Getting a grip on tetrapod grasping: form, function, and evolution

Human beings have been credited with unparalleled capabilities for digital prehension grasping. However, grasping behaviour is widespread among tetrapods. The propensity to grasp, and the anatomical characteristics that underlie it, appear in all of the major groups of tetrapods with the possible exception of terrestrial turtles. Although some features are synapomorphic to the tetrapod clade, such as well‐defined digits and digital musculature, other features, such as opposable digits and tendon configurations, appear to have evolved independently in many lineages. Here we examine the incidence, functional morphology, and evolution of grasping across four major tetrapod clades. Our review suggests that the ability to grasp with the manus and pes is considerably more widespread, and ecologically and evolutionarily important, than previously thought. The morphological bases and ecological factors that govern grasping abilities may differ among tetrapods, yet the selective forces shaping them are likely similar. We suggest that further investigation into grasping form and function within and among these clades may expose a greater role for grasping ability in the evolutionary success of many tetrapod lineages.

[1]  G. E. Goslow Adaptive Mechanisms of the Raptor Pelvic Limb , 1972 .

[2]  K. Nishikawa,et al.  Evolution of forelimb movement patterns for prey manipulation in anurans. , 1997, The Journal of experimental zoology.

[3]  K. Dial Avian Flight , 2006 .

[4]  C. Gans,et al.  ON THE ORIGIN OF THE JUMPING MECHANISM IN FROGS , 1966, Evolution; international journal of organic evolution.

[5]  A. Pusey The behavior guide to African mammals: by Richard Despard Estes, University of California Press, 1991. $75.00 hbk (xxii + 611 pages) ISBN 0 520 05831 3 , 1992 .

[6]  P Gorce,et al.  Evolution of grasping among anthropoids , 2008, Journal of evolutionary biology.

[7]  L. Trueb,et al.  Biology of Amphibians , 1986 .

[8]  P. Lemelin Micro-anatomy of the volar skin and interordinal relationships of primates. , 2000, Journal of human evolution.

[9]  R. Raikow Climbing adaptations in the hindlimb musculatures of the woodcreepers (Dendrocolaptinae) , 1994 .

[10]  W. Maclennan,et al.  The Locomotor System , 1984 .

[11]  J. Thewissen,et al.  Adhesive Devices on the Thumb of Vespertilionoid Bats (Chiroptera) , 1995 .

[12]  L. Einoder,et al.  The digital tendon locking mechanism of owls: variation in the structure and arrangement of the mechanism and functional implications , 2007 .

[13]  S. L. Berman The Hindlimb Musculature of the White-Fronted Amazon (Amazona albifrons, Psittaciformes) , 1984 .

[14]  I. Whishaw,et al.  On the origin of skilled forelimb movements , 2000, Trends in Neurosciences.

[15]  M Illert,et al.  Shaping of the cat paw for food taking and object manipulation: an X‐ray analysis , 1998, The European journal of neuroscience.

[16]  J. R. Napier,et al.  The Natural History Of The Primates , 1985 .

[17]  Mark R. Cutkosky,et al.  On grasp choice, grasp models, and the design of hands for manufacturing tasks , 1989, IEEE Trans. Robotics Autom..

[18]  Holger Preuschoft,et al.  Environment, behavior, and morphology: dynamic interactions in primates , 1979 .

[19]  V. Abdala,et al.  Comparative anatomy, homologies and evolution of the pectoral and forelimb musculature of tetrapods with special attention to extant limbed amphibians and reptiles , 2010, Journal of anatomy.

[20]  A. Herrel,et al.  Is phylogeny driving tendon length in lizards , 2012 .

[21]  Alan M. Wilson,et al.  Muscle architecture and functional anatomy of the pelvic limb of the ostrich (Struthio camelus) , 2006, Journal of anatomy.

[22]  D. Sustaita Musculoskeletal underpinnings to differences in killing behavior between North American accipiters (Falconiformes: Accipitridae) and falcons (Falconidae) , 2008, Journal of morphology.

[23]  Ian Q. Whishaw,et al.  Brain Size Is Not Correlated with Forelimb Dexterity in Fissiped Carnivores (Carnivora): A Comparative Test of the Principle of Proper Mass , 1999, Brain, Behavior and Evolution.

[24]  R. Kambic Multivariate analysis of avian and non-avian theropod pedal phalanges , 2008 .

[25]  M. Hamrick Development and evolution of the mammalian limb: adaptive diversification of nails, hooves, and claws , 2001, Evolution & development.

[26]  Y. Coppens,et al.  La préhension chez les Primates : précision, outils et perspectives évolutives , 2006 .

[27]  B. Wood,et al.  Soft‐tissue anatomy of the primates: phylogenetic analyses based on the muscles of the head, neck, pectoral region and upper limb, with notes on the evolution of these muscles , 2011, Journal of anatomy.

[28]  E. J. Sargis The grasping behaviour, locomotion and substrate use of the tree shrews Tupaia minor and T. tana (Mammalia, Scandentia) , 2001 .

[29]  Gerald W. Cortright Functional morphology of the evolving hand and foot , 1991, International Journal of Primatology.

[30]  John R Hutchinson,et al.  The evolution of hindlimb tendons and muscles on the line to crown-group birds. , 2002, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[31]  G. Clark Holding Food with the Feet in Passerines , 1973 .

[32]  R. Howe,et al.  Human grasp choice and robotic grasp analysis , 1990 .

[33]  K. Nekaris Foraging behaviour of the slender loris (Loris lydekkerianus lydekkerianus): implications for theories of primate origins. , 2005, Journal of human evolution.

[34]  M. Latash,et al.  Prehension Synergies , 2004, Exercise and sport sciences reviews.

[35]  R. Reynolds,et al.  Partitioning of Food and Niche Characteristics of Coexisting Accipiter During Breeding , 1984 .

[36]  J. Landsmeer Power Grip and Precision Handling , 1962, Annals of the rheumatic diseases.

[37]  M. Schieber Individuated finger movements of rhesus monkeys: a means of quantifying the independence of the digits. , 1991, Journal of neurophysiology.

[38]  J. Schwartzkopff Chapter 7 – MECHANORECEPTION , 1973 .

[39]  E. Pianka,et al.  Monitors , Mammals , and Wallace ’ s Line , 2007 .

[40]  A. Herrel,et al.  Slow but tenacious: an analysis of running and gripping performance in chameleons , 2013, Journal of Experimental Biology.

[41]  A. Pike,et al.  Scaling of bird claws , 2004 .

[42]  MH Schieber Muscular production of individuated finger movements: the roles of extrinsic finger muscles , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  D. Ksepka,et al.  A New Stem Parrot from the Green River Formation and the Complex Evolution of the Grasping Foot in Pan-Psittaciformes , 2012 .

[44]  A. Bishop Chapter 12 – Use of the Hand in Lower Primates , 1964 .

[45]  V. Bels,et al.  Food Prehension and Manipulation in Microcebus murinus (Prosimii, Cheirogaleidae) , 2011, Folia Primatologica.

[46]  I. Whishaw,et al.  The relationships between brain regions and forelimb dexterity in marsupials (Marsupialia): a comparative test of the principle of proper mass , 2000 .

[47]  A. Adams,et al.  The Muscular System , 2004 .

[48]  W. Barnes,et al.  Adhesion and Detachment of the Toe Pads of Tree Frogs , 1991 .

[49]  C. Woolsey,et al.  The Pyramidal Tract , 1957, Neurology.

[50]  K. Bard,et al.  Precision grips in young chimpanzees , 1996, American journal of primatology.

[51]  D. Gebo The nature of the primate grasping foot , 1985 .

[52]  A. Feduccia The origin and evolution of birds , 1996 .

[53]  M. Ravosa,et al.  PRIMATE ORIGINS: Adaptations and evolution , 2007 .

[54]  Philippe Gorce,et al.  Diversity of grip in adults and young humans and chimpanzees (Pan troglodytes) , 2011, Behavioural Brain Research.

[55]  B. Siemers,et al.  The sensory basis of prey detection in captive-born grey mouse lemurs, Microcebus murinus , 2008, Animal Behaviour.

[56]  C. J. Erickson,et al.  Independent digit control in foraging by the aye-aye (Daubentonia madagascariensis). , 1991, Folia primatologica; international journal of primatology.

[57]  W. A. Cox,et al.  A Phylogenomic Study of Birds Reveals Their Evolutionary History , 2008, Science.

[58]  Ian Q. Whishaw,et al.  Skilled reaching in rats and humans: evidence for parallel development or homology , 1992, Behavioural Brain Research.

[59]  Walter Joseph Bock,et al.  The scansorial foot of the woodpeckers, with comments on the evolution of perching and climbing feet in birds. American Museum novitates ; no. 1931 , 1959 .

[60]  Mark R. Cutkosky,et al.  Friction, Stability and the Design of Robotic Fingers , 1986 .

[61]  S. Reilly,et al.  Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking , 1997 .

[62]  A. Herrel,et al.  The interplay between claw morphology and microhabitat use in neotropical iguanian lizards. , 2009, Zoology.

[63]  M. Cartmill Rethinking primate origins. , 1974, Science.

[64]  A. Herrel,et al.  Morphology and function of the forelimb in arboreal frogs: specializations for grasping ability? , 2008, Journal of anatomy.

[65]  Zani The comparative evolution of lizard claw and toe morphology and clinging performance , 2000 .

[66]  D. Youlatos Hallucal grasping behavior in Caluromys (Didelphimorphia: Didelphidae): Implications for primate pedal grasping. , 2008, Journal of human evolution.

[67]  Ian D. Walker,et al.  Raptors-inroads to multifingered grasping , 1998, Proceedings. 1998 IEEE/RSJ International Conference on Intelligent Robots and Systems. Innovations in Theory, Practice and Applications (Cat. No.98CH36190).

[68]  V. Abdala,et al.  Sesamoids in Anurans: New Data, Old Issues , 2010, Anatomical record.

[69]  T. H. Quinn,et al.  Chiropteran tendon locking mechanism , 1993, Journal of morphology.

[70]  V. Bracha,et al.  The reaching reaction in the rat: A part of the digging pattern? , 1990, Behavioural Brain Research.

[71]  Matthew W. Tocheri,et al.  The evolutionary history of the hominin hand since the last common ancestor of Pan and Homo , 2008, Journal of anatomy.

[72]  F. Szalay,et al.  Evolution of hallucial grasping in the primates , 1988 .

[73]  M. Haffner A tendon‐locking mechanism in two climbing rodents, Muscardinus avellanarius and Micromys minutus (Mammalia, Rodentia) , 1996, Journal of morphology.

[74]  Michael E Alfaro,et al.  Evolutionary Consequences of Many‐to‐One Mapping of Jaw Morphology to Mechanics in Labrid Fishes , 2005, The American Naturalist.

[75]  N. Shubin,et al.  An Early Jurassic jumping frog , 1995, Nature.

[76]  A. Feduccia,et al.  Evidence from Claw Geometry Indicating Arboreal Habits of Archaeopteryx , 1993, Science.

[77]  M. Cartmill 2 – Pads and Claws in Arboreal Locomotion , 1974 .

[78]  L. Harris,et al.  Footedness in parrots: three centuries of research, theory, and mere surmise. , 1989, Canadian journal of psychology.

[79]  M W Marzke,et al.  Precision grips, hand morphology, and tools. , 1997, American journal of physical anthropology.

[80]  M. L. Allen,et al.  Adult Gray Jay Captures an Adult Black-capped Chickadee , 2004 .

[81]  R. K. Rose,et al.  Volar adhesive pads of the feathertail glider, Acrobates pygmaeus (Marsupialia; Acrobatidae) , 1999 .

[82]  K. Kardong,et al.  Vertebrates: Comparative Anatomy, Function, Evolution , 1994 .

[83]  Mary W. Marzke,et al.  Chimpanzee and human grips: A new classification with a focus on evolutionary morphology , 1996, International Journal of Primatology.

[84]  Robert D. Howe,et al.  Joint coupling design of underactuated hands for unstructured environments , 2011, Int. J. Robotics Res..

[85]  Karel F. Liem,et al.  Functional Anatomy of the Vertebrates: An Evolutionary Perspective , 1994 .

[86]  F. Hertel,et al.  In vivo bite and grip forces, morphology and prey-killing behavior of North American accipiters (Accipitridae) and falcons (Falconidae) , 2010, Journal of Experimental Biology.

[87]  M Watson,et al.  The Mechanism of Perching in Birds. , 1869, Journal of anatomy and physiology.

[88]  Brian G Richmond,et al.  Hand pressure distribution during Oldowan stone tool production. , 2012, Journal of human evolution.

[89]  T. Grand Body weight: its relation to tissue composition, segment distribution, and motor function. I. Interspecific comparisons. , 1977, American journal of physical anthropology.

[90]  H. Lillywhite,et al.  Body wiping behaviors associated with cutaneous lipids in hylid tree frogs of Florida , 2005, Journal of Experimental Biology.

[91]  R. Byrne,et al.  Manual dexterity in the gorilla: bimanual and digit role differentiation in a natural task , 2001, Animal Cognition.

[92]  Manipulierfähigkeit eines Wickelbären bei längeren Handlungsketten , 1969 .

[93]  R. Haines,et al.  The flexor muscles of the forearm and hand in lizards and mammals. , 1950, Journal of anatomy.

[94]  M. Hamrick Morphological diversity in digital skin microstructure of didelphid marsupials , 2001, Journal of anatomy.

[95]  B. Siemers,et al.  Sensory Basis of Food Detection in Wild Microcebus murinus , 2007, International Journal of Primatology.

[96]  L. Rome,et al.  Built for jumping: the design of the frog muscular system. , 1994, Science.

[97]  C. Byron,et al.  Rudimentary pedal grasping in mice and implications for terminal branch arboreal quadrupedalism , 2011, Journal of morphology.

[98]  G. Visser,et al.  Review of reproduction of Monitor lizards Varanus spp in captivity II , 1988 .

[99]  J. Losos,et al.  THE EVOLUTION OF FORM AND FUNCTION: MORPHOLOGY AND LOCOMOTOR PERFORMANCE IN WEST INDIAN ANOLIS LIZARDS , 1990, Evolution; international journal of organic evolution.

[100]  T. Cade The falcons of the world , 1982 .

[101]  J. Napier The prehensile movements of the human hand. , 1956, The Journal of bone and joint surgery. British volume.

[102]  M. Dagosto The Postcranial Morphotype of Primates , 2007 .

[103]  S. Reilly,et al.  Landing in basal frogs: evidence of saltational patterns in the evolution of anuran locomotion , 2010, Naturwissenschaften.

[104]  S. Gatesy,et al.  LOCOMOTOR MODULES AND THE EVOLUTION OF AVIAN FLIGHT , 1996, Evolution; international journal of organic evolution.

[105]  A. Billard,et al.  Comparison between macaques’ and humans’ kinematics of prehension: the role of morphological differences and control mechanisms , 2002, Behavioural Brain Research.

[106]  T. Kohlsdorf,et al.  Limb and tail lengths in relation to substrate usage in Tropidurus lizards , 2001, Journal of morphology.

[107]  R. E. Kambic,et al.  The Predatory Ecology of Deinonychus and the Origin of Flapping in Birds , 2011, PloS one.

[108]  R. Wunderlich,et al.  Hand and foot pressures in the aye-aye (Daubentonia madagascariensis) reveal novel biomechanical trade-offs required for walking on gracile digits , 2010, Journal of Experimental Biology.

[109]  Peter Aerts,et al.  Functional anatomy of the gibbon forelimb: adaptations to a brachiating lifestyle , 2009, Journal of anatomy.

[110]  D. Brinkman Structural correlates of tarsal and metatarsal functioning in Iguana (Lacertilia; Iguanidae) and other lizards , 1980 .

[111]  I. Whishaw,et al.  How skilled are the skilled limb movements of the raccoon (Procyon lotor)? , 1999, Behavioural Brain Research.

[112]  D. McClearn,et al.  Locomotion, Posture, and Feeding Behavior of Kinkajous, Coatis, and Raccoons , 1992 .

[113]  S. Viegas,et al.  Evolution of the power ("squeeze") grip and its morphological correlates in hominids. , 1992, American journal of physical anthropology.

[114]  V. Abdala,et al.  Relationships among morphology, clinging performance and habitat use in Liolaemini lizards , 2011, Journal of evolutionary biology.

[115]  D. Fowler,et al.  Predatory Functional Morphology in Raptors: Interdigital Variation in Talon Size Is Related to Prey Restraint and Immobilisation Technique , 2009, PloS one.

[116]  R. L. Susman Hand function and tool behavior in early hominids. , 1998, Journal of human evolution.

[117]  Timothy E Higham,et al.  Locomotion of lizards on inclines and perches: hindlimb kinematics of an arboreal specialist and a terrestrial generalist , 2004, Journal of Experimental Biology.

[118]  Noble S. Proctor,et al.  Manual of Ornithology: Avian Structure and Function , 1993 .

[119]  T. Burton VARIATION IN THE HAND AND SUPERFICIAL THROAT MUSCULATURE OF NEOTROPICAL LEPTODACTYLID FROGS , 1998 .

[120]  Ron Shahar,et al.  Morphometric and anatomic study of the forelimb of the dog , 2005, Journal of morphology.

[121]  M. Fischer,et al.  Evolution of chameleon locomotion, or how to become arboreal as a reptile. , 2010, Zoology.

[122]  P. Wainwright Ecological Explanation through Functional Morphology: The Feeding Biology of Sunfishes , 1996 .

[123]  J. Buettner‐Janusch The Antecedents of Man , 1963, The Yale Journal of Biology and Medicine.

[124]  Kiisa Nishikawa,et al.  Electromyography and the evolution of motor control: limitations and insights. , 2008, Integrative and comparative biology.

[125]  Adam D. Sylvester,et al.  Locomotor decoupling and the origin of hominin bipedalism. , 2006, Journal of theoretical biology.

[126]  D. Boire,et al.  Brain regions and encephalization in anurans: adaptation or stability? , 1995, Brain, behavior and evolution.

[127]  T. H. Quinn,et al.  The digital tendon locking mechanism of the avian foot (Aves) , 1990, Zoomorphology.

[128]  Haines Rw The flexor muscles of the forearm and hand in lizards and mammals. , 1950 .

[129]  Valentina Truppa,et al.  Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item. , 2004, American journal of physical anthropology.

[130]  P. Aerts,et al.  Functional morphology of the hindlimb musculature of the black-billed magpie, Pica pica (Aves, Corvidae) , 1998, Zoomorphology.

[131]  F. Szalay Evolutionary history of the marsupials and an analysis of osteological characters: References , 1995 .

[132]  D. Boyer,et al.  Evolution of pedal grasping in Primates. , 2007, Journal of human evolution.

[133]  O. Rossi,et al.  Bird claws and bird of prey talons: Where is the difference? , 2006 .

[134]  V. Abdala,et al.  Muscles of Vertebrates: Comparative Anatomy, Evolution, Homologies and Development , 2010 .

[135]  S. Moro,et al.  Análisis descriptivo de la miología flexora y extensora del miembro anterior de Polychrus acutirostris (Squamata, Polychrotidae) , 2004 .

[136]  H. Endo,et al.  Three-dimensional analysis of the manipulation system in the lesser panda , 2007 .

[137]  T. Burton Adaptation and Evolution in the Hand Muscles of Australo-Papuan Hylid Frogs (Anura: Hylidae: Pelodryadinae) , 1996 .

[138]  J. Schwartzkopff,et al.  Über Sitz und Leistung von Gehör und Vibrationssinn bei Vögeln , 1949, Zeitschrift für vergleichende Physiologie.

[139]  E. Moreno Musculature of the pelvic appendages of the treecreepers (Passeriformes : Certhiidae) myological adaptations for tail-supported climbing , 1991 .

[140]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[141]  S Grillner,et al.  Central pattern generators for locomotion, with special reference to vertebrates. , 1985, Annual review of neuroscience.

[142]  M. Vences,et al.  Intercalary Elements, Treefrogs, and the Early Differentiation of a Complex System in the Neobatrachia , 2007, Anatomical record.

[143]  M. Cartmill Arboreal Adaptations and the Origin of the Order Primates , 1972 .

[144]  N. J. Seo,et al.  Tactile feedback plays a critical role in maximum finger force production. , 2012, Journal of biomechanics.

[145]  R. Martin Primate origins and evolution , 1990 .

[146]  G. Rizzato,et al.  The locomotor system , 1994 .

[147]  Philippe Gorce,et al.  Biomechanical study of grasping according to the volume of the object: human versus non-human primates. , 2009, Journal of biomechanics.

[148]  I. Lennerstedt A Functional Study of Papillae and Pads in the Foot of Passerines, Parrots, and Owls , 1975 .

[149]  F. Hertel ECOMORPHOLOGICAL INDICATORS OF FEEDING BEHAVIOR IN RECENT AND FOSSIL RAPTORS , 1995 .

[150]  Marc H Schieber,et al.  Hand function: peripheral and central constraints on performance. , 2004, Journal of applied physiology.

[151]  R. Van Damme,et al.  Limb proportions in climbing and ground-dwelling geckos (Lepidosauria, Gekkonidae): a phylogenetically informed analysis , 2001, Zoomorphology.

[152]  Mariam Alaverdashvili,et al.  Similar hand shaping in reaching-for-food (skilled reaching) in rats and humans provides evidence of homology in release, collection, and manipulation movements , 2009, Behavioural Brain Research.

[153]  S. Emerson,et al.  Toe pad morphology and mechanisms of sticking in frogs , 1980 .

[154]  J. Petter ECOLOGICAL AND BEHAVIORAL STUDIES OF MADAGASCAR LEMURS IN THE FIELD , 1962, Annals of the New York Academy of Sciences.

[155]  M W Marzke,et al.  Chimpanzee thumb muscle cross sections, moment arms and potential torques, and comparisons with humans. , 1999, American journal of physical anthropology.

[156]  M. Marzke,et al.  Evolution of the human hand: approaches to acquiring, analysing and interpreting the anatomical evidence , 2000, Journal of anatomy.

[157]  P. Galton,et al.  Experimental analysis of perching in the European starling (Sturnus vulgaris: Passeriformes; Passeres), and the automatic perching mechanism of birds. , 2012, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[158]  S. Larson,et al.  Telemetered electromyography of peroneus longus in Varecia variegata and Eulemur rubriventer: implications for the functional significance of a large peroneal process. , 2007, Journal of human evolution.

[159]  D. Csermely,et al.  Prey killing by Eurasian Kestrels: the role of the foot and the significance of bill and talons , 1998 .

[160]  W. E. Clark The Problem of the Claw in Primates , 1936 .

[161]  P. Raven,et al.  Pollination by Lemurs and Marsupials: An Archaic Coevolutionary System , 1978, Science.

[162]  M. Gimenes POLLINATING BEES AND OTHER VISITORS OF LUDWIGIA ELEGANS (ONAGRACEAE) FLOWERS AT A TROPICAL SITE IN BRAZIL , 1997 .

[163]  K. Middleton The morphological basis of hallucal orientation in extant birds , 2001, Journal of morphology.

[164]  Morphology of the hallucial phalanges in extant anthropoids and fossil hominoids. , 2002, Zeitschrift fur Morphologie und Anthropologie.

[165]  M. Studdert-Kennedy,et al.  Primate handedness reconsidered , 1987, Behavioral and Brain Sciences.

[166]  Mark A. Minor,et al.  Avian-inspired passive perching mechanism for robotic rotorcraft , 2011, 2011 IEEE/RSJ International Conference on Intelligent Robots and Systems.

[167]  A. Herrel,et al.  The Tendinous Patterns in the Palmar Surface of the Lizard Manus: Functional Consequences for Grasping Ability , 2009, Anatomical record.

[168]  W. A. Wimsatt,et al.  Locomotor adaptations in the disc-winged bat thyroptera tricolor. I. Functional organization of the adhesive discs. , 1970, The American journal of anatomy.

[169]  J. A. Brush,et al.  Phalangeal morphology of the paromomyidae (?primates, plesiadapiformes): the evidence for gliding behavior reconsidered. , 1999, American journal of physical anthropology.

[170]  M. Christel Grasping techniques and hand preferences in Hominoidea , 1993 .

[171]  R. Winkelmann,et al.  The histochemistry and morphology of the cutaneous sensory end‐organs of the chicken , 1961, The Journal of comparative neurology.

[172]  M. Cartmill,et al.  Footfall patterns and interlimb co‐ordination in opossums (Family Didelphidae): evidence for the evolution of diagonal‐sequence walking gaits in primates , 2003 .

[173]  M. Hamrick,et al.  Functional and adaptive significance of primate pads and claws: evidence from New World anthropoids. , 1998, American journal of physical anthropology.

[174]  C. Argot Functional‐adaptive analysis of the hindlimb anatomy of extant marsupials and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus , 2002, Journal of morphology.

[175]  Michael M Günther,et al.  Functional adaptations in the forelimb muscles of non‐human great apes , 2012, Journal of anatomy.

[176]  Culum Brown,et al.  The Evolution of lateralized foot use in parrots : a phylogenetic approach , 2011 .

[177]  R. Estes,et al.  The Behavior Guide to African Mammals: Including Hoofed Mammals, Carnivores, Primates , 1991 .

[178]  David Payne,et al.  Dinosaur killer claws or climbing crampons? , 2006, Biology Letters.

[179]  D. Rasmussen Primate origins: Lessons from a neotropical marsupial , 1990, American journal of primatology.

[180]  P. Lemelin,et al.  Origins of primate locomotion: gait mechanics of the woolly opossum. , 2002, American journal of physical anthropology.

[181]  G. K. Noble The Biology of the Amphibia , 1954 .

[182]  M. Pagel Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[183]  S. Pellis,et al.  Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species , 1998, Behavioural Brain Research.

[184]  V. Bels,et al.  Influence of the Task on Hand Preference: Individual Differences among Gorillas (Gorilla gorilla gorilla) , 2011, Folia Primatologica.

[185]  K. Congdon Interspecific and Ontogenetic Variation in Proximal Pedal Phalangeal Curvature of Great Apes (Gorilla gorilla, Pan troglodytes, and Pongo pygmaeus) , 2012, International Journal of Primatology.

[186]  Thomas W. Schoener,et al.  15. Size Differences Among Sympatric, Bird-Eating Hawks: A Worldwide Survey , 1984 .

[187]  G. Yanega A comparative study of the functional morphology and ecology of insectivory in hummingbirds , 2007 .

[188]  M. Hamrick Primate origins: evolutionary change in digital ray patterning and segmentation. , 2001, Journal of human evolution.

[189]  M. Hamrick,et al.  Evolution and development of mammalian limb integumentary structures. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[190]  A. Herrel,et al.  Anatomical Basis of Differences in Locomotor Behavior in Anolis Lizards: A Comparison Between Two Ecomorphs , 2008 .

[191]  Ian Q. Whishaw,et al.  Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems , 1996, Behavioural Brain Research.

[192]  A. Herrel,et al.  The distal forelimb musculature in aquatic and terrestrial turtles: phylogeny or environmental constraints? , 2008, Journal of anatomy.

[193]  I. Whishaw Did a change in sensory control of skilled movements stimulate the evolution of the primate frontal cortex? , 2003, Behavioural Brain Research.

[194]  C. D. Marti FEEDING ECOLOGY OF FOUR SYMPATRIC OWLS , 1974 .

[195]  L. Carrascal,et al.  Morphological evolution and changes in foraging behaviour of island and mainland populations of Blue Tit (Parus caeruleus) — a test of convergence and ecomorphological hypotheses , 2005, Evolutionary Ecology.

[196]  I. Whishaw An endpoint, descriptive, and kinematic comparison of skilled reaching in mice (Mus musculus) with rats (Rattus norvegicus) , 1996, Behavioural Brain Research.

[197]  R. A. Davidoff The pyramidal tract. , 1990, Neurology.

[198]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[199]  W. Rymer,et al.  Extrinsic flexor muscles generate concurrent flexion of all three finger joints. , 2002, Journal of biomechanics.

[200]  P. Sereno,et al.  Early Evolution of Avian Flight and Perching: New Evidence from the Lower Cretaceous of China , 1992, Science.

[201]  A. Russell,et al.  The aponeuroses of the lacertilian ankle , 1993, Journal of morphology.

[202]  L. Einoder,et al.  ASPECTS OF THE HINDLIMB MORPHOLOGY OF SOME AUSTRALIAN BIRDS OF PREY: A COMPARATIVE AND QUANTITATIVE STUDY , 2007 .

[203]  Mark W. Westneat,et al.  Vertebrates: Comparative Anatomy, Function, Evolution.— Kenneth V. Kardong. 1998. Second Edition. McGraw-Hill, Boston, Massachusetts , 1998 .

[204]  P. Moler,et al.  THE AMPHIBIAN TREE OF LIFE , 2006 .

[205]  John R Hutchinson,et al.  Biomechanical modeling and sensitivity analysis of bipedal running ability. I. Extant taxa , 2004, Journal of morphology.

[206]  R. Raikow,et al.  The Hindlimb Musculature of the Mousebirds (Coliiformes) , 1982 .

[207]  V. Bels,et al.  Hand posture in the grey mouse lemur during arboreal locomotion on narrow branches , 2012 .

[208]  P. Aerts,et al.  Functional analysis of the foot and ankle myology of gibbons and bonobos , 2005, Journal of anatomy.

[209]  D. Youlatos,et al.  Use of forest canopy by European red squirrelsSciurus vulgaris in Northern Greece: claws and the small branch niche , 2010, Acta Theriologica.

[210]  A. Herrel,et al.  Functional consequences of morphological differentiation between populations of the Cape Dwarf Chameleon (Bradypodion pumilum) , 2011 .

[211]  P. D. Weigl,et al.  FUNCTIONAL MORPHOLOGY OF RAPTOR HINDLIMBS: IMPLICATIONS FOR RESOURCE PARTITIONING , 2002 .

[212]  N. Simmons,et al.  Evolution of the digital tendon locking mechanism in bats and dermopterans: A phylogenetic perspective , 1994, Journal of Mammalian Evolution.

[213]  Daniel E Lieberman,et al.  Hand biomechanics during simulated stone tool use. , 2011, Journal of human evolution.

[214]  T. Grand Body Weight: its Relationship to Tissue Composition, Segmental Distribution of Mass, and Motor Function III.* The Didelphidae of French Guyana , 1983 .

[215]  P. Aerts,et al.  Take-off and landing forces in jumping frogs , 2006, Journal of Experimental Biology.

[216]  A. Goswami,et al.  Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats , 2011, Journal of evolutionary biology.

[217]  C. E. Grelle Forest Structure and Vertical Stratification of Small Mammals in a Secondary Atlantic Forest, Southeastern Brazil , 2003 .

[218]  A. Channing,et al.  Comparison of toe pads of some southern African climbing frogs , 1983 .

[219]  R. Raikow Monophyly of the Passeriformes: Test of a Phylogenetic Hypothesis , 1982 .

[220]  Rui Diogo,et al.  Evolution and homologies of primate and modern human hand and forearm muscles, with notes on thumb movements and tool use. , 2012, Journal of human evolution.

[221]  B. Grzimek Grzimek's encyclopedia of mammals , 1990 .

[222]  Rodrigo Kaz,et al.  Finger joint motion generated by individual extrinsic muscles: A cadaveric study , 2008, Journal of orthopaedic surgery and research.

[223]  R. Hoffstetter Phylogénie des Primates. Confrontation des résultats obtenus par les diverses voies d'approche du problème , 1977 .

[224]  C. D. Hulsey,et al.  Many-to-One Mapping of Form to Function: A General Principle in Organismal Design?1 , 2005, Integrative and comparative biology.

[225]  S. Pellis,et al.  REACHING, GRASPING AND MANIPULATION OF FOOD OBJECTS BY TWO TREE KANGAROO SPECIES, DENDROLAGUS LUMHOLTZI AND DENDROLAGUS MATSCHIEI , 1998 .

[226]  R. Norberg,et al.  Treecreeper climbing; mechanics, energetics, and structural adaptations , 1986 .

[227]  Carl J. Erickson,et al.  Percussive Foraging: Stimuli for Prey Location by Aye-Ayes (Daubentonia madagascariensis) , 1998, International Journal of Primatology.

[228]  T. Burton Are the Distal Extensor Muscles of the Fingers of Anurans an Adaptation to Arboreality , 1998 .

[229]  S. Churchill,et al.  Australopithecus sediba Hand Demonstrates Mosaic Evolution of Locomotor and Manipulative Abilities , 2011, Science.

[230]  S. Lehman The Neural and Behavioural Organization of Goal‐Directed Movements , 1990, Neurology.

[231]  H. Pontzer,et al.  The Narrow Niche hypothesis: gray squirrels shed new light on primate origins. , 2011, American journal of physical anthropology.

[232]  G. L. Paukstis,et al.  Evolutionary trends in the morphology of the intercalary phalanx of anuran amphibians , 1991 .

[233]  Robert K. Colwell,et al.  Community Organization Among Neotropical Nectar-Feeding Birds , 1978 .

[234]  F. Hertel,et al.  THE ANTITROCHANTER OF BIRDS: FORM AND FUNCTION IN BALANCE , 2007 .

[235]  T. Garland,et al.  Integrating function and ecology in studies of adaptation: Investigations of locomotor capacity as a model system , 2001 .

[236]  P. Lemelin Morphological correlates of substrate use in didelphid marsupials: implications for primate origins , 1999 .

[237]  L. Einoder,et al.  An ecomorphological study of the raptorial digital tendon locking mechanism , 2006 .

[238]  S. Larson,et al.  Hallucal grasping in Nycticebus coucang: further implications for the functional significance of a large peroneal process. , 2010, Journal of human evolution.

[239]  C. Chiu,et al.  Evolution and development of the primate limb skeleton , 2002 .

[240]  E Trinkaus,et al.  Mechanical advantages of the Neanderthal thumb in flexion: a test of an hypothesis. , 1991, American Journal of Physical Anthropology.

[241]  Stephen M. Gatesy,et al.  Bipedalism, flight, and the evolution of theropod locomotor diversity , 1997 .

[242]  B. Valkenburgh Skeletal indicators of locomotor behavior in living and extinct carnivores , 1987 .

[243]  R. Ruibal,et al.  Skin Structure and Wiping Behavior of Phyllomedusine Frogs , 1976 .

[244]  J. Oates The niche of the potto,Perodicticus potto , 1984, International Journal of Primatology.

[245]  Robert W. Sussman,et al.  Primate origins and the evolution of angiosperms , 1991, American journal of primatology.

[246]  A. Vassallo,et al.  Experimental assessment of problem solving by Milvago chimango (Aves: Falconiformes) , 2007, Journal of Ethology.

[247]  S. J. Arnold,et al.  Morphology, Performance and Fitness , 1983 .

[248]  Christine L. MacKenzie,et al.  The Grasping Hand , 2011, The Grasping Hand.

[249]  D. Amadon,et al.  Eagles, Hawks and Falcons of the World , 1989 .

[250]  Shigeru Watanabe,et al.  Foot-use laterality in the Japanese jungle crow (Corvus macrorhynchos) , 2005, Behavioural Processes.

[251]  R. Pocock The External Characters and Classification of. the Procyonidæ. , 2009 .