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Evolution of Grasping Among Anthropoids

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Evolution of Grasping Among Anthropoids doi: 10.1111/j.1420-9101.2008.01582.x Evolution of grasping among anthropoids E. POUYDEBAT,* M. LAURIN, P. GORCE* & V. BELSà *Handibio, Universite´ du Sud Toulon-Var, La Garde, France Comparative Osteohistology, UMR CNRS 7179, Universite´ Pierre et Marie Curie (Paris 6), Paris, France àUMR 7179, MNHN, Paris, France Keywords: Abstract behaviour; The prevailing hypothesis about grasping in primates stipulates an evolution grasping; from power towards precision grips in hominids. The evolution of grasping is hominids; far more complex, as shown by analysis of new morphometric and behavio- palaeobiology; ural data. The latter concern the modes of food grasping in 11 species (one phylogeny; platyrrhine, nine catarrhines and humans). We show that precision grip and precision grip; thumb-lateral behaviours are linked to carpus and thumb length, whereas primates; power grasping is linked to second and third digit length. No phylogenetic variance partitioning with PVR. signal was found in the behavioural characters when using squared-change parsimony and phylogenetic eigenvector regression, but such a signal was found in morphometric characters. Our findings shed new light on previously proposed models of the evolution of grasping. Inference models suggest that Australopithecus, Oreopithecus and Proconsul used a precision grip. very old behaviour, as it occurs in anurans, crocodilians, Introduction squamates and several therian mammals (Gray, 1997; Grasping behaviour is a key activity in primates to obtain Iwaniuk & Whishaw, 2000). On the contrary, the food. The hand is used in numerous activities of manip- precision grip, in which an object is held between the ulation and locomotion and is linked to several func- distal surfaces of the thumb and the index finger, is tional adaptations (Godinot & Beard, 1993; Begun et al., usually viewed as a derived function, linked to tool use 1997; Godinot et al., 1997). In particular, the hand is and human morphological autapomorphies (Napier, involved in prehension, such as gripping of static foods 1956; Tuttle, 1965; Schultz, 1969; Susman, 1979, 1989; (fruits, leaves) and dynamic foods such as insects or other Marzke et al., 1992; Clark, 1993). The precision grip has prey (frogs, rodents, small antelopes). Some primates been considered the most important hand function of all such as chimpanzees (Pan troglodytes) and capuchins prehensile movements (Napier, 1980). (Cebus apella) use their hands to manipulate tools, to Our aim is to reconsider this simple model of grasping crack nuts, for example (Boesch & Boesch, 1990; Fraga- evolution in the light of morphometric data from szy et al., 2004), whereas gorillas (Gorilla gorilla) use their numerous species of primates and behavioural consider- hands to extract food from holes (Pouydebat et al., 2005). ations such as areas of contact between the fingers and The evolution of primates (humans included) is linked to the food grasped by extant primates. Therefore, the the development of those behaviours allowing organisms possible presence of a phylogenetic signal in the behavio- to exploit the resources in their environment. A general ural and relevant morphometric characters is investi- model of grasping in primates proposes an evolution from gated and the correlation between morphometric and a ‘power grip’ towards a ‘precision grip’, supposed to behavioural characters is also determined. We also have taken place in hominids; the precision grip has been present models that enable inference of behaviours from suggested to appear with Australopithecus afarensis (Mar- morphological characters, which we use to infer behav- zke, 1997) or with Homo (Napier, 1956, 1960). The power iours in three extinct primates: Proconsul africanus, grip is defined as a grasp with the palm, and is probably a Oreopithecus bambolii and Australopithecus afarensis, three species considered to have divergent grasping abilities. Correspondence: Michel Laurin, Comparative Osteohistology, UMR CNRS Proconsul africanus and Australopithecus afarensis are from 7179, Universite´ Pierre et Marie Curie (Paris 6), Paris, France. Africa, which is probably the cradle of hominoid diver- Tel.: (33) 1 44 27 36 92; e-mail: [email protected] sification (Arnason et al., 2000; Folinsbee & Brooks, ª 2008 THE AUTHORS. J. EVOL. BIOL. 21 (2008) 1732–1743 1732 JOURNAL COMPILATION ª 2008 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Evolution of grasping among anthropoids 1733 2007). Oreopithecus bambolii was found in Tuscany, Italy. object by using frame-by-frame analysis in the labora- It is included here because its prehensile behaviour has tory. We obtained a minimum of 90 min of observation been inferred in the literature (Moya´-Sola´ et al., 1999; of grasping behaviour for each chimpanzee, baboon, Susman, 2004). macaque and capuchin, and 180 min for each orang- utan, gorilla and gibbon. Material and methods Frame-by-frame analysis was performed with a Basler camera (Basler, Ahrensburg, Germany), recording 250 images per second. Each prehension technique was Quantification of areas of contact characterized by contacts between one or several lateral Subjects or ventral areas of a minimum of two digits or the The data represented in this study are based on a wide complete palm. From this analysis, we determined five variety of primates observed in captivity (Appendix S1): categories of object prehension. nine capuchins (C. apella), nine macaques (Macaca fuscata), nine baboons (Papio papio), three gibbons Size and nature of the objects (Hylobates lar), seven orang-utans (Pongo pygmaeus), three For all primates except humans, the objects were small gorillas (G. gorilla) and 14 chimpanzees (P. troglodytes). and scattered on the ground; the objects involved We also have observations from nine children, 2–5 years spherical cereals and fruits. In humans, the objects were of age (Homo sapiens), and nine adults (H. sapiens). Data spherical pearls. It was necessary to standardize the for three other species were collected from the literature diameter and the volume in order to calibrate these (Christel, 1993; Christel et al., 1998): black mangabey parameters according to the length of the hand of the (Cercocebus aterrimus), geladas (Theropithecus gelada) and species studied. In this paper, we always presented bonobos (Pan paniscus). These species represent a wide spherical objects to the animals and determined their array of body size, hand morphological traits and diameter. The diameter of the objects was calibrated anthropoid taxa. Indeed, capuchins do not possess an according to the length of the hand of the species. As we opposable thumb and none of the studied primate species knew the length of the hand of the smallest studied except humans has morphological traits usually associ- species (76.2 ± 5.3 mm for capuchin) and the diameter ated with precision grip. of the smallest object (3.0 ± 0.1 mm) grasped by this species, we deduced the diameter of objects for other Protocol of observations species as follows (D = diameter, L = length, all units The observations of grasping of small and large objects in mm): have been made in various groups of animals belonging to zoological gardens in France. All individuals observed D object for species x ¼L hand of the species xÂ3:0=76:2 in any given species belong to a single group and the For example, to calculate the diameter of objects to be hierarchical position of each specimen was established. grasped by chimpanzees, we used the length of the The animals were observed without modification of their chimpanzee’s hand (235.0 mm) and that of the smallest social (within their group) or environmental (e.g. logs, hand (the capuchins’ hand: 76.2 mm) and the diameter rocks, ropes) context to maintain: (i) all behavioural of the smallest object (3.0 mm). In this example, Dxc interactions between the members of the group; (ii) all corresponds to the determined diameter of the small constraints in relation to the environment; and (iii) all object for chimpanzees (c). We calculated the following possibility of opportunistic manipulation (Parker & value for objects in chimpanzees: Dxc is equal to 9.0 mm Gibson, 1977). (235.0 mm · 3.0 ⁄ 76.2). We followed the same method All observations of the animals were made for to calculate the diameter of objects for each species 7 months (Pouydebat, 2004). The duration of observa- (Appendix S2). tion for each specimen was standardized following the usual methods suggested in comparative ethology Number of grasps (Lehner, 1996). A preliminary analysis was conducted by A total of 5549 grasps were recorded for the eight studied ‘ad libitum sampling’ (Altmann, 1974) that permits the species (Table 1). The percentage of each prehension individual recognition of all subjects for each species and category was calculated on the basis of the total number the identification of a wide variety of areas of fingers in of grasping observed in each species. contact with the presented objects. During the study, each individual was observed according to the method of Morphometric data ‘focal animal sampling’ (Altmann, 1974). We filmed the Morphometric data were obtained from hand skeletons animals during two sessions of 2 h each for chimpanzees, belonging to the collection of the Muse´um National baboons, capuchins and macaques and six sessions of 2 h d’Histoire Naturelle (Paris). Our sample consisted of 17 each for orang-utans, gorillas and gibbons. Every 15 min, measurements of the hand of 26 taxa (Appendix S3). A sequences of grasping which lasted 5 min were
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