3775

The Journal of Experimental Biology 211, 3775-3789 Published by The Company of Biologists 2008 doi:10.1242/jeb.019802

Forelimb proportions and kinematics: how are small primates different from other small mammals?

Manuela Schmidt Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich Schiller Universität Jena, Erbertstrasse 1, D-07743 Jena, Germany e-mail: [email protected]

Accepted 25 September 2008

SUMMARY The crouched limb posture of small mammals enables them to react to unexpected irregularities in the support. Small arboreal primates would benefit from these kinematics in their arboreal habitat but it has been demonstrated that primates display certain differences in forelimb kinematics to other mammals. The objective of this paper is to find out whether these changes in forelimb kinematics are related to changes in body size and limb proportions. As primates descended from small ancestors, a comparison between living small primates and other small mammals makes it possible to determine the polarity of character transformations for kinematic and morphometric features proposed to be unique to primates. Walking kinematics of mouse lemurs, brown lemurs, cotton-top tamarins and squirrel monkeys was investigated using cineradiography. Morphometry was conducted on a sample of 110 mammals comprising of primates, marsupials, rodents and carnivores. It has been shown that forelimb kinematics change with increasing body size in such a way that limb protraction increases but retraction decreases. Total forelimb excursion, therefore, is almost independent of body size. Kinematic changes are linked to changes in forelimb proportions towards greater asymmetry between scapula and radius. Due to the spatial restriction inherent in the diagonal footfall sequence of primates, forelimb excursion is influenced by the excursion of the elongated hind limb. Hindlimb geometry, however, is highly conserved, as has been previously shown. The initial changes in forelimb kinematics might, therefore, be explained as solutions to a constraint rather than as adaptations to the particular demands of arboreal locomotion. Key words: joint kinematics, angular excursion, intralimb proportions, limb length scaling, Microcebus murinus, Eulemur fulvus, Saguinus oedipus, Saimiri sciureus.

INTRODUCTION Tomita, 1967; Shapiro and Raichlen, 2005; Wallace and Demes, A support that has a small diameter relative to the size of an animal 2007), it is superior to the lateral footfall pattern in terms of the places particular challenges on the locomotor performance and dynamic stability of locomotion (control and transfer of moments morphology of the musculoskeletal system. A small-diameter imposed on the body axes). As the diagonally paired fore- and support is inherently unstable; twigs and branches may swing, yield hindlimb make contact with the support concurrently, a dynamic or even break. An animal travelling on such a support has two major weight shift from side to side (=balance) is possible at any moment concerns – balance and compliance. Balance prevents the animal of a stride cycle. At the same time, the other fore- and hindlimbs from falling down. Compliance reduces the branch oscillations, swing forward synchronously, thus counterbalancing the momentum which would otherwise disturb cyclic locomotor performance and on the transverse body axis. Compliance is basically provided by a increase the energy costs of motion enormously. The distinctive crouched limb posture which extant arboreal primates certainly characteristics of primate locomotion – powerful pedal grasping, inherit from their non-primate ancestors. hind limb dominance and diagonal sequence of footfalls (Martin, Along with the locomotion-related primate features listed by 1968; Martin, 1986) – have been interpreted as adaptive solutions Martin (Martin, 1968; Martin, 1986), various relative characters have to locomotion on terminal branches smaller in diameter than the been proposed to be unique to primates: larger limb excursion, animal (Cartmill, 1972; Rose, 1973; Cartmill, 1974; Sussman, 1991; greater step length, lower step frequency and longer limbs Cartmill et al., 2002). Powerful prehensile feet enable primates to (Alexander et al., 1979; Alexander and Maloiy, 1984; Reynolds, influence their substrate reaction forces via simultaneously 1987; Larson et al., 2001). The adaptive advantage of these features transferred substrate reaction moments (Preuschoft, 2002; Witte et for locomotion on narrow branches is discussed in numerous recent al., 2002). The counter-transfer of moments onto the trunk permits publications. For example, lower step frequency means longer a dynamic weight shift from the forelimbs to the hindlimbs similar contact time for the limbs, which significantly reduces the peak to the mechanism proposed by Reynolds (Reynolds, 1985). forces the limbs are subjected to by gravity and, thus, further Combined with a diagonal footfall pattern – hindlimb contact prior enhances the compliance of primate walking (Demes et al., 1990; to contralateral forelimb contact (Hildebrand, 1967) – this enables Schmitt, 1999). Although assessment of the polarity of these relative the hindlimbs to carry most of the body weight at the moment of characters greatly depends on sample composition, phylogenetic forelimb touchdown (Reynolds, 1985; Cartmill et al., 2002). hypotheses have often played a minor role in selecting species for Although the diagonal footfall pattern is less advantageous in terms comparison. Rather, comparative studies between ‘typical’ primates of the static stability of locomotion relating the support polygon of belonging to Cebidae, Cercopithecidae, and even Hominoidea and the limbs to the location of the centre of body mass (Gray, 1944; ‘typical’ members of the artificial taxon ‘non-primates’ (e.g. cats,

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3776 M. Schmidt dogs, horses) form the majority of literature in this field of research. in four species of small arboreal quadruped primates (mouse lemur, Furthermore, small sample size often weakens some of the most brown lemur, cotton-top tamarin and squirrel monkey) with regard frequently cited references. For example, the notion that primates to the kinematic principles displayed by other small mammals: the have longer limb bones and, thus, longer limbs than other mammals predominance of scapula excursion in limb protraction and (Alexander et al., 1979) is based on data from six primate species. retraction, the parallel motion of scapula and forearm and the Reynolds’ assumption (Reynolds, 1987) that primates display function of the intrinsic limb joints in providing limb compliance. greater hindlimb angular excursion is based on a sample of four As the three-segmented fore- and hindlimbs of quadruped primates (chimpanzee, gibbon, spider monkey and brown lemur). mammals are constrained to display the same pivot height and Larson (Larson, 1998) and Larson et al. (Larson et al., 2000; Larson angular excursion, intralimb proportions and the length ratio between et al., 2001) went to great lengths to test the hypothesis proposed fore- and hindlimbs play a crucial role in adjusting limb kinematics by Reynolds on the basis of a much larger sample (53 primates and to certain biomechanical demands such as postural stability and 49 ‘non-primates’ of several phylogenetic groups). Although this stress reduction. A crucial factor in the primate-specific diagonal outstanding sample could potentially have allowed the ancestral sequence gait is the relationship between limb length and body size pattern for each phylogenetic lineage to be derived, the authors because long limbs increase the risk of interference between compared the mean values of each group, making it impossible to ipsilateral fore- and hindlimbs. It can be hypothesized that the estimate character polarity. The comparative evidence relating to relationship between limb length and body size and the ratio between whether limb lengths, angular excursion and step length in primates fore- and hindlimb length act as constraints on limb geometry. are uniquely large thus needs to be surveyed critically with regard Therefore, the second part of this study examines the scaling pattern to character polarity. In an earlier study, Schmidt (Schmidt, 2005a) of forelimb length, the length ratio between forelimbs and hind limbs compared the hindlimb kinematics of small arboreal quadruped and the intralimb proportions of the forelimb. Fischer and Blickhan primates with those of other non-cursorial mammals and suggested demonstrated that the crouched forelimb posture of small mammals that the differences that occur with increasing body size result from is combined with skeletal intralimb scapula, humerus and radius the decreasing angular excursion in cursorial mammals, with larger proportions of approximately 1:1:1 (Fischer and Blickhan, 2006). primates merely retaining the primitive condition of large hindlimb A more extended limb posture requires asymmetrical proportions excursion seen in the smaller primates, tree-shrews, rodents and for self-stability (Seyfarth et al., 2001). In this morphometric part marsupials. of the paper, a broader sample of quadrupeds is considered in an Fischer and his team (Fischer et al., 2002) proposed kinematic attempt to test whether primates in general differ from other principles for the locomotion of small mammals, which is suggested mammals or whether previously suggested differences in limb bone as being adaptive to postural stability in unanticipated situations lengths characterize only larger primates that display more derived within a disordered spatial arrangement of surfaces. These principles locomotor behaviours such as terrestrial quadrupedalism. include a permanent crouched limb posture in which the most Finally, the discussion section proposes a hypothesis about the proximal element is predominant in the protraction and retraction hierarchical structure of dependencies in the character evolution of of the limb. Intrinsic limb joints (shoulder, elbow, knee and ankle) primate locomotion. This section explores the way in which mainly serve to provide limb compliance. It has further been concurrence between initial adaptations to walking on narrow suggested that some of these principles increase the self-stability of supports (prehensile hindlimbs, diagonal footfall sequence and the limb and, thus, minimize neural control effort (Fischer and dynamic weight shift mechanism) and subsequent adaptations to Blickhan, 2006). These are the so-called ‘pantograph behaviour’ other locomotor modes constrain the limb geometry in primates. (parallel motion of scapula and forearm and femur and tarsometatarsus, respectively) and the placement of the forelimb right MATERIALS AND METHODS below the eye. These features characterize the locomotion of small Animals mammals regardless of their phylogeny. Their adaptive advantage Forelimb kinematics were compared in four species of arboreal for locomotion on irregular and uncertain substrates is further evident quadrupedal primates: the grey mouse lemur (Cheirogaleidae: in the re-acquisition of a crouched posture in small-sized mammals Microcebus murinus J. F. Miller 1777), the brown lemur (Lemuridae: that descent from larger-sized ancestors such as the hyraxes Eulemur fulvus E. Geoffroy St Hilaire 1796), the cotton-top tamarin (Hyracoidea), the mouse deer (Tragulidae) or the ferrets (Mustelidae) (Callitrichidae: Saguinus oedipus Linnaeus 1758) and the squirrel (Jenkins, 1971; Fischer et al., 2002). It, therefore, seems reasonable monkey (Cebidae: Saimiri sciureus Linnaeus 1758). Motion analysis to assume that small arboreal primates would benefit greatly from was conducted on two adult individuals of each species. Their body retaining these principles but it has been demonstrated that primates mass, sex and age are listed in Table1. All animals were kept in display a more extended and more protracted forelimb posture at accordance with German animal welfare regulations, and the beginning of a step cycle than other mammals (Larson, 1998; Larson et al., 2000). The ultimate objective of the present study is to find out whether Table 1. Body mass, sex and age of the animals used for the these changes in forelimb posture are related to changes in body kinematic analysis size and/or to changes in the skeletal intra- and interlimb proportions. Individuals Body mass (g) Sex Age (years) Considering the forelimb geometry of other small mammals on the Microcebus murinus 90 Male 2 one hand and the overall uniformity of hindlimb geometry in small Microcebus murinus 110 Male 3 mammals including primates on the other hand, it will be Eulemur fulvus 3.000 Male >20 hypothesized that, in primates, changes in forelimb geometry are Eulemur fulvus 2.100 Female 10 caused by constraints rather than by their increased adaptive value Saguinus oedipus 450 Male 10 for arboreal locomotion on narrow supports. The present paper Saguinus oedipus 520 Female 17 attempts to find out what kind of constraints act on forelimb Saimiri sciureus 1.100 Male 6 geometry. The first part of the study investigates forelimb kinematics Saimiri sciureus 850 Male 3

THE JOURNAL OF EXPERIMENTAL BIOLOGY Forelimb kinematics and proportions in primates 3777 experiments were registered with the Committee for Animal Research of the Freistaat Thüringen, Germany. A Criteria for species selection were derived from the hypotheses placing the adaptive origin of primates in a small branch milieu (Napier, 1967; Cartmill, 1972; Rose, 1973; Sussman, 1991). Accordingly, the animals needed to be small in terms of body size but had to span a significant size range in order for the influence of size variation to be studied. Animals had to use arboreal quadrupedalism as their preferred locomotor mode. The four selected species fulfil these criteria. They prefer to run and walk on horizontal and oblique branches but are also capable of leaping. Grey mouse lemurs are the smallest primates in the world. Cotton- top tamarins and squirrel monkeys are small quadrupedal New BC World monkeys. Lift-off Touchdown Shoulder blade Shoulder joint Retraction Protraction Motion analysis angle angle Animals were habituated to walk on a raised pole or on a horizontal Upper arm Elbow motor-driven rope-mill – an arboreal analogue of a treadmill. The Forearm joint diameter of the support was adapted to the preferred natural substrate of the species (mouse lemur, 10mm; cotton-top tamarin, Hand Total angular Wrist joint excursion 25mm; squirrel monkey, 30mm; brown lemur, 50mm). Data on substrate preferences were obtained from several sources (Walker, 1979; Garber, 1980; Arms et al., 2002). The speed of the rope-mill Fig. 1. Motion analysis: (A) skeletal landmarks of the forelimb exemplified was not fixed but was adjusted to obtain the animal’s preferred on the brown lemur, (B) calculated joint and segment angles, (C) calculated excursion angles of the forelimb. walking velocity. The walking velocity of each species varies moderately. Isolated very slow or very fast strides were excluded from the study. To compensate for differences in body mass across the sample, velocity angular excursions of the forelimb – measured as the angle between was converted into Froude number using the Formula Fr=v2/gl the lines connecting the point of contact with the ground and the (Alexander and Jayes, 1983), where v is raw speed, g is gravitational proximal pivot at touchdown and lift-off (Fig.1C). The proximal acceleration and l is a characteristic length of the animal. The cube pivot of the forelimb is the instantaneous centre of scapular rotation, root of body mass was used here as a characteristic length variable held and guided by muscles. The pivot corresponds to the point of instead of hip height or hindlimb length because geometric similarity zero velocity and is usually marked by the intersection of the two of hindlimb geometry is not present among the four primates. overlaying scapular spines near the vertebral border. The forelimb Uniplanar cineradiographs were collected in lateral view at 150 pivot can thus generally be estimated to be the proximal end of the frames per second. The methods of collecting and processing scapular spine. (5) Protraction angle and retraction angle of the kinematic variables from cineradiographs have been described in detail forelimb – total angular excursion was divided into an anterior and elsewhere (Schmidt, 2005b) and will be summarized only briefly here. a posterior angle by drawing a vertical line through the point of The X-ray equipment consists of an automatic Phillips® unit with one ground contact (Fig.1C). (6) The relationship between anatomical X-ray source which applies pulsed X-ray shots (Institut für den limb length and the shortest functional limb length – distance Wissenschaftlichen Film, Göttingen). The X-ray images were recorded between the proximal pivot and the point of ground contact – at from the image amplifier either onto 35mm film (Arritechno R35- mid-support, which, here, is used as a kinematic key point, namely 150 camera, Arnold & Richter Cine Technik, München, Germany) the vertical alignment of ground contact point and the proximal pivot or using a high-speed CCD camera (Mikromak® Camsys; Mikromak of the limb. The term ‘mid-support’ is normally defined as the instant Service K. Brinkmann, Berlin, Germany). X-ray films were then of the peak vertical substrate reaction force, which nearly coincides analyzed frame-by-frame to identify previously defined skeletal with the instant at which the shoulder joint passes the wrist joint. landmarks (software ‘Unimark’ by R. Voss, Tübingen, Germany) (Fig.1A). The software ‘Unimark’ calculates angles and distances Morphometry based on the x and y coordinates of the landmarks, correcting the Skeletal specimens (N=222) of 110 mammalian species were distortions of the X-ray maps automatically with reference to the x examined at the Phylogenetisches Museum Jena, Germany, at and y coordinates of a recorded grid. the Museum für Naturkunde Berlin, Germany and at the The complete dataset obtained for individuals of the four primate Naturhistorisches Museum Bern, Switzerland. Over 50% of the species in this study includes approximately 13,000 X-ray frames, sample was composed of specimens collected in the wild (N=113), with at least 25 steps analyzed for each species. nine specimens were captured wild and then kept in a zoo. The The following kinematic variables were measured or calculated: remaining specimens died in a zoo and were probably born in (1) segment angles – calculated relative to the horizontal plane (the captivity. The adult status of the specimens was judged on the basis term ‘protraction’ is used for the cranial displacement of the distal of the fusion of the epiphyses of the long bones. In those species end of each segment, ‘retraction’ describes its caudal displacement) for which more than one specimen was available, the largest (Fig.1B). (2) Limb joint angles – defined anatomically and measured specimen in terms of total fore- and hindlimb length was chosen. at the flexor side of each joint (Fig.1B). (3) Maximum amplitudes It was decided not to calculate mean values for each species because of joint excursions during the support phase – difference between the intraspecific and interspecific allometry of limb bones can be maximum extension angle and maximum flexion angle. (4) Total different (e.g. Steudel, 1982). While static intraspecific allometry

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3778 M. Schmidt

Table 2. Morphometry: species (number of specimens), body mass and limb segment lengths

Maximum articular Maximum articular length (mm) length (mm) Body Body Specimen mass (g) Scapula Humerus Radius Specimen mass (g) Scapula Humerus Radius Primates Primates Cheirogaleidae Cercopithecidae Cheirogaleus major 283 25 43 41 Macaca nemestrina 14500* 86 189 183 Microcebus murinus (4) 110 15 23 23 Macaca nigra 4500* 66 144 150 Microcebus myoxinus 31 10 14 15 Macaca sylvanus (3) 7513 74 144 140 Microcebus rufus (3) 70* 14 22 24 Miopithecus talapoin 820* 32 76 75 Lemuridae Papio hamadryas (5) 23500 122 216 222 Eulemur coronatus (2) 1250 35 69 76 Theropithecus gelada (2) 20400 120 203 221 Eulemur fulvus fulvus (4) 2500 46 88 93 Colobus badius (2) 6250 58 138 132 Eulemur fulvus collaris (2) 2110 43 84 91 Colobus guereza 9800 76 158 155 Eulemur fulvus albifrons 2250 43 84 88 Colobus pennantii 7000* 57 144 141 Eulemur macaco (3) 2400* 40 86 89 Colobus polykomos 9000* 66 145 139 Eulemur mongoz (2) 1685 40 74 77 Nasalis larvatus (4) 7000 58 192 198 Hapalemur griseus (2) 895 32 59 66 Presbytis melalophos (2) 6300 60 141 152 Lemur catta (3) 2680* 47 92 96 Pygathrix nemaeus (4) 8000* 56 188 200 Varecia variegata (4) 3520 54 106 102 Trachypithecus obscurus 6000* 54 137 137 Galagonidae Scandentia Galago alleni (2) 314 23 43 45 Tupaia glis (2) 200 23 30 28 Galago senegalensis 193* 16 30 31 Tupaia glis belangeri (2) 200 22 30 26 Otolemur crassicaudatus (4) 1122 32 59 61 Tupaia minor 80 17 23 21 Otolemur garnetti 725 36 59 66 Tupaia tana 230 25 34 33 Loridae Marsupialia Arctocebus aureus (2) 210* 22 61 59 Chironectes minimus 400* 31 41 38 Loris tardigradus (3) 223 22 63 71 Dasyuroides byrnei 158 21 26 30 Perodicticus potto (6) 1200* 37 76 79 Didelphis marsupialis 1500* 47 61 56 Nycticebus coucang (2) 610* 34 73 73 Didelphis virginiana (2) 2200 57 69 67 Daubentoniidae Isoodon obesulus 600* 31 34 28 Daubentonia madagasc. (2) 2500* 45 89 89 Marmosa robinsoni (2) 86 17 22 21 Callitrichidae Monodelphis domestica 77 18 22 22 Callimico goeldii (2) 500* 30 55 50 Philander opossum 800* 34 44 44 Callithrix argentata (3) 320 25 52 45 Caluromys philander 300* 20 24 27 Callithrix geoffroyi 250* 23 48 43 Spilocuscus maculatus (2) 5500 54 95 95 Callithrix jacchus (4) 481 27 49 43 Trichosurus vulpecula (3) 3500* 54 76 83 Cebuella pygmaea (2) 130* 18 34 31 Carnivora Leontopithecus rosalia (2) 550* 28 61 61 Nasua nasua 6000* 67 93 74 Saguinus fuscicollis 200 18 45 36 Potos flavus (3) 2000* 43 82 67 Saguinus imperator (2) 500 25 53 44 Procyon lotor 6800 64 97 100 Saguinus labiatus 667 28 57 50 Felis nigripes (2) 2500* 58 88 81 Saguinus midas (2) 586 26 53 47 Felis geoffroyi 2500* 59 84 71 Saguinus oedipus (5) 339 28 54 48 Felis planiceps 2500* 58 82 73 Cebidae Felis sylvestris (2) 3300 69 102 100 Aotus nigriceps (2) 825 29 68 65 Mustela putorius (4) 1200 34 50 34 Aotus trivirgatus 800* 35 76 68 Martes martes (2) 1849 41 74 56 Cacajao calvus (2) 3450 57 136 120 Genetta genetta (2) 1450 45 67 57 Cacajao melanocephalus (3) 3000* 51 133 120 Genetta tigrina 1550 53 76 64 Callicebus moloch (3) 800* 33 77 65 Paradoxurus hermaphrod. 3500* 57 86 63 Cebus albifrons 1615 41 104 97 Viverricula indica 2500* 49 63 56 Cebus apella (4) 3250 58 110 107 Rodentia Cebus capucinus 1300* 46 100 94 Atlantoxerus getulus 350 24 32 27 Chiropotes satanas 2000* 46 111 92 Callosciurus prevosti (2) 250 27 41 36 Pithecia irrorata (4) 2500* 46 119 103 Callosciurus notatus 220 25 35 30 Pithecia monachus 1500* 28 78 67 Cynomys ludovicianus 900* 26 38 31 Pithecia pithecia 1000* 42 102 97 Ratufa indica 1500* 39 65 51 Saimiri sciureus (3) 800* 32 70 65 Sciurus carolinensis 550 29 42 41 Primates Sciurus vulgaris (3) 400* 27 42 39 Cercopithecidae Spermophilus citellus 200* 21 27 23 Cercopithecus cephus 2900* 41 97 100 Spermophilus lateralis (2) 250 24 30 26 Cercopithecus diana (2) 5000* 62 137 134 Tamias sibiricus 108 17 23 21 Cercopithecus hamlyni 3680* 55 116 125 Glis glis (2) 123 15 22 21 Cercopithecus mona 2750 44 107 104 Muscardinus avellanarius 15 8 11 13 Chlorocebus aethiops (4) 5500 67 145 159 Acomys minous 70 16 17 15 Erythrocebus patas (3) 4900 89 149 157 Mus musculus 50 12 12 11 Lophocebus albigena (2) 7000* 70 161 161 Rattus norvegicus (3) 350 25 28 27 Macaca fascicularis 2500 41 79 99 Apodemus flavicollis 34 12 15 14 Macaca mulatta (3) 9000* 74 155 144 Lemmus lemmus 60 14 17 17 *The asterisk denotes that body weight is compiled from one of the following sources: Grzimek, 1987; Rowe, 1996; Garbutt, 1999; Nowak, 1999.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Forelimb kinematics and proportions in primates 3779 between different sized adults of a species is determined by Comparison took place on the lowest taxonomic level of families, ontogenetic development (Wayne, 1986; Lammers and German, among primates at least. The lower sample size of tree-shrews, 2002; Schilling and Petrovitch, 2005), interspecific allometry marsupials, rodents and carnivores made a further subdivision into reflects size-related mechanical adaptations. Accordingly, the limb families less appropriate. Because sample sizes are unequal across proportions of different sized conspecifics do not scale isometrically the taxa, the GT2 method was employed (Hochberg, 1974; Sokal and can be very different. The taxa included and the sample and Rohlf, 1995) to compare group means and to calculate lower representing each taxon can be seen in Table2, along with the and upper comparison limits for each sample mean. Means are corresponding body mass values and the measured lengths of significantly different if their comparison intervals do not overlap scapula, humerus and radius. Those specimens labelled with an (Hochberg, 1974; Sokal and Rohlf, 1995). The comparison interval asterisk denote specimens for which body masses were compiled is different from the confidence interval because its computation from the literature. The available head–trunk length in those uses the critical values of the studentized maximum modulus specimens was used to decide whether the mean or the maximum distribution for the comparison of multiple means instead of the body mass values were more appropriate in estimating the unknown Student’s t-distribution used to calculate confidence intervals. mass (Grzimek, 1987; Rowe, 1996; Garbutt, 1999; Nowak, 1999). It was investigated whether the allometric scaling of the relative All other body mass values relate to the skeletal specimens. segment lengths is a significant source of their variation. Relative The majority of taxa included in the primate sample consist of segment lengths and body mass values were log-transformed (ln) arboreal quadrupedal primates. The members of the Cheirogaleidae, to produce log shape variables. Bivariate regressions were derived Lemuridae, Callitrichidae and Cebidae prefer to walk and run using the reduced major axis (RMA) line-fitting technique. The quadrupedally along narrow branches but also use other modes of coefficient of determination r2 was calculated in order to estimate progression such as climbing and leaping. However, none of these the portion of variation in relative segment length that can be taxa exhibits distinct specializations for leaping (e.g. extremely explained by the variation of body mass (Sokal and Rohlf, 1995). elongated hind limbs) (Rowe, 1996; Fleagle, 1999). Included Galagonidae are mostly such species that prefer to walk and run RESULTS quadrupedally but do not show the morphological specializations The first part of this section describes forelimb kinematics in four of vertical clingers and leapers with the exception of the Northern small arboreal quadruped primates (the grey mouse lemur, the brown lesser bush baby. Loridae walk and climb with large limb excursions lemur, the cotton-top tamarin and the squirrel monkey) with regard but none of these primates has been observed to leap (Walker, 1979; to the kinematic principles displayed by other small mammals: the Demes et al., 1990; Schmitt and Lemelin, 2004). Quadruped predominance of scapula excursion in limb protraction and climbing is – along with walking and leaping – a preferred mode retraction, the parallel motion of scapula and forearm and the of locomotion in Colobinae (Napier, 1963; Morbeck, 1979; Isler function of the intrinsic limb joints in providing limb compliance. and Grüter, 2005). Cercopithecine Old World monkeys (baboons, The body mass of the animals ranges from 100 to 3000g, thus macaques, patas monkeys, guenons) are primarily adapted to semi- allowing some conclusions to be drawn regarding the influence of terrestrial and terrestrial quadrupedalism (Napier, 1967; Rollinson size on forelimb kinematics. Walking speed varies considerably in and Martin, 1981; McCrossin et al., 1998). Still, most guenons and all four species (grey mouse lemur, 0.39–0.89ms–1; brown lemur, some macaques have returned to arboreality. Re-adaptations to 0.56–1.45 m s–1; cotton-top tamarin, 0.40–0.87 m s–1; squirrel arboreality in guenons have been observed to affect the morphology monkey, 0.39–1.00ms–1) but its influence of limb kinematics is of the autopodia more than that of proximal limb elements lower than one might expect. Like various other small non-cursorial (Meldrum, 1991; Schmitt and Larson, 1995). The marsupial, rodent mammals (Fischer et al., 2002; Schilling and Fischer, 1999), the and carnivore samples mostly include small arboreal and terrestrial primates modify their walking speed mainly by changing temporal species. The majority of these mammals tend to move in a roughly gait parameters. Contact phase duration decreases with increasing similar fashion characterized by a crouched limb posture (Jenkins, speed and thereby step frequency increases. Spatial gait parameters 1971; Fischer et al., 2002). Cursorial specializations were attributed like step length and body progression during the contact phase were to the larger carnivores (racoon, cats and viverrids) (Jenkins and not or only to a minor degree modified to increase velocity. Only Camazine, 1977; Nowak, 1999). the cotton-top tamarin increases its walking speed by increasing both In order to evaluate the proportions of a three-segmented limb step frequency and step length. Fig.2 shows the variation of step structure, intralimb proportions in this study are expressed as the duration and step length over the range of dimensionless speed. The percentage each segment length represents of the sum of the lengths majority of steps of the grey mouse lemur, the brown lemur and of the segments. The hand is omitted due to its negligible quantitative the tamarin overlap with respect to Froude numbers but the squirrel contribution to forelimb protraction and retraction in palmigrade monkeys moved somewhat slower. At Froude numbers equal to mammals (Fischer et al., 2002; Schmidt, 2005b). Only a few species those of the other primates, squirrel monkeys preferred to run. in the sample use their hands in a digitigrade posture (some Although kinematic parameters vary considerably in all species, on terrestrial cercopithecines and some carnivores) but for comparative average less than 20% of this variation results from variation in reasons their hand proportions were not considered in this study. speed. Speed-dependence is, therefore, considered in the description Interlimb ratio is calculated for the three-segmented limbs using only for those kinematic parameters that consistently and to a higher the following formula: scapula+humerus+radius/femur+tibia+ percentage change with increasing walking velocity. r2 values are tarsometatarsus in percent. The morphometric data of the hindlimb given to characterize the strength of the relationship between for this sample were taken from a previous publication (Schmidt, walking speed and the respective parameter. 2005a). Original data on hindlimb length for the new specimens in The second part of this section focuses on intra- and interlimb the sample (Loridae, Galagonidae, Daubentoniidae and Colobinae) proportions in primates and other mammals. In the primate-specific can be provided on request. diagonal footfall sequence, the relationship between limb length and A one-way fixed-factor analysis of variance (ANOVA) was used body size and the ratio between fore- and hindlimb length can act to determine the degree of variance of forelimb proportions. as constraints on limb kinematics. Therefore, the scaling pattern of

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3780 M. Schmidt

1.40 A hindlimbs the same functional length. Lemurs, however, seem to have unequal functional limb lengths, judging by the strong 1.20 downward incline of their trunks when they walk, meaning that 1.00 their proximal scapular border is lower than their hip joint. The scapula excursions of the brown lemur are very large and the two 0.80 spines hardly overlap at touchdown or lift-off indicating that the 0.60 point of zero velocity is situated outside the body (Fig.3). The measured angle of total forelimb excursion in the brown lemur 0.40 Step duration (s) Step duration (86±3deg.), therefore, is not only significantly larger than that of 0.20 the other primates but is also larger than its hindlimb excursion angle (74deg.) (Schmidt, 2005a). With the exception of the brown 0 lemur, total forelimb excursion is fairly similar among the primates 0 0.02 0.04 0.06 0.08 0.10 0.12 0.14 0.16 0.18 (Table3). Angular excursion hardly changes with increasing speed. Froude number Variations in step length are often accompanied by variations of 2 2 Microcebus murinus r =0.674 Saimiri sciureus r =0.860 limb stiffness and functional limb length. Therefore, angular 2 2 Saguinus oedipus r =0.603 Eulemur fulvus r =0.685 excursion does not necessarily increase with increasing step length. By drawing a vertical line through the point of ground contact, 0.50 B the total angular excursion of the forelimb can be split into a 0.45 retraction angle and a protraction angle. The protraction angle of 0.40 the forelimb is always larger than the retraction angle. The retraction 0.35 angle is fairly constant in the grey mouse lemur, the cotton-top 0.30 tamarin and the squirrel monkey but larger in the brown lemur 0.25 (Table3). Accordingly, protraction is more variable. The forelimb 0.20 of the brown lemur is the most protracted; the forelimb of the squirrel monkey is the least protracted. Obviously, body size has no

Step length (m) 0.15 significant effect on angular excursion in the three smaller primates 0.10 but the brown lemur exhibits a higher degree of forelimb protraction. 0.05 0 0 0.02 0.04 0.06 0.08 0.10 0.12 0.14 0.16 0.18 Kinematics of limb segments As previously shown for the hindlimbs in these species (Schmidt, Froude number 2005a), highly uniform limb excursion can be the result of quite Microcebus murinus r2=0.175 Saimiri sciureus r2=0.216 different segment and joint kinematics. This is also the case for the Saguinus oedipus r2=0.481 Eulemur fulvus r2=0.180 forelimb. Fig.4 shows the typical excursion of scapula, humerus, Fig. 2. Influence of walking velocity on step duration (A) and step length radius and hand during the support phase of a step cycle. Table4 (B). Walking velocity is transformed to the dimensionless Froude number. lists mean values, standard deviations and the overall range of the touchdown and lift-off angles, as well as the amplitude of excursion during the stance phase. forelimb length, the length ratio between fore- and hindlimbs and The movement of the scapula is the most similar factor among the intralimb proportions of the forelimb are examined. In this the species (Fig.4). Mean angles at touchdown and lift-off and the morphometric section of the paper, a broader sample of quadrupeds mean amplitude of scapula retraction hardly differ among the species is considered in an attempt to test whether primates in general differ (Table4). Scapula retraction starts at an angle of approximately from other mammals. 45deg., continues more or less regularly throughout the support phase and ends at an angle of approximately 90deg. No yield has Forelimb kinematics in grey mouse lemurs, brown lemurs, been observed in the scapulo–thoracic ‘joint’, and in this respect cotton-top tamarins and squirrel monkeys the most proximal forelimb joint is comparable with the hip joint Angular excursion of the forelimb of the hindlimb. The proximal pivot of the forelimb is the instantaneous centre of Humeral excursion differs much more among the species and scapular rotation, held and guided by muscles. This point is on the in such a way that body size seems to influence the degree of same height level as the ipsilateral hip joint providing fore- and humeral protraction. The brown lemur exhibits the greatest

Fig. 3. Scapula position of the brown lemur at touchdown (A) and lift-off (B).

THE JOURNAL OF EXPERIMENTAL BIOLOGY Forelimb kinematics and proportions in primates 3781 humeral protraction and the largest Table 3. Protraction angle, retraction angle and total excursion of the forelimb amplitude of humeral excursion. The Protraction angle (deg.) Retraction angle (deg.) Total excursion (deg.) lowest mean touchdown angle was measured in the grey mouse lemur at less N Means±s.d. Range Means±s.d. Range Means±s.d. Range than 90 deg. Cotton-top tamarins and Microcebus murinus 25 42±3 35–47 32±4 26–39 74±5 66–87 squirrel monkeys protract their humeri to Eulemur fulvus 20 47±2 44–50 39±2 35–43 86±3 81–90 a similarly larger degree. The average Saguinus oedipus 20 43±3 40–47 33±5 28–42 76±5 66–85 touchdown angle is approximately Saimiri sciureus 22 38±4 28–44 32±3 26–38 70±5 57–79 100 deg. but increases with increasing walking velocity in both species (Saguinus, r2=0.245; Saimiri, stance phase when the humerus reaches a more or less horizontal r2=0.516). It should be noted, however, that despite the lower position. This positioning is influenced by walking speed in the degree of humeral protraction, the forelimb in the mouse lemur brown lemur (r2=0.241). At higher speeds, the distal end of the exhibits the same degree of protraction as in the cotton-top tamarin humerus is raised upon the level of the shoulder. It might be and the squirrel monkey. In all four species, the angular velocity affected by the overall slower walking speed that the humerus of of humeral protraction is higher in the first half of the support the squirrel monkey is markedly less retracted and seldom, if ever, phase and slows down to near zero during the last 10% of the reaches a horizontal position.

100 Fig. 4. Angular excursion of forelimb segments and Shoulder blade 90 forelimb joints during the support phase of the limb. 80 Microcebus murinus 70 Eulemur fulvus 60

50 Saguinus oedipus 40 30 Saimiri sciureus 20

120 Upper arm 180 Shoulder joint 100 160 80 140 60 120 40 100 20 80 0 60 –20 40

120 Forearm 180 Elbow joint Angle (deg.) 100 160 140 80 120 60 100 40 80 20 60 0 40

100 Hand 270 Wrist joint 90 250 80 70 230 60 210 50 40 190 30 170 20 10 150 0 130 0 20 40 60 80 100 0 20 40 60 80 100 Stance duration (%)

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3782 M. Schmidt

Table 4. Forelimb segments: angles at touchdown and lift-off, and the amplitude of excursion Touchdown angle (deg.) Lift-off angle (deg.) Amplitude (deg.) Means±s.d. (N) Range Means±s.d. (N) Range Means±s.d. (N) Range Shoulder blade Microcebus murinus 41±7 (76) 27–59 87±6 (92) 73–104 48±6 (76) 36–64 Eulemur fulvus 46±6 (60) 31–57 86±9 (60) 70–100 51±9 (60) 30–69 Saguinus oedipus 42±3 (46) 37–50 90±5 (52) 73–104 49±6 (25) 37–61 Saimiri sciureus 43±5 (60) 37–52 84±6 (60) 80–90 56±8 (60) 47–63 Upper arm Microcebus murinus 78±9 (76) 52–103 –5±8 (92) –26–9 87±8 (76) 64–105 Eulemur fulvus 125±9 (60) 88–145 6±9 (60) –21–33 123±9 (60) 85–148 Saguinus oedipus 102±8 (47) 74–119 4±5 (57) –4–19 95±8 (31) 72–108 Saimiri sciureus 100±7 (73) 85–114 21±6 (73) 6–37 81±9 (73) 67–100 Forearm Microcebus murinus 11±9 (72) 4–39 112±6 (84) 95–128 102±8 (72) 82–121 Eulemur fulvus 24±4 (35) 15–31 121±9 (35) 103–131 109±9 (35) 75–123 Saguinus oedipus 21±5 (46) 9–33 102±9 (50) 85–125 80±9 (36) 55–105 Saimiri sciureus 36±3 (65) 28–41 110±4 (65) 101–120 75±5 (65) 65–88 Hand Microcebus murinus 10±8 (59) 2–16 80±9 (54) 56–105 69±9 (38) 61–104 Eulemur fulvus 16±7 (30) 3–22 74±9 (30) 60–95 65±9 (30) 51–87 Saguinus oedipus 16±5 (26) 3–24 76±9 (33) 54–104 67±9 (24) 46–90 Saimiri sciureus 13±7 (45) 3–22 78±9 (45) 67–97 60±9 (45) 46–77

Throughout most of the support phase, the forearm moves forelimb of the grey mouse lemur is the most flexed throughout the exactly in parallel to the scapula (Fig.4). This matched-motion support phase. At touchdown, it forms 82% of the anatomical limb pattern of the first and the third segment is said to be typical of a length and at lift-off, 74%. In the most flexed posture, functional three-segmented leg and can also be seen in the hindlimb between forelimb length is 62% of the anatomical length. The most extended thigh and foot (Fischer and Witte, 1998; Fischer et al., 2002). The forelimbs are exhibited by the squirrel monkey (ratio: touchdown matched-motion pattern is only broken at the beginning and end of 96%, lift-off 91%). Although the ratio between functional and the support phase, when forearm excursions exceed scapula anatomical limb length is very similar to that in the brown lemur excursions. The variability of forearm excursion among the four (touchdown 95%, lift-off 94%), limb flexion at mid-stance is less species does not appear to be related to size. In the cotton-top pronounced in the squirrel monkey (77%) than in the brown lemur tamarin, the degree of forearm retraction is influenced by speed (73%). Generally, the forelimb is most extended at the beginning (r2=0.274) in such a way that step length increases by an increasing of the step cycle. The grey mouse lemur and the brown lemur lift-off angle of the forearm. significantly decrease limb compliance with increasing speed. In While the upper arm and forearm undergo large angular the grey mouse lemur, the amount of shoulder flexion (r2=0.338) excursions and the scapula dominates limb retraction due to its high and elbow flexion (r2=0.327) during the contact phase decreases. pivot, the hand plays a minor role in forelimb excursion. All four Limb compliance in the brown lemur is reduced due to a decrease species place their hands in a palmigrade posture. The touchdown of elbow flexion (r2=0.429). angle deviates from zero only because of the thickness of the palmar Fig.4 depicts the joint excursions for the shoulder, elbow and patches. Carpus and metacarpus are lifted from the support during wrist joint of the four species during the support phase of a step the second half of the stance phase. The angles at lift-off vary widely cycle. Maximum shoulder joint extension occurs at the beginning in each species but their mean values are similar (Table4). of the cycle. The shoulder joint is almost fully extended in the brown lemur but only moderately extended in the grey mouse lemur. A Kinematics of forelimb joints significant yield followed by a re-extension phase was observed Almost all quadrupedal mammals flex their limbs to a certain degree only in the squirrel monkey. In the other three species, shoulder during the support phase. This means that the anatomical limb length, flexion lasts until mid-stance, from whence on the shoulder joint i.e. the sum of the lengths of limb segments, does not correspond seems to be frozen at a constant angle and the humerus is further to the functional limb length, i.e. the distance between the point of displaced only by scapular retraction. ground contact and the proximal pivot of a limb. The ratio between The flexion and re-extension pattern of the elbow joint reveals functional limb length and anatomical limb length expresses the the prominent role it plays in yielding (Fig.4; Table5). With the degree of overall limb flexion and normally varies throughout the exception of in the grey mouse lemur, the elbow joint is at its most support phase. Functional limb length is at its minimum when the extended at touchdown. Maximum flexion occurs at mid-stance. hand passes under the scapula pivot. Several authors term this While the hand is resting on the support, the wrist joint extends posture ‘mid-stance’ or ‘mid-support’ regardless of its timing continuously (dorsiflexion) as a result of the retraction of the forearm relative to stance duration because it marks the transition from the during the first half of the stance phase. Maximum extension occurs braking phase to the propulsive phase in limb retraction. Table5 when the hand passes under the elbow joint. Then, the hand is gives the mean angles at mid-stance of the limb joint illustrating subsequently lifted from the ground by the flexion of the wrist. This how each joint contributes to overall limb flexion and, thus, to the motion can be fairly rapid, as observed in the grey mouse lemur compliance of the limb. Of the four primates in this study, the and the squirrel monkey.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Forelimb kinematics and proportions in primates 3783

Table 5. Forelimb joints: angles at touchdown and lift-off, the amplitude of excursion and angle at mid-stance Touchdown angle (deg.) Lift-off angle (deg.) Amplitude (deg.) Mid-stance (deg.) Means±s.d. (N) Means±s.d. (N) Means±s.d. (N) Means±s.d. (N) Range Range Range Range Shoulder joint Microcebus murinus 120±9 (76) 82±6 (92) 49±8 (75) 80±8 (75) 93–141 64–98 26–75 60–97 Eulemur fulvus 165±9 (60) 89±9 (60) 84±9 (60) 82±9 (60) 132–179 64–115 52–103 54–96 Saguinus oedipus 144±8 (44) 94±7 (51) 51±8 (27) 98±7 (25) 119–162 72–109 28–64 84–107 Saimiri sciureus 140±7 (73) 106±6 (92) 39±9 (73) 105±9 (73) 127–156 93–115 29–55 87–118 Elbow joint Microcebus murinus 85±9 (74) 101±9 (89) 40±8 (74) 63±6 (74) 61–105 76–117 24–61 41–74 Eulemur fulvus 153±9 (35) 126±9 (35) 60±7 (35) 76±9 (35) 137–169 98–144 51–83 50–97 Saguinus oedipus 122±8 (42) 106±9 (46) 36±6 (35) 86±7 (25) 103–140 89–128 18–58 73–100 Saimiri sciureus 135±4 (65) 132±3 (65) 30±6 (65) 104±7 (65) 122–142 126–137 21–43 78–113 Wrist joint Microcebus murinus 187±7 (63) 215±9 (89) 76±9 (63) 225±9 (74) 172–201 168–248 46–109 201–249 Eulemur fulvus 195±6 (30) 223±9 (30) 61±8 (30) 228±8 (30) 186–203 208–239 36–80 221–238 Saguinus oedipus 186±4 (26) 202±9 (33) 43±9 (25) 211±9 (25) 181–196 181–225 19–66 200–229 Saimiri sciureus 194±3 (45) 212±6 (45) 50±9 (45) 219±9 (40) 188–199 199–225 28–75 198–233

Forelimb length and limb proportions in quadrupedal subdivision of the primate sample into the eight families would be primates and other mammals less illustrative, primates were subdivided into Strepsirhini, The evaluation of limb proportions focuses on the basic difference Platyrrhini and Catarrhini for graphical reasons. Allometry between primates and other mammals of small body size. Greater coefficients are shown in Table6 along with the corresponding effort was, therefore, made to obtain large samples of small-sized confidence intervals at the various taxonomic levels, which indicate taxa, in order to permit comparison between those animals thought that the scaling pattern strongly depends on the degrees of to be closest to the presumed ancestral morphometric pattern of each relationship between the taxa considered. Slopes were considered phylogenetic lineage. to deviate significantly from isometry if the 95% confidence interval Biewener emphasizes that scaling analyses in a large and did not include the isometric expectation (0.33). The F-value phylogenetically diverse sample are often marred by the fact that indicates that body mass influences forelimb length significantly in body size-related effects cannot accurately be distinguished from all groups but the Galagonidae and Colobinae. phylogenetic signals and other functional determinants of skeletal Forelimb length tends to scale with positive allometry in most form (evolutionary ancestry, life style, locomotor behaviour) primate families, tree-shrews, rodents and carnivores but only in (Biewener, 2005). Therefore, morphometry in this study focuses on comparison at the family level within primates. Differences in 6.5 forelimb length and proportion can be expected to reflect size-related effects much more accurately on this lower taxonomic level due to 6.0 the greater similarity of locomotor behaviours. The cercopithecid Old World monkeys were divided into the two subfamilies 5.5 Cercopithecinae and Colobinae because the colobus monkeys and 5.0 leaf monkeys generally use more quadrupedal climbing, suspensory behaviour and leaping in progression than the macaques, baboons 4.5 and guenons. The lower sample size of tree-shrews, marsupials, ln Forelimb 4.0 Primates: Scandentia rodents and carnivores made a further subdivision into families less Strepsirhini Marsupialia appropriate. 3.5 Platyrrhini Rodentia Catarrhini Carnivora 3.0 Scaling of forelimb length to body mass 345678910 Fig.5 shows the scaling pattern of forelimb length to body mass for ln Body mass the entire sample of quadrupedal mammals included in this study. Body mass ranges between 15 g (dormouse Muscardinus Fig. 5. Scaling of forelimb length to body mass on logarithmic coordinates avellanarius) and 23.5kg (baboon Papio hamadryas). Because in primates and other groups of quadruped mammals.

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3784 M. Schmidt

Table 6. Scaling of forelimb length to body mass primates investigated in the kinematic F-value* r2 y-intercept±95% C.I. RMA-slope±95% C.I. N study exhibit the following interlimb ratios: grey mouse lemur 75, brown lemur 73, Marsupialia 167.641*** 0.949 2.49±0.39 0.35±0.06 11 cotton-top tamarin 70 and squirrel monkey Rodentia 131.883*** 0.886 2.34±0.36 0.37±0.05 17 77. Carnivora 19.292** 0.617 1.94±1.40 0.43±0.17 13 Scandentia 22.122* 0.917 2.54±1.59 0.35±0.31 4 Primates 994.920*** 0.943 2.49±0.17 0.39±0.02 69 Intralimb proportions of the forelimb Cheirogaleidae 57.863* 0.967 2.07±1.17 0.46±0.25 4 Fig.7 shows the mean values of the relative Lemuridae 304.157*** 0.978 2.56±0.37 0.37±0.05 9 segment lengths and their associated Loridae 22.939* 0.920 4.13±0.85 0.16±0.14 4 comparison intervals at the taxonomic level Galagonidae 14.686 0.880 2.17±2.78 0.43±0.45 4 of families (primates) or higher Callitrichidae 33.289*** 0.787 2.61±0.63 0.32±0.11 11 Cebidae 35.400*** 0.763 2.40±0.97 0.41±0.13 13 phylogenetic levels in the other mammals. Cercopithecinae 165.146*** 0.927 2.77±0.50 0.36±0.06 15 Primates differ significantly from other Colobinae 0.646 0.097 0.02±5.60 0.66±0.56 8 mammals in the relative lengths of their *Significance level of F: *** P<0.001; ** P<0.01; * P<0.05. C.I., confidence interval; RMA, reduced major scapula and radius, with Cheirogaleidae axis. being intermediate. Scapula proportion in primates has reduced to approximately 20% of forelimb length whereas radius primates does the confidence interval of the allometry coefficient proportion has increased to approximately 38–40%. The relative fail to overlap with the isometric expectation of 0.33. However, this length of the middle segment, however, is fairly constant. In most is not the case for primate families. The y-intercept and its 95% cases, the comparison intervals of the humerus mutually overlap confidence interval indicate that primates as a group do not have among the groups. Changes in forelimb proportion are, thus, mainly significantly longer forelimbs than the other mammals. Adaptive brought about by alterations in the relative lengths of the outer differences among primates are reflected by the huge variation in segments. y-intercepts but the confidence intervals do widely overlap (Table6). The intermediate position of the Cheirogaleidae results from size- Among the smallest species of all groups, where body mass is below related differences between the grey mouse lemurs and the dwarf 150g, forelimb lengths are equal (Fig.5). A clear distinction between primates and other mammals appears if body mass exceeds 200g. The forelimbs of primates, then, are relatively longer than those of other mammals, regardless of the locomotor habitat or phylogenetic position of the latter.

Interlimb proportions MarsupialiaCarnivoraRodentiaScandentiaCheirogaleidaeLemuridaeLoridaeGalagonidaeDaubentoniidaeCallitrichidaeCebidaeCercopithecinaeColobinae Almost all species considered here have shorter forelimbs than 35 hindlimbs (Fig.6). Interlimb ratio is calculated for the three- 30 segmented limbs using the following formula: scapula+ 25 humerus+radius/femur+tibia+tarsometatarsus in percent. The majority of specimens up to a body size of about 5kg have interlimb 20 ratios below 90, except in the case of marsupials. No distinction 15 can be made between rodents, carnivores, primates and tree-shrews. % Scapula Scaling effects emerge if body mass exceeds 2.5kg but they are 10 significant only for the Cebidae and Cercopithecinae, in which the interlimb ratio increases with increasing body size. The four 50 45 40 Primates: Strepsirhini Platyrrhini Catarrhini 110 Scandentia ϫ Marsupialia Rodentia + Carnivora 35 100 30 % Humerus 90 25 80 70 50 60 45 50 40

Forelimb / hindlimb ratio Forelimb 40 35 30 30 % Radius 345678910 25 ln Body mass Fig. 7. Intralimb proportions of the forelimb: Analysis of variance. Mean Fig. 6. Forelimb / hindlimb ratio over body mass (ln-transformed) in values of the relative segment lengths and their comparison intervals are primates and other groups of quadruped mammals. compared across the sample. Primates are subdivided into families.

THE JOURNAL OF EXPERIMENTAL BIOLOGY Forelimb kinematics and proportions in primates 3785 lemur. The genus Microcebus differs from Cheirogaleus and all arboreal quadruped primates but don’t revert to the forelimb other primates in having forelimb proportions of nearly 1:1:1, fairly proportions of the primarily small grey mouse lemurs. similar to other small mammals. The forelimb proportions of A scaling analysis of the relative segment lengths was carried Cheirogaleus tend to approximate proportions of 1:2:2, the pattern out to test the influence of body mass variation on forelimb found in most other primates. proportions. The overall scaling pattern of the relative segment Although group-specific differences occur to some degree in lengths is shown in Fig.8. Body mass values are log-transformed primates, the general pattern is less dependent on body size, phylogeny (ln) but to make it easier to distinguish between the groups the and locomotor habitat than one might expect. The significant relative segment lengths were not log-transformed here. Regression exceptions of Loridae and Colobinae may be related to the two groups’ was, of course, computed from bivariate log-transformed data. It preference for quadruped climbing. A relatively short scapula probably turns out that body mass has almost no influence on forelimb facilitates forelimb excursions outside the parasagittal plane (e.g. proportions in most of the groups, as is indicated by the F-values reaching above the head). The secondarily dwarfed Callitrichidae have and the coefficients of determination (Table7). Proportions are size- relatively longer shoulder blades and shorter forearms than other independent in Marsupialia, Carnivora, Scandentia and most primate families except Cheirogaleidae and Lemuridae. Body mass affects the relative length of the humerus in Rodentia, Cheirogaleidae and 35 A Lemuridae, in which humerus proportion increases with increasing size. Size seems to influence radius proportions in primates as a 30 whole but this effect is not visible at the family level, indicating again that the taxonomic level chosen for analysis affects the 25 interpretation of the results. 20 DISCUSSION b C.I.

% Scapula 15 Primates 0.09 0.02 Like many other mammalian lineages, primates descended from Scandentia 0.04 0.12 ancestors whose body size was small (Jenkins, 1974; Gebo, 2004; 10 Marsupialia 0.07 0.05 Soligo and Martin, 2006). Several authors have, therefore, emphasised Rodentia 0.08 0.04 Carnivores 0.16 0.10 the importance of studying the behaviour and ecology of small arboreal 5 mammals in reconstructing the early evolution of primates and understanding the functional significance of special morphological 50 B adaptations (LeGros Clark, 1959; Cartmill, 1972; Martin, 1972; Cartmill, 1974; Jenkins, 1974; Rasmussen, 1990; Gebo, 2004; Sargis 45 et al., 2007). Various locomotor studies have shown that small 40 mammals display a high level of similarity in their locomotor kinematics and limb proportions independent of phylogeny and 35 locomotor habitat (Jenkins, 1971; Fischer et al., 2002). These common

b C.I. kinematic principles (crouched limb posture, operational division

% Humerus 30 Primates 0.04 0.01 between propulsive proximal elements and limb joints that serve for Scandentia 0.04 0.11 compliance) have been proposed to be adaptive to postural stability 25 Marsupialia 0.03 0.02 Rodentia 0.05 0.02 in unanticipated situations within a disordered spatial arrangement of Carnivores 0.11 0.06 surfaces (Fischer, 1994). This section of the paper will, thus, 20 investigate why primate forelimb geometry differs in some regards from that of other small mammals by combining the present results 50 C on forelimb geometry with the author’s previous study of hindlimb geometry (Schmidt, 2005a). Links will be made to other distinctive 45 characters of primate locomotion such as the preference for a specific 40 footfall sequence, the particular weight distribution pattern between fore- and hindlimbs, and subsequent adaptations to other locomotor 35 modes. It will be discussed how this set of factors generated a frame b C.I. of constraints within which limb geometry evolved. A hierarchical % Radius 30 Primates 0.04 0.01 structure of dependencies between the individual characters can, thus, Scandentia 0.06 0.18 be proposed which will assist in differentiating between true 25 Marsupialia 0.05 0.04 Rodentia 0.05 0.03 adaptations (to the small-branch locomotor habitat) and constrained Carnivores 0.15 0.08 character transformations. The latter are better regarded as 20 1357911evolutionary by-products [‘spandrels’ according to Gould and ln Body mass Lewontin (Gould and Lewontin, 1979)] as recently proposed by Raichlen and Shapiro (Raichlen and Shapiro, 2007). Primates: Strepsirhini Platyrrhini Catarrhini Scandentia ϫ Marsupialia Rodentia + Carnivora How are small primates different from other small mammals in terms of limb geometry? Fig. 8. Scaling of forelimb proportions to body mass. For graphical reasons, A condition of symmetrical tetrapod locomotion is that the proximal relative segment lengths were not ln-transformed to permit better differentiation between the groups. Reduced major axis (RMA) slopes and pivots of fore- and hindlimbs are on the same level (Kuznetsov, the confidence intervals (CI) given for each group were calculated on 1985; Fischer and Witte, 1998). This is also the case for the majority bivariate ln-transformed variables. of quadruped mammals. Exceptions occur, for example in

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3786 M. Schmidt

Table 7. Significance test of the scaling analysis of relative lengths of forelimb segments with between functional and anatomical limb log-transformed body mass (ln) of quadruped mammals length and, thus, the adaptability of limb Scapula Humerus Radius geometry to biomechanical demands through the adjustment of limb 2 2 2 NF-value* r F-value r F-value r segmentation and angulation. For primates Marsupialia 11 2.465 0.215 2.654 0.228 0.226 0.025 displaying a specific diagonal sequence Rodentia 17 2.306 0.133 27.583*** 0.648 1.944 0.115 gait, another crucial factor is the Carnivora 13 0.007 0.001 3.920 0.246 2.551 0.175 relationship between limb length and body Scandentia 4 0.016 0.008 0.115 0.055 0.074 0.036 size because long limbs increase the risk Primates 67 9.635** 0.126 0.491 0.007 10.926** 0.140 Cheirogaleidae 4 1.772 0.470 39.283* 0.952 0.462 0.188 of interference between ipsilateral fore- and Lemuridae 9 0.006 0.001 17.874*** 0.719 6.379* 0.477 hindlimbs. Most primates have Loridae 4 11.459 0.850 2.092 0.511 1.098 0.354 significantly longer limbs relative to their Galagonidae 4 1.525 0.433 0.411 0.170 0.376 0.158 body size than other mammals, except in Callitrichidae 11 0.226 0.025 0.677 0.070 0.150 0.016 the case of the very small species which Cebidae 13 0.036 0.003 0.019 0.002 0.249 0.022 weigh less than 200g. The anatomical Cercopithecinae 13 7.343* 0.361 2.987 0.187 2.105 0.139 Colobinae 8 0.704 0.105 0.017 0.003 1.799 0.231 length differences between fore- and hindlimbs, however, remain similar to *Significance level of F: *** P<0.001; ** P<0.01; * P<0.05. those in other mammals, with an interlimb ratio of between 70 and 85 being typical chimpanzees, giraffes and hyenas, in which adaptations to other for smaller mammals in general. Hindlimbs, then, are always more locomotor modes or to non-locomotor activities are predominant. flexed than forelimbs. Interestingly, hindlimb lengthening in primates In mammals, the level of the proximal limb pivots is not necessarily affects neither intralimb proportions nor limb kinematics in the four constant during the support phase but can raise and fall species studied here (Schmidt, 2005a). Hindlimb elongation is simply synchronously in a pair of fore- and hind limbs (Fig.9), thus achieved through the proportional lengthening of all three limb permitting vertical oscillations of the centre of body mass that are segments. Thus, limb lengthening has no effect on intralimb essential for whole-body mechanics (Cavagna et al., 1977; Biewener, proportions, limb excursion angle or limb kinematics. Fig.9 shows 2006; Biknevicius and Reilly, 2006). Fore- and hindlimbs, thus, have that the prosimian primates and the small callitrichid New World the same functional length regardless of differences in anatomical monkeys share a similar hindlimb posture with other mammals of length. This guarantees that the limbs move with the same step their body size. In Cebidae (e.g. Saimiri sciureus) and frequency and that the same step length is brought about by the same Cercopithecidae, hindlimb kinematics have changed in the direction angular excursion. As a result, it largely determines the relationship of a more erect limb posture. As a result of this very conservative

Fig. 9. Comparison of forelimb and hindlimb postures at touchdown and lift-off among primates and other quadrupeds with estimated protraction and retraction FLp: 42°, FLr: 32°, HLp: 39°, HLr: 37° FLp: 43°, FLr: 35°, HLp: 43°, HLr: 40° Other angles (FLp – forelimb protraction, FLr – forelimb Microcebus murinus Monodelphis domestica retraction, HLp – hindlimb protraction, HLr – hindlimb Primates mammals retraction). Body size ranges from 100 g (grey mouse lemur and shrew-like opossum) to 20 kg (dog). Stick figure drawing data were compiled from several publications (Jenkins and Camazine, 1977; Goslow et al., 1980; FLp: 38°, FLr: 35°, HLp: 35°, HLr: 37° FLp: 41°, FLr: 45°, HLp: 35°, HLr: 47° Meldrum, 1991; Kuhtz-Buschbeck et al., 1994; Whitehead Loris tardigradus Tupaia glis and Larson, 1994; Schilling and Fischer, 1999; Fischer et al., 2002; Lemelin et al., 2003; Schmitt and Lemelin, 2004).

FLp: 43°, FLr: 33°, HLp: 36°, HLr: 42° FLp: 43°, FLr: 39°, HLp: 47°, HLr: 37° Saguinus oedipus Increase in body size Caluromys philander

Scapula Thigh Upper arm Lower leg Forearm Foot

FLp: 38°, FLr: 32°, HLp: 37°, HLr: 36° FLp: 33°, FLr: 35°, HLp: 35°, HLr: 37° Saimiri sciureus Rattus norvegicus

FLp: 47°, FLr: 39°, HLp: 33°, HLr: 41° FLp: 27°, FLr: 31°, HLp: 29°, HLr: 28° Eulemur fulvus Felis catus

FLp: 35°, FLr: 30°, HLp: 38°, HLr: 27° FLp: 25°, FLr: 30°, HLp: 28°, HLr: 16° Chlorocebus aethiops Canis familiaris

THE JOURNAL OF EXPERIMENTAL BIOLOGY Forelimb kinematics and proportions in primates 3787 hindlimb geometry, the point of touchdown of the hind limb is shifted which are convergent with primates. Although Schmitt and Lemelin cranially – and, thus, into the excursion sphere of the forelimb. (Schmitt and Lemelin, 2002) argued that the touchdown position In the diagonal footfall sequence of primates, hindlimb touchdown of the forelimb of the woolly opossum Caluromys philander is is followed by the touchdown of the contralateral forelimb primate-like, the photographs in their study and in Lemelin et al. (Hildebrand, 1967; Tomita, 1967). Moreover, the ipsilateral forelimb (Lemelin et al., 2003) show that it is quite similar to the forelimb is still on the ground when the hindfoot is positioned. Primates can position of tree-shrews (Schilling and Fischer, 1999), with the hand avoid interference between the ipsilateral limbs by overstriding placed right below the eye and the touchdown angle of the humerus (Hildebrand, 1967; Larson and Stern, 1987; Demes et al., 1994; almost vertical. The majority of quadruped mammals place their Wallace and Demes, 2007). This is very typical for many species forefeet right below the eye, not for visual control but as a fixed when walking on the ground but it has been less frequently observed point to control the geometry of the touchdown position (Fischer during arboreal locomotion (Wallace and Demes, 2007). Obviously, et al., 2002). This strategy makes the angle of attack of the centre many primates avoid overstriding on arboreal substrates. Therefore, of body mass very constant. Some authors have explained this limb interference has to be avoided by means of another strategy. invariant angle as a mechanical parameter to control limb stability Arboreal primates avoid limb interference by a cranial shift of (Fischer and Blickhan, 2006; Hackert et al., 2006). the forelimb step (Fig.10). They display much greater asymmetry From this comparative perspective, the question of why primates between the angles of protraction and retraction. As the protraction have abandoned this strategy deserves attention and further angle increases, retraction decreases, with the forelimb thus discussion. Is the ‘new’ forelimb posture at touchdown really better sacrificing part of its caudal excursion sphere to avoid interference adapted to the specific demands of primate locomotion than the ‘old’ with the hindlimb. Total forelimb excursion, however, can thus one? One argument against this assumption is that the extended and remain equal to hind limb excursion (Fig.10). Larson (Larson, 1998) protracted forelimb of primates is more susceptible to gravitational has already proposed that forelimb protraction could be a strategy loading than the crouched posture of other mammals as the substrate to avoid limb interference – an assumption supported by the present reaction force vector is far removed from the limb joints (Biewener, survey of both limb kinematics and limb proportions. A significantly 1983; Schmitt, 1999; Larney and Larson, 2004; Schmidt, 2005b). higher degree of forelimb protraction has been observed in those Only the ability of many primates to reduce the weight borne by primates with very long hindlimbs (e.g. Lemuridae). Species with the forelimb may help to overcome this problem (Reynolds, 1985). short limbs (e.g. grey mouse lemurs) do not display greater forelimb Those primate species that do not reduce forelimb loading – Loridae protraction than other small mammals. This also applies to those (Ishida et al., 1990; Demes et al., 1994; Schmitt and Lemelin, 2004) arboreal marsupials that show certain locomotor characteristics, and Callitrichidae (Schmitt, 2003) – display significant changes in the contractile properties of their forelimb muscles (Schmidt and Leuchtweis, 2007; Schmidt and Schilling, 2007). Principles of limb geometry in mammals (Fischer et al., 2002): As some strategies of stabilizing the forelimb posture Forelimb and hindlimb display the same mechanically (e.g. through an invariant touch down angle) have pivot height + step length + angular excursion given way to a restrictive footfall sequence combined with limb elongation, it might well be that the observed changes in forelimb proportions reflect advanced mechanical strategies to deal with the problem of limb instability. As a result of the shift towards a (relatively speaking) shorter scapula and longer forearm, forelimb proportions go from being symmetrical to being asymmetrical. Based on numerical simulations, Seyfarth et al. suggested that the asymmetric structuring of a three-segmented limb enhances the self- stability of movement (Seyfarth et al., 2001). The hindlimb of mammals generally corroborates this hypothesis (Seyfarth et al., 2001; Schmidt and Fischer, 2008). Whether the basic change in Hindlimb elongation in larger primates has no forelimb proportions in primates really enhances limb stability, effect on limb geometry however, remains to be proven using mathematical simulations. but it shifts the touchdown position craniad Proposal of a hierarchical structure of dependencies in character evolution As the smallest living primates, grey mouse lemurs have often been Two substrate-dependent strategies to avoid limb interference suggested to be reliable models of the last common ancestor of primates (Martin, 1972; Gebo, 2004). In the present study, it has been shown that grey mouse lemurs display exactly the same limb Cranial shift of forelimb step geometries as other small mammals. Limbs are not elongated and ‘Overstriding’ (flat ground) (narrow support) move in a crouched posture during the entire step cycle. However, grey mouse lemurs differ from other small mammals in having powerful prehensile hindfeet. They walk in a diagonal-sequence gait and they are able to shift weight dynamically from the forelimbs to the hindlimbs (M.S., unpublished observations). As the set of these three characters evolved convergently in arboreal mammals three Fig. 10. Relationship between pivot height and excursion angle of fore- and times at least, namely in primates (Hildebrand, 1967; Martin, 1968; hindlimbs in small mammals, and the consequences of elongated hindlimbs Kimura et al., 1979; Reynolds, 1985), in some marsupials (Goldfinch in primates. and Molnar, 1978; Cartmill et al., 2002; Schmitt and Lemelin, 2002;

THE JOURNAL OF EXPERIMENTAL BIOLOGY 3788 M. Schmidt

Cartmill et al., 2008) and in some carnivores (Rollinson and Martin, as leaping in lemurs or acrobatic climbing in lorises. These 1981; Cartmill et al., 2007), it is plausible to assume that the constraints and their solutions were the driving force behind primate characters not only coincide but are mutually interdependent, as locomotor evolution. Once the transfer of moments by prehensile already suggested by several authors (Rollinson and Martin, 1981; feet was part of the standard locomotor repertoire, a gradual Cartmill et al., 2002; Schmitt and Lemelin, 2002; Lemelin et al., caudalization of the centre of body mass from its anterior position 2003). The reasons for these interdependencies have been discussed in quadrupeds to a more posterior location, for example in hominoids for many years but are not yet completely understood. (Stern, 1976; Reynolds, 1985; Raichlen et al., 2007), was possible Grasping feet have the unique capacity to produce moments about without any mechanical constraints. Once primates had learned to the substrate axes, which can, in turn, be transmitted to the body, stabilize the protracted and extended forelimb against disruptive thus allowing a dynamic weight shift from side to side (Cartmill, forces, they were able to use the forelimb to reach out and test the 1985; Preuschoft, 2002) or from the forequarter to the rear (Witte support, to increase gait compliance and, of course, in many other et al., 2002; Schmidt, 2005b). A consistent posterior weight shift locomotory and non-locomotory functions as suggested by Larson does not occur if forelimbs are equipped with the same capacity for (Larson, 1998). powerful grasping and weight shifts in any direction, as seems to be the case in Loridae (Ishida et al., 1990; Schmitt and Lemelin, 2004). This research was supported by the Deutsche Forschungsgemeinschaft (Innovationskolleg ʻBewegungssystemeʼ, INK 22/B1-1). I wish to thank Dieter The production of moments requires forces to be exerted from more Haarhaus (Institut für den Wissenschaftlichen Film, Göttingen) and his team for than one point of the plantar surface onto the substrate. Moments their patience and competence in cineradiography. Danja Voges kindly provided can also be produced on flat ground but the substrate reaction the X-ray films of the cotton-top tamarins. Thanks also to the German Primate Research Centre (Göttingen), Gettdorf Zoo and the Institute of Zoology at the moments will be lower under these conditions. Once powerful pedal Veterinary University Hannover for kindly providing our institute with animals. I am grasping had evolved in primates, it could be used to actively regulate also grateful to the curators of the Phylogenetisches Museum Jena, Museum für Naturkunde Berlin, Bayrische Staatssammlung München and Naturhistorisches the weight distribution between the limbs regardless of the position Museum Bern for access to skeletal material in their care. Iʼm grateful to Martin S. of the centre of body mass (Witte et al., 2002). Only under these Fischer, Hartmut Witte, and Nadja Schilling for insightful discussions during the circumstances was a change in the footfall sequence to hindlimb stages of this project. I thank the anonymous reviewers for providing many constructive comments and useful advice on the previous draft of the manuscript contact prior to forelimb contact meaningful because it could reduce and Lucy Cathrow for thoroughly editing the language of the manuscript. the impact of touchdown of the forelimb. 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