for thumb movement are the extensor pollicis longus, the extensor pollicis brevis, and the abductor pollicis longus (Behnke, 2001). These muscles are responsible for the extension and abduction of the thumb (spreading thumb away from the midline of the hand). The abductor pollicis longus is very similar in Cebus and Pan, however the extensor pollicis longus and brevis are highly variable in hominoids. The extensor pollicis longus is independent of the profundus (deep) extensor musculature in hominoids, and the homologous muscle in Cebus is described as independent as well (Lewis, 1989). In humans, the extensor pollicis brevis inserts at the base of the proximal phalanx and assists thumb motion by extension at the metacarpophalangeal joint (Behnke, 2001). The extensor pollicis brevis is absent in New World Monkeys and most Old World primates, however a rudimentary form exists in Pan that doesn t quite reach the proximal phalanx (Lewis, 1989). It is possible that its absence or reduced form in non-human primates lessens the degree of thumb movement and control compared to humans. Intrinsic muscles of the hand are involved with movement of the phalangeal joints and include three muscles that move the fifth digit (the little finger); the interossei, which are the muscles between the phalangeal bones that are responsible for abduction and adduction (spreading and closing) the digits; and the lumbricals, which assist with the flexion of the MP joints and the extension of the PIP and DIP joints (Behnke, 2001). The intrinsic muscles of the hand are also important for individuation of the digits (Pehoski, 1992), and are described as more specialized and clearly defined in humans compared to non-human primates (Lewis, 1989). Also, Lewis (1989) describes some intrinsic musculature in chimpanzees, such as the transverse lamina

15 6 (an interosseous muscle), as more homologous than Cebus monkeys to human musculature. In humans, intrinsic muscles that are important for thumb opposition are the abductor pollicis brevis, the flexor pollicis brevis, the opponens pollicis, and the adductor pollicis brevis (Behnke, 2001). These muscles are very similar in non-human primates, with the exception of the opponens pollicis in New World monkeys, which is referred to by Lewis (1989) as the opponens pollicis subdivision. In Cebus, this muscle is more complex than the primitive condition found in marsupial mammals, but it is further augmented in hominoids (Lewis, 1989). It is possible that the lesser developed opponens pollicis reduces New World monkeys ability to oppose the thumb, compared to apes and humans. However, the extent to which these differences in musculature in humans and non-human primates (as discussed in this section) influence differences in hand function is unclear. Primate Hand Function Static Hand Postures in Humans Several classification systems have been created to describe the variety of grips and grasps used by the human hand based on Napier and Napier s initial descriptions of the power and precision grips. The power grip is used when grasping large objects in the palm and when force is needed to stabilize an object, the thumb is used for directional control. The precision grip is used for fine control and accuracy in object manipulation and is executed between the pulp surfaces of the thumb and fingertips. Napier and Napier defined two other prehensile grips that do not involve thumb opposition (Napier and Napier, 1985). The hook grip involves flexion of the four fingers, as in holding a suitcase, and the scissor grip involves adduction and abduction of the second two digits (the index and middle fingers), grasping an object between the two.

16 7 Elliott and Connolly (1984) created a system to describe human hand movements, including grasps. While the grasps are named and described in terms of movement (like the movement of the digits when plunging a syringe), the final positions of the digits are static grasps. Elliott and Connolly (1984) define prehensile movements that involve the digits converging simultaneously as simple synergies and name three types: a pinch, involving thumb and index finger opposition; a dynamic tripod, in which the thumb opposes both the index and middle fingers; and a squeeze, in which the thumb opposes all digits. In simple synergies, all digits converge simultaneously to grasp. This system simply and concisely describes basic precision grips and in-hand movements, and is therefore the model from which the present study s classification system was developed. Many researchers have created their own taxonomies to name and describe the variety of grip types performed by humans. The various proposed taxonomies are summarized in Table 1, which depicts the synonymous terminology used to refer to the same grip types. Table 1 presents terminology in columns from left to right starting with Napier s (1985) categories, from which later classification systems were derived, going to Elliott and Connolly s (1984) categories, which the present study s classification system is derived, and finally to categories put forth by Kamakura, Matsuo, Ishii, Mitsuboshi, and Miura (1980) and Wong and Whishaw (2004), which provide further examples of the terminology that is used to describe human grip types. Static Hand Postures in Non-Human Primates As in studies of human grip types, several researchers have developed classification systems to name and describe the grip types used by non-human primates. Table 2 depicts the synonymous terminology used in various studies to refer to the same grip types in studies involving great apes. From left to right is that of Napier and Napier (1985), upon which all later

17 8 classification systems are based, Marzke and Wullstein (1996), who observed manual function in captive chimpanzees manipulating a variety of objects in their environment, Byrne and Corp (2001), who observed wild gorillas foraging, and Tonooka and Matsuzawa (1996), who observed captive chimpanzees reaching for and picking up raisins. By comparing these grip types with those from Table 1, one can see that humans and great apes share many static grip types. For example, Marzke and Wullstein s (1996) Cup Hold and Byrne and Corp s (2001) Power-grip and Squeeze-grip are equivalent to Elliott and Connolly s (1984) Squeeze and Kamakura, et al. s (1980) Power Grip category. Byrne and Corp s (2001) Pencil-grip and Tonooka and Matsuzawa s (1996) Radial-Palmar Grasp are equivalent to Elliott and Connolly s (1984) Dynamic Tripod and Wong and Whishaw s (2004) Triangular Grasp. Cebus monkeys have also demonstrated the use of a variety of precision grips (Costello and Fragaszy, 1988). Most New World monkeys and prosimians have whole hand control (Bishop, 1964; Schoneich, 1993), with the exception of the genus Cebus, which is the only genus of New World monkeys known to exhibit manual dexterity similar to apes and Old World monkeys (Costello and Fragaszy, 1988; Fragaszy, 1998). Cebus monkeys use tools in the wild (Fragaszy, Izar, Visalberghi, Ottoni, and Gomes de Oliveira, 2004) and in captivity and are extractive foragers (Fragaszy, 1998). Costello and Fragaszy (1988) compared the manipulative abilities of two species of New World monkeys, Cebus (capuchin monkeys) and Saimiri (squirrel monkeys) when grasping small food items. Costello and Fragaszy observed nine types of precision grips in capuchin monkeys, whereas Squirrel monkeys used only whole hand power grips. Costello and Fragaszy suggest that manipulative abilities in Cebus are an adaptation to their extractive style of foraging, and that capuchin monkeys can integrate sensory-motor information to a higher degree than other New World monkeys (1988). Thus, it is possible that

18 9 there is some degree of convergent evolution in manual function between two New and Old World primate lineages, due to similar ecological pressures and foraging techniques (Fragaszy, Visalberghi, and Fedigan, 2004). In-hand Movements A large part of human hand function involves the ability to manipulate objects within the hand. Humans routinely handle objects within the hand when fine manipulation of objects is necessary (Elliott and Connolly, 1984), as in using utensils to eat or when handling small objects like bolts and nails. A few researchers have investigated these movements in humans, namely Elliott and Connolly (1984) and Exner (1992). Their classifications describe the action of the digits to change an object s position within the hand. Elliott and Connolly (1984) divide hand movements into simultaneous and sequential movements. Simultaneous movements are further divided into simple and reciprocal synergies, or patterns of movement. As described above, simple synergies describe the prehension of objects using a pinch, tripod or squeeze technique (see Table 1). Once an object is prehended, the digits involved in the pinch, tripod or squeeze can flex and extend to move the object through space. Reciprocal synergies also involve movement of the digits after prehension to move the object about one of its axes. These movements include a twiddle, rock, and several types of rolls, all of which involve the thumb moving in the opposite direction of one or more other digits simultaneously, such as twisting a bolt or rolling a ball of clay. Sequential patterns of movement involve all of the digits moving independently and in sequence in order to rotate or turn an object. Examples include turning a pen from end to end or turning a large dial with the fingers alone, not using any wrist, elbow or shoulder movement. Elliott and Connolly also describe a pattern of movement called a Palmar Combination, in which

19 10 an object is stabilized in the palm and intrinsic movements are used to manipulate part of the object, as in pushing off a pen cap. Exner (1992) describes three categories of in-hand movement: translation (finger-to-palm and palm-to-finger), shift, and rotation (simple and complex). Translation of an object is a movement of an object from the fingers to the palm or from the palm to the fingers, as in picking up a small object and hiding it in the palm. To shift an object in the hand, a grip is maintained while the thumb and fingers flex and extend to slide the object to a new and better position for use. An example is moving the fingers down a pen for a better grip to write. Rotation of an object within the hand involves movement of the object along one or more of its axes. A simple rotation corresponds with Elliott and Connolly s (1984) rolls; Exner describes a simple rotation as turning or rolling an object through alteration between the thumb and finger movements. A complex rotation involves independent movements of the digits and the object turning between 180 and 360 degrees. These hand movements are described with and without the subject holding another object within the same hand. Exner s categories best correspond with Elliott and Connolly s reciprocal synergies and sequential patterns, as these movements require the movement of digits after prehension, and the object turning about some axis by the action of the fingers. Although in-hand movements in non-human primates have not been explicitly investigated, a few laboratory studies provide evidence that Old World primates may have this capability. While Marzke and Wullstein (1996) did not attempt to elicit in-hand manipulation of the objects used in their study, they were open to the possibility of spontaneous in-hand manipulations occurring but did not observe any. The chimpanzees were, however, observed extending the index finger alone to probe or hook objects. It is possible that the objects the

20 11 chimpanzees used in Marzke and Wullstein s study did not promote the use of in-hand movements. Capuchin monkeys have also been documented probing a single index finger into holes (Fragaszy, 1998). Schieber (1991) has shown that macaques possess independent control of the digits, particularly the thumb and index finger. Schieber s research supports the macaque s propensity to use a precision grip in natural behaviors, but did not explore their ability to use digital independence in object manipulation. While these studies do not demonstrate dynamic hand movements, they imply the possibility of such capabilities by demonstrating individual control of one or more of the digits. Many field studies refer to primates using their hands dexterously in the wild, as in the foraging strategies of capuchin monkeys, apes and geladas, the grooming techniques of macaques, and the use of tools in chimpanzees and capuchin monkeys described above (Fragaszy, 1998; Byrne and Corp, 2001; Maier, 1993; Tanaka, 1998; Boesch and Boesch, 1993; Fragaszy, et al., 2004, respectively). With the digital independence described in the laboratory studies above, these behaviors suggest the possibility that these primates possess individuated digital control and potentially the ability to manipulate objects within the hand, as described by Elliott and Connolly (1984). In fact, Byrne and Corp (2001) use the phrase intrinsic movements of the hand and cite Elliott and Connolly s descriptions of in-hand movements to describe a hand movement used by gorillas when foraging, called digital role differentiation. Digital role differentiation refers to the gorillas moving food from one part of the hand to another in order to grasp new food items and manipulation refers to rearranging the position or shape of items held in one hand by using the fingers alone. Byrne and Corp s (2001) description provides the only documented case of the presence of in-hand movements in a non-human species and draws an explicit comparison between human and non-human primate hand movements.

21 12 Neuroanatomy Building on Byrne and Corp s findings are studies in neuroanatomy in Old World primates and Cebus monkeys that further imply their ability to use in-hand movements. Prehensile movements of the hand are primarily dependent upon the corticospinal tract, which is made up of pyramidal neurons in the cortex that synapse with motoneurons in the spinal cord (Lemon, 1993). Corticospinal neurons that influence hand movement are mostly derived from the primary motor cortex (Lemon, 1993). It has been shown that the extent to which corticospinal neurons make direct connections with motoneurons in the ventral gray area of the spinal cord influences the degree of digital independence a primate species is capable of (Lemon, 1993; Pehoski, 1992). Therefore, as monosynaptic connections between corticospinal neurons and motoneurons extending to the hand increase, manual dexterity increases. In addition, several morphological characteristics of the corticospinal tract have been shown to correspond with sophistication of manual skill. Heffner and Masterson (1983) compared the cross-sectional area of the corticospinal tract (mm 2 ) at the level of the lower medulla in several mammalian species, including both chimpanzees (7.77 mm 2 ) and capuchin monkeys (2.0 mm 2 ). Their findings suggest that the overall size of the corticospinal tract, independent of body size and weight, most highly correlates with the level of digital dexterity that can be achieved. From this it can be inferred that the overall size of the corticospinal tract is correlated with in-hand manipulative abilities as well. Interestingly, the data on the corticospinal tract parameters that Heffner and Masterson (1983) collected showed that capuchin monkeys (Cebus aella) have a relatively large corticospinal tract: the two macaques used in their sample had tract sizes comparable to the capuchin s (Macaca irus, 1.18 mm 2 ; Macaca mulatta, 2.89 mm 2 ), yet the macaques were more than twice the capuchin s body size, indicating that when body size is accounted for, capuchin

22 13 monkeys have a relatively larger corticospinal tract than some Old World primates. Thus, it is possible that capuchin monkeys have the neural equipment for a relatively high level of manual dexterity. Further supporting this hypothesis, Bortoff and Strick (1993) compared the corticospinal tract in two New World monkeys, Cebus and Saimiri and found that capuchin monkeys have three main regions of corticospinal neuron termination in the spinal cord, whereas squirrel monkeys have two, and that the corticospinal neuron terminations in the spinal cord of capuchin monkeys are denser in the ventral horn and more widely distributed in the intermediate zone of the spinal cord. The increased density of terminations increases the likelihood (but does not guarantee or specify quantity) of direct synapses with motor neurons projecting to the hand. The discovery of this neuromuscular specialization in Cebus monkeys provides physical evidence to support speculations that there is convergent evolution of manual dexterity in New and Old World lineages, which may be due to their similar ecology and foraging styles (Costello and Fragaszy, 1988; Fragaszy, Visalberghi, and Fedigan, 2004). Furthermore, these findings suggest the potential ability of capuchin monkeys to manipulate objects within the hand. The density of corticospinal neuron termination in comparable regions of the spinal cord in chimpanzees and humans is not known at this time. Conclusions and Predictions Few studies have looked for dynamic hand movements in non-human primates and only one has noted that the capability is present in a primate species. The neurological research and the skilled precision handling observed in natural behaviors suggest that some manual capabilities in some New and Old World primates have yet to be acknowledged. Specifically,

23 14 Cebus monkeys accomplish many of the same functional outcomes as chimpanzees, as in their methods of extractive foraging and tool-use. Are these behaviors achieved through similar motor abilities, such as in-hand movements? The present study is the first to attempt to elicit the inhand manipulation of small objects in non-human primates and compare the abilities of Cebus monkeys with an Old World primate species: chimpanzees. The objectives of this study were first to document whether chimpanzees and capuchin monkeys are capable of in-hand movements, and if so, to describe and compare the types of movements that were performed, and to consider the cognitive and motor factors that may contribute to similarities and differences in hand function between genera. The subjects were presented with small three-dimensional objects and were requested to insert them into correspondingly-shaped apertures in Plexiglas panels ( cutouts ). Both species were able to solve the task and insert the objects through the cutouts. Both chimpanzees and capuchins were predicted to use in-hand movements when aligning the objects to the cutouts, but to different extents. Due to the nature of the task, static grasps were predicted to account for a large percent of total hand movements for both species. But because chimpanzee neuromuscular anatomy of the forelimb more closely parallels that of humans, it was hypothesized that the chimpanzees would be more adept at in-hand movements and that such movements would be more varied and account for a larger percent of total hand movements than in the capuchins, reflecting more individual control of the digits.

24 15 CHAPTER 2 METHODS Subjects Six adult male capuchin monkeys and three adult female chimpanzees participated in this study. The chimpanzees live at the Primate Research Institute of Kyoto University in Inuyama, Japan. The chimpanzee participants were tested in September, 2001, and included Ai (age 24), Pan (age 17), and Chloe (age 20). The capuchins live at the University of Georgia in Athens, GA, USA, and were tested during the academic year. The capuchins that participated in experimental sessions included Nick, Leo, Chris, Xenon and Xavier, ages Two additional adult male capuchin monkeys (Jobe and Mickey, ages 12 18) participated in pilot testing sessions. Materials Each subject was presented with a set of Plexiglas panels, each with a small cutout of a shape. The chimpanzees equipment included five panels with circular, square, triangular, star and asymmetrical cross cutouts and corresponding three-dimensional objects (Figure 2a illustrates panel and object sizes used by the chimpanzees). The panels were approximately 37 x 27 cm, with a cutout at approximately 13 cm from the sides and 9 cm from the bottom of the panel. The three dimensional objects were made from PVC and were approximately 6 x 3 x 3 cm. The capuchins equipment included three panels with circular, square, and triangular cutouts and corresponding three-dimensional objects. The panels were approximately 36 x 22.5

25 16 cm, each with a cutout at approximately 11.5 cm from the sides and 8.5 cm from the bottom of the panel. The three-dimensional objects were made from stainless steel and were approximately 1 x 1 x 0.5 cm (see Figure 2b). Pilot testing sessions were conducted with the capuchins using panels and objects of a larger size, including circle, square, triangle, and star (sizes approximately 5.5 x 2.5 x 2.5 cm). These objects were used for training and other purposes, but were proportionally too large for their hands and the smaller objects were used during experimental testing sessions. All of the three-dimensional objects fit through the appropriate cutouts with approximately 1 mm clearance and were designed to be an appropriate size for each species to grasp and manipulate comfortably (Figure 3a and 3b illustrate the relative object sizes within the hands of the chimpanzees and capuchins). Each object constituted a different experimental condition to enhance the probability of eliciting in-hand movements, as each object was predicted to vary in its level of difficulty in alignment. Chimpanzee sessions were recorded with a Sony digital camcorder and capuchin sessions were recorded with either one or both Canon or Panasonic digital camcorders. Experimental Setting and Procedure The chimpanzees at the Primate Research Institute voluntarily came inside the building through tunnels to a large testing booth with transparent Plexiglas windows to participate in this study. While participating in the task, the chimpanzees sat face-to-face with the human experimenter inside the booth (see Figure 4a). The experimenter held the Plexiglas panels vertically on the floor of the booth between himself and the chimpanzee and either passed the

26 17 chimpanzee the object though the cutout or placed the object on the floor and allowed the chimpanzee to pick it up and begin attempting to insert the object towards the experimenter. The capuchins were moved from their home cages to a transparent Plexiglas testing box (approximately 1 x 1.5 x 1 m). The experimental panels constituted one portion of a side wall of the testing box; the bottom edge of the panel rested approximately 10 cm from the floor of the testing box. The experimenter passed the objects to the capuchins through the cutout or through a small aperture in an upper corner of the testing box (see Figure 4b). The subjects were requested to align and insert three-dimensional objects corresponding to each cutout through the panel to the experimenter. All of the subjects were familiarized with this procedure prior to testing. Trials began with the circle because it is the easiest to align and pass through the cutout. Trials loosely followed the following object order: circle, triangle, square, star and cross. This order was predicted to follow the difficulty of inserting the objects through the cutout as the number of discrete angles increased. Cross was typically the last trial presented in a given testing session as it was the only object that was asymmetrical in one plane and most difficult to pass through the cutout. The capuchins did not receive the star and cross objects because they had difficulty passing them through the panel in preliminary trials and the other objects elicited sufficient activity. In both species, subjects varied individually in their reaction to difficulty of the task and experimenters decided to move to the next condition according to the subject s behavior. Successful insertion of the objects through the cutout was unnecessary for our purposes. Subjects were rewarded for attempts at insertion regardless of success.

27 18 Chimpanzees Before testing began, the experimenter demonstrated the task a few times by placing the object on the floor, picking it up, and inserting it through the cutout. A trial began by the experimenter placing the Plexiglas panel on the floor and making an object available to the chimpanzee. The trial ended when the chimpanzee either successfully passed the object through the cutout or gave up and stopped attempting insertion. Panel orientation remained vertical and slightly tilted away from the chimpanzee and on the floor during trials where successful returns were easy, but was sometimes lifted from the floor, extremely tilted and/or horizontal during trials when the chimpanzees were experiencing difficulty. Testing sessions took place over several days, each chimpanzee with her own experimenter. Table 3 shows the number of trials each subject performed in each condition. Capuchins The capuchins were presented with the larger set of objects for training and to gather pilot data on their manipulative ability. The capuchins were trained to return the circle object through the cutout to the experimenter by rewarding successive approximations. The panels for the larger set of objects were too large to slide into the door frame of the testing box, so an experimenter held each panel on the outside of the testing box so that the cutouts were aligned with an aperture in the side of the testing box approximately 10 cm in diameter. The capuchins averaged 34 trials in each condition with the large objects. Data from these pilot testing sessions were used for the selection of participants and to make improvements for further testing. Based on their level of attentiveness during training, six out of eight capuchins were chosen to continue to experimental testing sessions. It was also determined from these pilot sessions that a smaller object would be more easily handled by

28 19 capuchins and more equivalent to the object-hand size proportions in the chimpanzees. Based on the sizes of adult male capuchins hands measured in a study by Fragaszy, Adams-Curtis, and Baer (1989), a smaller set of objects were fashioned from metal for experimental testing sessions. Experimental trials began with the small metal objects. The capuchins easily transferred to the task with the small objects after a short familiarization. Trials began with the experimenter passing the object to the subject and ended when the subject successfully passed the object back through the cutout or dropped or ejected the object from the testing box. Table 3 shows the number of trials each subject performed in each condition. Coding Hand Movements A sub-sample of the data was selected for coding. Table 4 shows the number of trials in each condition that were scored for each subject. Four trials from each condition were deemed sufficient to obtain the total range of movements that were observed in all subjects (from preliminary coding). The first two trials that were conducted with each subject were skipped to avoid extraneous behaviors and movements that may have been due to recent learning of the task. The following four trials in the circle condition were selected and for the remaining conditions, the first four trials were selected. This selection resulted in twenty scored trials for each chimpanzee, except for chimpanzee Ai, for whom only two Star trials were conducted, resulting in 18 scored trials. Twelve trials were scored for each capuchin, which included four trials of the Circle, Triangle and Square objects, except for capuchin Nick, who did not have trials with the triangle and for whom six trials with the Circle and Square objects were scored. The selection resulted in 58 trials scored for the chimpanzees and 72 trials scored for the capuchins.

29 20 Chimpanzee and capuchin hand movements were coded from the digital video using The Observer 4.0 and 5.0, Noldus Technologies. A new movement was recorded when the digits released the object and re-grasped or when the digits moved the object within the hand to grasp in a new position. It should be noted that, due to the camera angles, views of the hand movements were not always clear. In such cases, the coder was conservative in judging new hand movements; if the hand movement could not be clearly determined, it was not recorded. The categories and behaviors described in Table 5 were modified from Elliott and Connolly s (1984) scheme describing human grasps and in-hand movements. Simultaneous Convergent Movements are equivalent to what Elliott and Connolly (1984) called Simple Synergies, or movements in which the digits converge simultaneously upon an object. Within the Simultaneous Convergent Movements (SCV) category, pinch, tripod, tripod-with-support, squeeze and scissor grasps were recorded when the coder observed their occurrence. These grasps differed in the digits that contacted the object (see Table 5 definitions and Figure 5 illustrations). The behaviors tripod-with-support and scissor are grasps that were not included in Elliott and Connolly s (1984) scheme, but were added because they described hand movements that were frequently observed in one or both of the two species. Within the Simultaneous Divergent Movements (SDV) category, Roll and Palmar Combination movements were recorded. Simultaneous Divergent Movements are equivalent to what Elliott and Connolly (1984) called Reciprocal Synergies. Elliott and Connolly (1984) distinguish between three different types of rolls and do not include Palmar Combinations in the Reciprocal Synergies category. It was found that the capuchins and chimpanzees did not perform rolls with the same clarity of digit movement as humans. Because of this, the coder looked for any roll type, as long as the digits moved in an opposite direction to one another concurrently.

30 21 The Palmar Combination was also seen as a simultaneous movement with digits moving in opposite directions and was therefore incorporated into the SDV category. Figure 6 provides an illustration of a roll by a chimpanzee. Within Sequential Movements (SQM), Rotations and Turnovers were recorded. Elliott and Connolly (1984) referred to this category as Sequential Patterns and distinguished between three different types of rotations. As with the SDV category, these differences were not clearly distinguishable in the chimpanzees, so a general category of rotation was recorded. The Turnover was a sequence that was not described by Elliott and Connolly (1984), but was added because it was a common sequence used by the chimpanzees to pick up the object from the floor. It is most closely described by Elliott and Connolly s (1984) interdigital step, from the Sequential Patterns category. Figure 7 provides an illustration of a Turnover as an example of a Sequential Movement. Twenty percent of the data (26 trials) were re-scored to assess intra-observer reliability. The re-scored trials were chosen randomly and included trials of each of the conditions and with each of the subjects (13 were chimpanzee trials and 13 were capuchin trials). The behaviors within the categories SCV, SDV and SQM were pooled and the frequencies of movements scored within each category were compared in the original trials and the re-scored trials. The correlation between the original and re-scored sets yielded a Spearman s rho of for chimpanzee data and for capuchin data. Data Analysis Three aspects of hand movements were analyzed. The frequency of each movement type and the percent of each type of total hand movements were analyzed to determine the propensity

31 22 for each species to use in-hand movements. Both genera were observed using the surface of the panel frequently, so the nature of this use and whether or not the use assisted in-hand movements were analyzed. Finally, a few typical examples of each type of in-hand movements made by chimpanzees and the few that were made by the capuchins were analyzed in terms of digit movement and the areas on the digits that made contact with the object. This final analysis provided an in-depth look at the digit coordination during in-hand movements for each species, and the similarities and differences in the movements that were achieved by both species. Frequency and Percent of Total Movements To determine the types of movements that each species used in this task, the frequency of movements that occurred within each category was counted and the percent of total movements was calculated for each category. As in-hand movements were predicted to be elicited in both species, analysis of the data focused on the types of in-hand movements that were observed and the percent of total movements that they comprised compared to Simultaneous Convergent Movements. Before comparing the hand movements of the two species, the rate at which each group performed hand movements was calculated to assure that species differences were not due to differing activity levels during trials. A t-test revealed a non-significant difference between the rates of hand movements in the two groups, however the assumption of homogeneity of variance was violated. Due to the heteroskedasticity and the small and unequal sample sizes, the data were transformed using the reciprocal (1/x). A second t-test again revealed a non-significant difference in rates of hand movements between the groups.

32 23 Surface-brace and Assistance Due to the vertical position of the panel during testing, it was often necessary for subjects to support the object against gravity while attempting to insert it through the cutout. The extent to which the subjects used the surface of the panel to assist their movements ( surface-brace ) was investigated in several trials with both species. In particular, the variables that were considered most important were the types of movements that coincided with a surface-brace and whether or not an in-hand movement was assisted by the surface of the panel. Six chimpanzee trials were selected based on relatively high frequencies of in-hand movements in order to observe use of the surface during both grasping and in-hand movements. The trials included two Ai trials (square and triangle), two Pan trials (star and cross), and two Chloe trials (both cross) (390 seconds total). Capuchin trials were not selected based on frequency of in-hand movements because in-hand movements were extremely rare. Therefore, the capuchin trials could be chosen randomly and 12 of the trials that were selected for the reliability check were used to observe use of the surface (excluding Chris s circle trial) (210 seconds total). Because these trials did not include the few instances of in-hand movements in capuchins, those instances were separately observed for surface use. The percent of time that the surface was used within each trial was also recorded to demonstrate variation between and within individual subjects in the amount of time spent using the surface of the panel. In-depth Analysis of Movement Finally, several in-hand movements were observed in detail to determine how the digits moved the objects within the hand. For the chimpanzees, examples of each type of in-hand movement were chosen to describe the typical way in which these movements were achieved by movement of the digits. Two examples of Roll, Palmar Combination and Rotation, and one

33 24 example of Turnover were chosen based on the clarity of the video and typicality of the movement (as deemed by the coder). The few examples of capuchin Rolls were also described. To describe the movements, the temporal sequence of digit movement was recorded, identifying the digits used and areas of the digits that made contact with the object throughout the movement.

34 25 CHAPTER 3 RESULTS Frequency and Percent of Total Movements Data on each subject s trial durations and overall frequency of hand movements are shown in Table 6. The chimpanzees performed an average of 152 movements and the capuchins performed an average of 39 movements. Because fewer trials were scored for the capuchin subjects, their summed trial durations were less than the chimpanzees and overall fewer hand movements were recorded for each capuchin subject. However, from this table it is unclear whether or not the capuchins were less active than the chimpanzees or simply performed fewer and shorter trials. To determine if the capuchins made fewer hand movements due to fewer trials scored or to their level of activity, the average rate of movements per minute was calculated for each subject. From Table 7, one can see that three capuchin subjects (Solo, Xenon and Leo) performed hand movements at a rate within the range of the chimpanzee rates (between 21.0 and 28.2 movements per minute), while the other three subjects performed hand movements at a lower rate ( movements per minute). As depicted in Table 7, a t-test revealed a nonsignificant difference between the rates of hand movements in the two groups (t = , p = ). The frequencies of movements and percent of total movements performed within each category are shown in Table 8 for each subject. The majority of hand movements performed by both species were Simultaneous Convergent Movements, or static grasps, comprising % of chimpanzee hand movements and % of capuchin hand movements. The chimpanzees performed several in-hand movements each, including both Simultaneous

35 26 Divergent Movements ( %) and Sequential Movements ( %). Only two capuchins performed in-hand movements, each performing one Simultaneous Divergent Movement. The frequencies of in-hand movements (Simultaneous Divergent and Sequential Movements) for each subject are depicted in Figure 8. Surface-brace and Assistance Surface-assistance was observed in a subset of trials for chimpanzees and capuchins. The amount of time that a surface-brace or assistance was used varied extensively within and between individual subjects. In the selected trials, the chimpanzees spent between 8% and 25% of a trial engaging in a surface-brace and use of the surface co-occurred with four out of the thirteen in-hand movements that occurred in those trials. Of the four, surface use did not cooccur with the entire in-hand movement, but appeared to assist briefly at various times during the in-hand movement. The capuchins spent between 10% and 81% of a trial engaged in surfacebrace. They did not perform in-hand movements during the selected trials, however, the two instances of Simultaneous Divergent Movements in capuchins were both aided by the surface in one instance, the object was balanced within the cutout, and in the other instance, the object was braced against the surface of the panel by the subject s digits. The actions that were performed during a surface-brace and whether or not the surfacebrace assisted an in-hand movement are depicted in Table 9 for each of the selected trials. These actions typify the ways in which each species used the surface of the panel. The percent of time that each of the forms were employed was not investigated at this time. The chimpanzees typically used a static grasp of some sort when bracing the object against the surface, sometimes using the surface to assist an in-hand movement, and the capuchins typically used their mouth,

36 27 palm, heel of the hand, and a static grasp of some sort to brace the object against the surface of the panel. Frequently, the capuchins cupped the objects in their palm and then used their palm to hold the object against the surface and slid the object around until it went through the cutout. The capuchins also often held the object to the panel with the palm and extended the index finger and sometimes the index and thumb of the other hand to move the object toward the cutout. This behavior was not observed in the chimpanzees. In-depth Analysis of Movement To look more closely at in-hand movements, the digits involved and areas of contact made between the object and fingers were analyzed for chimpanzees, including two rolls, two palmar combinations, two rotations and one turnover, and for capuchins, two rolls. Figure 9 provides a diagram of the hand with the areas of contact labeled (a human hand is used for illustration). Chimpanzee rolls typically involved the use of the thumb and index digit, but were also frequently observed using the thumb and the index and middle digits. The two chimpanzee rolls described in detail were observed in Ai s second trial with the triangle and both involved just digits one and two. In the first roll, the triangle was initially grasped with the distal aspect of the thumb pad and the palmar aspect of the proximal and distal pads of the index digit. The objects were frequently grasped in this manner by chimpanzees because of their relatively short thumb: the thumb held the object to the slightly flexed index finger, allowing the object to come into contact with the either the palmar or lateral aspect of both the proximal and distal pads of the index finger. To roll the triangle, the thumb extended slightly as the index flexed slightly, turning the object to be finally grasped between the distal thumb pad and the lateral-proximal aspect of the index digit (tip-to-side pinch grasp). In the second roll, the triangle was initially grasped

37 28 between the medial side of the distal thumb pad and the proximal pad of the index digit, turned to the lateral side of the index digit in the same manner as described above, and finally grasped between the distal thumb pad and lateral-proximal aspect of the index digit (tip-to-side pinch grasp). Palmar combinations typically involved the thumb and index, and often digits three and four as well. One palmar combination is described for Ai and the other is described for Pan. Ai s palmar combination involved the thumb, index and middle digits. The triangle was initially grasped with the medial-distal aspect of the thumb, the distal pad of the index and the distallateral aspect of the middle digit. The thumb extended, pushing the triangle forward in the hand as the index and middle digits flexed slightly toward the palm, so that the triangle was grasped between the medial-distal aspect of the thumb and lateral-distal pad of the index finger (tip-toside pinch grasp). Pan s palmar combination involved the thumb, index, middle and fourth digits. The star was initially grasped in a tripod-with-support grasp between the distal and proximal pads of the thumb, index and middle digits and proximal pad of the fourth digit. As in Ai s case, the thumb extended, pushing the star forward in the hand as the four digits flexed slightly toward the palm, ending with the star between the thumb tip, proximal and distal pads of the index digit and the lateral-proximal aspect of the middle digit (tripod grasp). The two rotations described in detail were observed in Chloe s second and third trials with the cross. Both rotations involved the thumb and index, middle and fourth digits. The first rotation began palm-up with the cross in a tip-to-side pinch between the distal thumb pad/thumb tip and the lateral-distal pad of the index digit. Chloe pushed against the surface of the panel allowing the thumb to release and flex as the index, middle and fourth digits extended slightly and cradled the cross, all three digits contacted with the proximal and distal pads. The thumb tip

38 29 then came into contact with the end of the cross and extended, pushing the cross forward in a palmar combination, the other three digits flexing toward the palm. At the end of the palmar combination, the thumb tip, proximal and distal pads of the index and the medial side of the middle digit were in contact with the cross. The thumb then abducted, pushing the end of the cross out of the palm and pulling the cross from the surface of the panel, the index flexed inward toward the palm, turning the cross so that the end that previously touched the panel was in contact with the palm and the end that previously touched the palm was facing the panel. The cross was finally grasped between the distal thumb pad and the lateral-distal aspects of the index and middle digits. The second example of a rotation described did not involve use of the surface to assist rotation of the cross. The rotation again began with the cross in a tip-to-side pinch between the distal thumb pad and lateral-distal side of the index digit. The cross was then rolled by thumb adduction and index flexion; concurrently, digits three, four and five extended outward and then flexed inward to contact the other end of the cross on the distal pads of digits three and four. Digits three, four and five continued to flex, pulling the end of the cross toward the palm as the thumb abducted, pushing the end of the cross that previously touched the palm toward the surface of the panel. The cross was finally grasped in a tip-to-side pinch between the distal thumb pad and lateral side of the index. The turnover described in detail was observed in Ai s third trial with the square and involved the thumb, index and middle digits. The example provided describes the typical sequence of movements involved in a turnover. First, the square was picked up from the floor with a scissor grip between the medial-distal side of the index and lateral-distal side of the middle digit, the index and middle digits converging to the thumb tip, gripping the square in a

39 30 tripod grasp. The middle digit then lost contact with the square as the thumb abducted and extended and the index flexed, rolling the square to the lateral-distal side of the index digit. The square was finally grasped in a tip-to-side pinch grasp between the distal thumb pad and proximal-lateral index pad (Figure 7 provides a generalized example). In capuchins, rolls were observed in Nick s fifth trial with the circle and Xenon s third trial with the square. Both examples were assisted by the surface of the panel. Nick s roll involved the thumb and index digit. The circle was aligned with the cutout, but not pushed through to the experimenter, so that it rested in the cutout. Nick grasped the circle in a tip-to-side pinch between the distal thumb pad and lateral-distal aspect of the index digit. The thumb then abducted slightly as the index flexed toward the palm, turning the circle along its axis inside the cutout. Xenon s roll involved the thumb, index and middle digits. The square was braced against the surface of the panel in a tripod grasp between the distal pads of the thumb, index and middle digits. The middle digit then flexed toward the palm as the thumb adducted, turning the square about its axis while remaining braced against the surface of the panel. The index digit remained in the same position. Most of the rolls observed in the chimpanzees were similar to Nick s rolls in that the lateral side of the index digit came into contact with the object. However, because the chimpanzee s thumb is relatively short compared to the fingers, the object frequently came into contact with the proximal aspect of the lateral side of the index, whereas Nick s roll was achieved with the distal aspect of the lateral side of the index. Xenon s roll was also achieved with the distal aspects of the digits. Additionally, due to the position of the panel in each experimental setting, the chimpanzees frequently performed rolls with the arm supinated (see Figure 6), most often without assistance from the surface of the panel, while Nick and Xavier

40 31 performed their rolls with the arm in the pronate position with surface assistance (similar to the hand position of the capuchin tripod in Figure 5).

41 32 CHAPTER 4 DISCUSSION General Discussion Although extremely rare, the capuchins demonstrated an ability to move an object in one hand by movement of the digits alone, an ability that was clearly and frequently demonstrated by chimpanzees. As in foraging and tool-using behaviors, the capuchin subjects accomplished the same functional end of aligning and inserting small objects through apertures in a panel as the chimpanzee subjects. However, the capuchins achieved the task differently than the chimpanzees; this study highlighted differences between species in type and extent of performance of in-hand movements, and strategic differences in aligning the objects to the cutouts. That in-hand movements were observed in both species supports our hypothesis that there is some degree of convergent evolution of manual motor capabilities in Cebus and Pan. On the other hand, it is likely that cognitive and perceptual factors also contributed to the differences in hand movements and strategies that were observed. For example, the capuchins and chimpanzees perception of and/or attention to the physical attributes of the objects and cutouts may have affected their approach to the task and manipulation of the objects. As predicted, static grasps accounted for the majority of movements performed by both species. The chimpanzees proved more proficient at in-hand movements as they used every form recognized by our classification scheme and these movements accounted for a larger percentage of total movements than in the capuchins. Furthermore, the one type of in-hand movement that both species shared (the roll) is one of the less sophisticated forms. Rolls and palmar combinations are viewed as less sophisticated because digit movement is simultaneous

42 33 and often follows prehension as a slight modification to a static grasp, whereas Sequential Movements involve the complete release of a particular grasp and multiple re-grasps via temporal changes in digit movement and placement. The capuchin rolls were similar to typical chimpanzee rolls in object placement on the digits and the movement of thumb extension to roll the object to the lateral aspect of one of the digits. However, the degree to which the object was turned by chimpanzees often exceeded that which was observed in the two capuchin rolls. Also, the chimpanzees often performed rolls without use of the surface of the panel, whereas use of the surface was evident in both Nick and Xenon s rolls. The chimpanzees performance supports our hypothesis that an increased ability to perform in-hand movements reflects their greater independent digital control (further discussed below). Although the percent of time that the chimpanzees and capuchins spent bracing the object against the surface was not investigated systematically, it appeared to the coder that the capuchins braced the object against the surface of the panel more often than the chimpanzees. This may have been because the panel position relative to the capuchin s bodies (and subsequent arm position) required more resistance from gravitational forces. In the chimpanzees case, the surface of the panel appeared to assist their in-hand movements, possibly by freeing the hand from gravitational forces and facilitating greater individuation of the digits. (The effects of relative panel position and arm positions are discussed further below.) The chimpanzees and capuchins also differed in the ways in which the surface of the panel was used. While the percent of time the subjects used these different forms of surface-brace was not systematically investigated, some patterns became evident to the coder. Besides the occasional use of the surface during in-hand movements, the chimpanzees typically used a static grasp and occasionally used their mouth when bracing the object against the surface. The capuchins

43 34 typically used the heel and palm of the hand when bracing the object against the surface of the panel, but like chimpanzees, they also used static grasps and their mouth. The capuchins did not use the panel to assist movements, but used a palm-brace in order to keep the object near the cutout during attempts. Often during a palm-brace, the capuchins would extend the index finger and sometimes both the index and thumb to assist movement of the object toward the cutout. This particular bimanual strategy was not observed in the chimpanzees, possibly due to the difference in panel position relative to the body, but it may also reflect the capuchins solution to the problem of manipulating a small object given cruder dexterity. Again, differences in perception of the cutouts and/or cognitive approach to the problem might have also contributed to this difference in strategy. Digital Independence and Hand Coordination By performing a variety of forms of in-hand movements and using them more often than the capuchins, the chimpanzees demonstrated a relatively high degree of individual digit control. The chimpanzees also demonstrated flexibility of in-hand movements, as the hand movements that qualified for a particular category were sometimes achieved differently (by different digits and/or digital movements), and occasionally combined assistance from the surface of the panel. The chimpanzees flexibility and control of movement of the hand imply that the chimpanzees have relatively sophisticated coordinative abilities compared to the capuchins. Muscle linkage, or a coordinative structure, is a group of functionally linked muscles that work together as a unit, facilitating a high degree of control and reduced need to control several muscles independently (Tuller, Turvey, and Fitch, 1982). When the hand is viewed as a coordinative structure, it appears that the chimpanzees have a higher degree of muscle linkage in the hand, possibly supported by

44 35 increased neurological connections, as compared to the capuchins. The chimpanzees in the present study had many similarities with humans in hand coordination and movement, despite notable differences in digit length and proportions. A prominent difference between humans and chimpanzees, however, was refinement of movement: the chimpanzees maneuvered the objects with seemingly clumsier and more inefficient digit movements, especially for rotations. The chimpanzees often used a different sequence of actions, from that described for humans by Elliott and Connolly (1984), to accomplish the same goal (i.e. rotation or change of object placement within the hand). These complexities in chimpanzee hand movement warrant further investigation, particularly in individuals spanning different age and sex classes, as the present study focused on three adult females. Differences in muscular anatomy may have also led to differences in how the chimpanzee hand and the capuchin hand achieve an in-hand movement. For example, it is possible that chimpanzees have greater control and/or strength of the thumb because of the differentiation of the flexor pollicis longus above the carpal bones, the possession of a rudimentary extensor pollicis brevis muscle, and the more specialized opponens pollicis muscle. Such muscular differences may lead to the chimpanzee using its thumb in a different way than the capuchins to achieve the same movement of an object. Moreover, greater control or strength of the thumb may have facilitated the ability to perform the Sequential Movements, such as rotating and turning the object in the hand, which were absent in the capuchins. Further investigation of the muscles that control different hand movements is necessary to understand the behavioral differences that were observed between the chimpanzees and the capuchins.

45 36 Classifying Chimpanzee and Capuchin Hand Movements For the purposes of the present study, the coding scheme was satisfactory. Because the chimpanzees and capuchins performed cruder forms of the Elliott and Connolly (1984) hand movements, the merging of several of their categories proved extremely useful. The terminology used in the present study was designed to be accessible to a generalized audience and bridge commonly used terminology in studies of hand function in both humans and non-human primates. Use of this system in future hand research with non-human primates is suggested, however, further elaboration may be necessary depending on the capabilities of different species. For example, further investigation of chimpanzee in-hand movements may produce subcategories within the Sequential Movements category, similar to that of Elliott and Connolly (1984), to describe more accurately the types of in-hand movements of which chimpanzees are capable. Because the present study s classification system was successful and builds on Napier and Napier (1967, 1985, 1993 Rev. Ed.) for descriptions of static grasps and Elliott and Connolly (1984) for descriptions of dynamic movements, it is reasonable that this classification system could provide the basis for further research in dynamic hand movements in non-human primates. Encountered Problems It is possible that differences in coordinative abilities and neural and muscular anatomy cannot fully account for the rare appearance of in-hand movements in the capuchins. Two distinct methodological confounds stand out as possible sources of the near-absence of in-hand movements in the capuchins. The differences in extent and form that were observed between the rolls produced by the chimpanzees and capuchins may also be due to these confounds. The first confound is the difference in length and relative proportions of the objects to the subjects hands.

46 37 The chimpanzees objects were elongated compared to the capuchins objects. Greater length may have facilitated in-hand movements in the chimpanzees compared to the capuchins as there is a larger surface area on longer objects for grasping during movement. The size and relatively smaller surface area of the capuchin objects may have required the majority of their efforts to be put toward maintaining a grip on the object. Indeed, the capuchins often cupped the objects in the palm and quickly pressed them to the surface of the panel, then slid them around near the cutout until they went through. Thus, the capuchins found a solution to the task that didn t even involve a static grasp. The tendency for all of the capuchins to use this strategy during most trials contributed to fewer total hand movements scored, as depicted in Table 6. The chimpanzees were never observed using this strategy. The chimpanzees occasionally used a form of cradling, rather than cupping, that resembled a palm-up hook grip, but with fingers very loosely flexed around the object, simply supporting the object on the proximal pads of digits 1-4. It is possible that the cupping strategy used by the capuchins reflects a basic perceptual or cognitive approach to the problem that differs from the way chimpanzees and humans solve the task, but it is possible that the size and dimensions of the objects played a significant role in the adoption of the strategy. The strategy, compounded with the proportionally small size of the objects, may have contributed to the lack of in-hand movements observed in the capuchins. The second methodological confound was the inconsistency of panel position and orientation between the two species. In testing the chimpanzees, experimenters placed the panel vertically on the floor and the panels were not fixed into a wall, as was the case for the capuchins. Consequently, for the chimpanzees, the panels were in a different position relative to the body and the orientation of the panel was flexible. Because the cutout in the panel was close to the floor (9 cm), as the chimpanzees sat on the floor to participate in the task, the arm was

47 38 often supinated when attempting to insert the objects through the cutouts (see Figure 4a). This arm position may have facilitated in-hand movements because the palm helped support the object against gravity, allowing more independence of the digits. For the capuchins, the panels were fixed in a vertical position and the cutouts were approximately 18.5 cm from the bottom of the testing cage. Thus, the capuchins could be anywhere from chest- to eye-level with the cutout (see Figure 4b). In this position, the capuchins tended to attempt insertions with the arm pronated and palm facing forward away from the body (see Figure 4b). With the arm in that position, the capuchins had to use their hand to support the object against gravity, which may have hindered the ability to perform in-hand movements. The differences in the extent to which the surface was used and the types of movements that coincided with bracing the object on the surface might also be partially attributed to the differing panel positions between the two species. Next Steps Future comparative studies on behavior and neural and muscular anatomy are needed to clarify the phylogenetic differences in hand function in primates, including Old World monkeys and great and lesser apes. The present study has shown that the capuchins are capable of a higher level of manual sophistication than what has been previously attributed to monkeys, and chimpanzees have sophisticated manual capabilities similar to humans. Both species abilities suggest relatively advanced neural and muscular contributions, however these elements have not been fully differentiated. To what extent does deviation and elaboration in hand musculature influence the ability to perform in-hand movements? What environmental conditions influence the evolution of musculature that supports in-hand movements? Comparative investigation of these questions are necessary to illuminate neurological and muscular correlates among non-

48 39 human primates and the ecological pressures that might have favored the selection of sophisticated hand movements, such as intrinsic movements of the hand. While the capuchins have demonstrated their ability to use in-hand movements, the extent to which they do so remains unclear because of the procedural limitations discussed above. It is possible that the capuchins natural uses of in-hand movements might emerge if the objects were elongated and if the panel position was made to mirror that of the chimpanzees. Replication of this study with these parameters is currently being planned. After replication, it will be possible to compare the common movements, like rolls, more directly because elements such as object size, panel position, and their effects on surface-reliance will be removed and strategic differences between the two species can then be clarified. Specifically, the capuchins tendency to cup the objects in the hand might not be necessary if they didn t have to support the object against gravity while attempting to align and insert through the cutout, although their general strategy of bracing the object to the surface and sliding it around until it goes through the panel might still be used, if it is due to a difference in cognitive approach to the problem and not to the methodological confounds of panel position and shape dimensions. A useful addition to this study might also be an investigation of bimanual actions and use of the mouth to manipulate objects. This study focused on in-hand movements as a way to modify the object s position within the hand, however the chimpanzees and capuchins frequently performed bimanual actions and used the mouth either to hold while the hand re-grasped, or to attempt alignment and insertion directly. Non-human primates commonly use the mouth to explore and manipulate objects (Napier, 1993 Rev. Ed). To describe object manipulation and the types of hand movements used by non-human primates completely, these two behaviors must be taken into account in future research.

49 40 The present study has thus constituted a pilot study on the motor contributions to in-hand movements in capuchin monkeys and chimpanzees, of which further differentiation between muscular and neural mechanisms and consideration of the above mentioned variables, are necessary. This study has again demonstrated that capuchin monkeys stand out among New World monkeys, now with a manual capability that may explain their relatively sophisticated natural behaviors. Their ability to use in-hand movements supports the hypothesis that there is some convergent evolution in manual motor abilities in New and Old World lines. Though the present study focused on motor similarities and differences, it became clear that the capuchins and chimpanzees employed different cognitive strategies in solving the same problem. From the data, it can be hypothesized that the chimpanzees were more mindful of the goal (insertion) than the capuchins, and selected the particular strategies (the grasps and hand movements) that might lead to the achievement of the goal. It is possible that this scenario is also true of wild chimpanzees and capuchins when learning foraging and tool-using behaviors. Exploring the cognitive and perceptual differences between the two species when manipulating small objects will be valuable to future research on dynamic hand movements. In general, cognitive and perceptual factors should be incorporated into future investigations of hand movements in object manipulation in non-human primates.

50 Dynamic Hand Movements 41 REFERENCES Andrews, P. & Groves, C. P. (1976). Gibbons and Brachiation. In D. M. Rumbaugh (Ed.), Gibbon and siamang, vol. 4: suspensory behavior, locomotion, and other behaviors of captive gibbons; cognition (pp ). Switzerland: S. Karger. Behnke, R. S. (2001). Kinetic anatomy. Champaign, IL: Human Kinetics. Bishop, A. (1964). Use of the hand in lower primates. In J. Buettner-Janusch (Ed.), Evolutionary and genetic biology of primates (pp ). New York: Academic Press. Boesch, C. & Boesch, H. (1993). Different hand postures for pounding nuts with natural hammers by wild chimpanzees. In H. Preuschoft & D. J. Chivers (Eds.), Hands of primates (pp ). New York: Springer-Verlag Wien. Bortoff, G.A. & Strick, P.L. (1993). Corticospinal terminations in two new world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. Journal of Neuroscience, 13, Byrne, R. W. & Corp, N. (2001). Manual dexterity in the gorilla: bimanual and digit role differentiation in a natural task. Animal Cognition, 4, Christel, M. (1993). Grasping techniques and hand preferences in Hominoidea. In H. Preuschoft & D. J. Chivers (Eds.), Hands of primates (pp ). New York: Springer-Verlag Wien. Christel, M., & Fragaszy, D. (2000). Manual function in Cebus aella. Digital mobility, preshaping, and endurance in repetitive grasping. International Journal of Primatology, 21, Corp, N. & Byrne, R. W. (2002). Leaf processing of wild chimpanzees: physically defended leaves reveal complex manual skills. Ethology, 108, Costello, M. B. & Fragaszy, D. M. (1988). Prehension in Cebus and Saimiri: 1. grip type and hand preference. American Journal of Primatology, 15, Elliott, J. M., & Connolly, K. J. (1984). A classification of manipulative hand movements. Developmental Medicine and Child Neurology, 26, Exner, C. E. (1992). In-hand manipulation skills. In J. Case-Smith & C. Pehoski (Eds.), Development of hand skills in the child (pp. 1-11). Bethesda, MD: American Occupational Therapy Association, Inc.

51 Dynamic Hand Movements 42 Fleagle, J. G. (1999). Primate adaptation and evolution, 2 nd ed. San Diego, CA: Academic Press. Fragaszy, D. (1998). How non-human primates use their hands. In K. J. Connolly (Ed.), The psychobiology of the hand (pp ). London: Mac Keith Press. Fragaszy, D. M., Adams-Curtis, L. E., Baer, J. F. (1989). Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus aella): developmental and comparative aspects. American Journal of Primatology, 17, Fragaszy, D., Izar, P., Visalberghi, E., Ottoni, E. B., & Gomes de Oliveira, M. (2004). Wild capuchin monkeys (Cebus aella) use anvils and stone pounding tools. American Journal of Primatology, 64, Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin. Cambridge, UK: Cambridge University Press. Heffner, R.S. & Masterson, R.B. (1983). The role of the corticospinal tract in the evolution of human digital dexterity. Brain, Behavior and Evolution, 23, Jouffroy, F. K., Godinot, M., & Nakano, Y. (1993). Biometrical characteristics of primate hands. In H. Preuschoft & D. J. Chivers (Eds.), Hands of Primates (pp ). New York: Springer-Verlag Wien. Kamakura, N., Matsuo, M., Ishii, H., Mitsuboshi, F., & Miura, Y. (1980). Patterns of static prehension in normal hands. American Journal of Occupational Therapy, 34, Lemon, R. N. (1993). Cortical control of the hand. Experimental Physiology, 78, Lewis, O. J. (1989). Functional morphology of the evolving hand and foot. Oxford: Clarendon Press. Maier, W. (1993). Adaptations in the hands of cercopithecoids and callitrichids. In H. Preuschoft & D. J. Chivers (Eds.), Hands of primates (pp ). New York: Springer-Verlag Wien. Marzke, M. W. & Wullstein, K. L. (1996). Chimpanzee and human grips: A new classification with a focus on evolutionary morphology. International Journal of Primatology, 17, Napier, J. (1993). Hands (Rev. Ed). Princeton, NJ: Princeton University Press. Napier, J. R. & Napier, P. H. (1967). A handbook of living primates. London: Academic Press. Napier, J. R. & Napier, P. H. (1985). The natural history of the primates. Cambridge, MA: The MIT Press.

52 Dynamic Hand Movements 43 Pehoski, C. (1992). Central nervous system control of precision movements of the hand. In J. Case-Smith & C. Pehoski (Eds.), Development of Hand Skills in the Child (pp. 1-11). Bethesda, MD: American Occupational Therapy Association, Inc. Schieber, M. (1991). Individuated finger movements of rhesus monkeys: a means of quantifying the independence of the digits. Journal of Neuroscience, 65, Schoneich, S. (1993) Hand usage in the ring-tailed lemur (Lemur catta Linnaeus 1758) when solving manipulative tasks. In H. Preuschoft & D. J. Chivers (Eds.), Hands of primates (pp ). New York: Springer-Verlag Wien. Schultz, A. H. (1969). The life of primates. New York: University Books. Tanaka, I. (1998). Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Animal Behavior, 56, Tonooka, R. & Matsuzawa, T. (1995). Hand preferences of captive chimpanzees (Pan troglodytes) in simple reaching for food. International Journal of Primatology, 16, Tuller, B., Turvey, M. T., and Fitch, H. L. (1982). The Bernstein Perspective: II. The concept of Muscle Linkage or Coordinative Structure. In J. A. Scott Kelso (Ed.), Human motor behavior: an introduction (pp ). Hillsdale, NJ: Lawrence Erlbaum Associates, Publishers. Wilson, F. R. (1998). The hand: how its use shapes the brain, language, and human culture. New York: Pantheon Books. Wong, I. J., & Whishaw, I. Q. (2004). Precision grasps of children and young and old adults: individual differences in digit contact strategy, purchase pattern, and digit posture. Behavioral Brain Research, 154,

53 Dynamic Hand Movements 44 Table 1. Synonymous Terminology Used to Describe Static Grasping Patterns in Humans 1. Napier and Napier (1985) Power Precision Elliott and Connolly (1984) Simple Synergies Simple Synergies Squeeze Pinch Dynamic Tripod Power Grip Precision Grip Intermediate Grip Kamakura, et al. (1980) Standard Type Index Finger Extension Type Extension Type Distal Type Tip Prehension Parallel Mild Flexion Grip Surrounding Mild Flexion Grip Parallel Extension Grip Lateral Grip Tripod Grip Tripod Variation 1 Tripod Variation 2 Wong and Whishaw (2004) Proper Pincer Improper Pincer Five Digit Flower Grasp Supported Pincer Triangular Grasp Four Digit Flower Grasp Improper Triangular Grasp Hook Power Grip Hook Type Grip With Scissor Adduction Grip No Thumb 1. Napier and Napier (1985) begin the list on the left because later classification systems built on these four main grip types. Elliott and Connolly (1984), Kamakura et al., (1980), and Wong and Whishaw (2004) were chosen to represent different classification systems that are in use to describe human hand movements. Though various names are invented to describe different hand movements, they all are encompassed by Napier and Napier s original categories.

54 Dynamic Hand Movements 45 Table 2. Synonymous Terminology Used to Describe Static Grasping Patterns in Great Apes. Napier and Napier (1967) Power Precision Hook Marzke and Wullstein (1996) Cup Hold Tip-to-Tip Hold Pad-to-Tip Hold Pad-to-Side Hold Transverse Hook Diagonal Hook Extended Transverse Hook Extended Diagonal Hook Byrne and Corp (2001) Power-grip Squeeze-grip Pinch-grip Pencil-grip Tonooka and Matsuzawa (1995) Radial-Palmar Grasp Imprecise Grasp Pincer Grip Hook Ulnar-palmar Grasp 1 Index Finger Hook Scissor Scissor-grip Index and Middle Finger Grip 1. Ulnar digits 4 and 5 hold raisin to volar surface of metacarpal joints, digits 2 and 3 flexed as well, so hand is effectively in hook-grip position.

55 Dynamic Hand Movements 46 Table 3. Number of Trials Each Subject Performed With Each Object (Condition). Subjects Total Trials Circle Triangle Square Star Cross Pan Ai Pan Chloe Sum Cebus Solo Chris Xenon Xavier Nick Leo Sum

56 Dynamic Hand Movements 47 Table 4. The Number of Trials of Each Condition that were Scored for All Subjects. Subject Circle Square Triangle Star Cross Total Pan Ai Pan Chloe Sum Cebus Solo Chris Xenon Xavier Nick Leo Sum

57 Dynamic Hand Movements 48 Table 5. Categories of Hand Movements, Coded Behaviors, and their Definitions. Category Behaviors Definition All digits converge upon the object simultaneously. Simultaneous Convergent Movements (SCV) Simultaneous Divergent Movements (SDV) Sequential Movements (SQM) Pinch Tripod Tripod-with- Support Squeeze Scissor Roll Palmar Combination Rotation Turnover Thumb and index converge simultaneously upon the object (includes both tip-to-tip and tip-to-side pinches). Thumb, index, and third digit (middle) converge simultaneously upon an object. Thumb, index, and middle digit converge simultaneously upon the object, digits four and/or five provide additional support. All five digits converge simultaneously upon the object. Index and middle digit converge simultaneously on the object. Thumb and one or more digits move in opposite directions simultaneously to turn or move the object within the hand. Once grasped, thumb and index move opposite to one another to twist or roll the object along one of its axes; up to three other digits may contact and/or provide support. Object is stabilized in the palm by at least two digits and thumb, digits flex toward palm as thumb extends object forward in the hand. Digits move sequentially through time to rotate the object in the hand. The thumb and at least one other digit move sequentially through time to rotate the object within the hand; object may move about more than one axis. A sequence of grasps in which the object is picked up with a scissor grip and rolled around the index finger to be grasped. Usually follows the order scissor, tripod, roll, pinch/tripod.

58 Dynamic Hand Movements 49 Table 6. Number of Trials, the Summed Trial Durations (in Seconds), the Average Trial Length (in Seconds), and the Total Number of Movements Performed Across All Trials for Each Subject. Subject Number of Trials Summed Trial Durations (sec) Average Trial Duration (sec) Total Movements Pan Ai Pan Chloe Sum (Mean) (21.2 min) Mean (7.1 min) Cebus Solo Chris Xenon Xavier Nick Leo Sum (16.6 min) Mean (2.8 min) Because there were double the participants in the capuchin group, a greater number of capuchin trials were scored overall, but there were fewer trials scored for each capuchin in comparison to each chimpanzee. 2. Although there were more capuchin trials scored overall, the summed capuchin trials were shorter in duration than the chimpanzee trials; similarly, each capuchin s average trial duration was shorter than the chimpanzees.

59 Dynamic Hand Movements 50 Table 7. Average Rate of Movements per Minute (Original Data and Transformed Data); Variance in the Original and Transformed Data for Each Species. Pan Subject Average Rate (movements/minute) Transformed Rates (1/x) Ai Pan Chloe Mean (Variance) 24.4 (13.12) Cebus Solo Chris Xenon Xavier Nick Leo Mean (Variance) (56.44) Difference between groups is non-significant (t = , p = ), assumption of homogeneity of variance violated. 2. Difference between groups is non-significant (t = , p = ).

60 Dynamic Hand Movements 51 Table 8. Frequency and Percent of Movements (in Parentheses) Performed Within Each Category. Subject SCV (% of total) SDV (% of total) SQM (% of total) Total Pan Ai 112 (86.2%) 15 (11.5%) 3 (2.3%) 130 Pan 135 (86%) 17 (10.8%) 5 (3.2%) 157 Chloe 147 (86.5%) 16 (9.4%) 7 (4.1%) 170 Sum Mean (86.23%) 16 (10.6%) 5 (3.2%) Cebus Solo 41 (100%) Chris 37 (100%) Xenon 52 (98.1%) 1 (1.9%) 0 53 Xavier 26 (100%) Nick 37 (97.4%) 1 (2.6%) 0 38 Leo 40 (100%) Sum Mean 38.8 (99.25%) 0.33 (0.075%)

61 Dynamic Hand Movements 52 Table 9. Ways in Which Object was Braced Against the Surface of the Panel. Trial Action during brace Movement Assist Ai Triangle 2 none Ai Square 3 none Pan Star 2 grasp PCM X Pan Cross 4 grasp roll grasp Chloe Cross 2 rotation X rotation partially X roll Chloe Cross 3 grasp rotation partially X Solo Triangle 2 mouth to panel grasp Solo Square 4 mouth to panel Nick Square 1 grasp palm to panel Nick Square 5 none Leo Circle 4 none Leo Triangle 2 palm to panel Chris Triangle 2 none Chris Square 3 grasp heel of hand to panel Xenon Triangle 1 palm to panel mouth to panel grasp Xenon Square 4 palm to panel grasp Xavier Circle 4 palm to panel mouth to panel Xavier Triangle 3 grasp palm to panel Chimpanzees used static grasps when bracing object against the surface of the panel and sometimes used the surface to assist in-hand movements. Capuchins used their palm, the heel of their hand, mouth and static grasps to brace the object against the surface of the panel. Not shown here are the two instances of in-hand movements in capuchins, both of which were assisted by the surface of the panel.

62 Figure 1. Posterior View of the Human Hand Skeleton. Image taken directly from Behnke, Dynamic Hand Movements 53

63 Dynamic Hand Movements 54 Figure 2a. Relative Sizes of the Panels and Objects Used by the Chimpanzees. Objects not drawn to scale; large PVC objects; the panel with the circle cutout is used for illustration, as well as the circle, square, triangle, star and cross objects. Figure 2b. Relative Sizes of the Panels and Objects Used by the Capuchins. Objects not drawn to scale; small steel objects and large PVC objects; the panel with the circle cutout is used for illustration, as well as the circle, square, and triangle objects.

64 Dynamic Hand Movements 55 Figure 3a. Chimpanzee Holding Circle Object in a Tripod Grasp. (Approximately ½ of actual size.) Figure 3b. Capuchin Holding Circle Object in a Pinch Grasp. (Approximately ½ of actual size.) Illustrations by Cheryl Reese 2005.

65 Dynamic Hand Movements 56 Figure 4a. Chimpanzee Ai Inserting the Circle Object Toward the Tester. Figure 4b. Capuchin Monkey Chris Holding the Circle Object.

66 Dynamic Hand Movements 57 Capuchin Pinch Capuchin Tripod Capuchin Squeeze Chimpanzee Pinch (tip-to-side) Chimpanzee Pinch (tip-to-tip) Chimpanzee Tripod Chimpanzee Scissor grip Figure 5. Examples of Simultaneous Convergent Movements. Illustrations Cheryl Reese, 2005.

67 Dynamic Hand Movements 58 Figure 6. Illustration of a Roll. After prehension, the index flexes upward from the metacarpal joint as the thumb adducts slightly, to roll the object clockwise from the distal-lateral aspect of the index to a more proximal-lateral aspect. Illustrations Cheryl Reese, 2005.

68 Dynamic Hand Movements 59 Figure 7. Illustration of a Turnover. Object is prehended in scissor grip, digits 2 and 3 flex toward thumb. Object is held briefly in a tripod grip, then the thumb rolls the object over the tip of digit 2; thumb and digit 2 move in opposite directions to roll object to lateral aspect of digit 2. Object is finally pushed slightly forward by thumb to be finally grasped in a pinch grip. Illustrations Cheryl Reese, 2005.

69 Dynamic Hand Movements Frequency SQM SDV Ai Pan Chloe Solo Chris Xenon Xavier Nick Leo Subjects Figure 8: Frequency of In-hand Movements: Simultaneous Divergent Movements (SDV) and Sequential Movements (SQM).

70 Dynamic Hand Movements 61 Figure 9. Diagram of Human Hand. Areas depicted within white circles were coded to describe the areas of object contact during in-hand movements.