Uniqueness of primate forelimb posture during quadrupedal locomotion

Uniqueness of Primate Forelimb Posture DuringQuadrupedal Locomotion

SUSAN G. LARSON,1* DANIEL SCHMITT,2 PIERRE LEMELIN,2AND MARK HAMRICK3

1Department of Anatomical Sciences, State University of New York atStony Brook, Stony Brook, New York 11794-80812Department of Biological Anthropology and Anatomy, Duke UniversityMedical Center, Durham, North Carolina 277103Department of Anthropology, Kent State University, Kent, Ohio 44242

ABSTRACT Among the characteristics that are thought to set primatequadrupedal locomotion apart from that of nonprimate mammals are a moreprotracted limb posture and larger limb angular excursion. However, kine-matic aspects of primate or nonprimate quadrupedal locomotion have beendocumented in only a handful of species, and more widely for the hind thanthe forelimb. This study presents data on arm (humerus) and forelimb pos-ture during walking for 102 species of mammals, including 53 nonhumanprimates and 49 nonprimate mammals. The results demonstrate that pri-mates uniformly display a more protracted arm and forelimb at hand touch-down of a step than nearly all other mammals. Although primates tend to enda step with a less retracted humerus, their total humeral or forelimb angularexcursion exceeds that of other mammals. It is suggested that these featuresare components of functional adaptations to locomotion in an arboreal habi-tat, using clawless, grasping extremities. Am J Phys Anthropol 112:87–101,2000. © 2000 Wiley-Liss, Inc.

The form of quadrupedalism displayed byprimates differs from that of nonprimatemammals in a variety of ways (Vilensky,1987, 1989; Larson, 1998). Among these dif-ferences are large limb angular excursions(Alexander and Maloiy, 1984), broughtabout in part by a more protracted positionof the limb at touchdown (Reynolds, 1987).These generalizations regarding limb pos-ture and excursion, however, are basedmainly on observations for the hind limb,and for very limited samples of either pri-mates (Reynolds, 1987; Demes et al., 1990)or nonprimates (McMahon, 1975, 1984). Al-though a more protracted limb posture andlarger angular excursion have been as-sumed to also characterize the primate fore-limb (e.g., Schmitt et al., 1994), relativelylittle comparative data exist in support ofthis supposition (for review, see Larson,1998). To explore the generality of thisclaim, the present study was undertaken to

survey forelimb posture and excursion dur-ing quadrupedal walking across the primateorder, as well as for a variety of nonprimatemammals.

METHODS

Forelimb positional data were derivedfrom videotapes of captive animals taken atthe following zoos and research centers:Brookfield Zoo, Chicago, IL; Bronx Zoo, NewYork, NY; Cleveland Zoo, Cleveland, OH;Pittsburgh Zoo, Pittsburgh, PA; San DiegoZoo; San Diego, CA; Duke Primate Center,Durham, NC; Primate Locomotion Labora-tory, Stony Brook, NY; and Laboratoire

Grant sponsor: L.S.B. Leakey Foundation; Grant sponsor:NSF; Grant numbers: BCS 9806291, SBR-9320237, SBR-9318750.

*Correspondence to: Susan G. Larson, Department of Anatom-ical Sciences, State University of New York at Stony Brook,Stony Brook, NY 11794-8081.E-mail: [email protected]

Received 3 June 1999; accepted 13 January 2000.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 112:87–101 (2000)

© 2000 WILEY-LISS, INC.

d’Ecologie Generale, CNRS/Unite de Re-cherche 1183, Brunoy, France. Most of thevideotapes were recorded by one of the au-thors (S.G.L.) with a hand-held PanasonicAG 195 camcorder equipped with an elec-tronic shutter (1/500 sec) at 60 fields/sec.Additional video was recorded by P.L. usinga tripod-mounted Sony HandyCam Super8-mm camcorder, and by M.H. using a tri-pod-mounted Panasonic PV 900 camcorder.In most cases the subjects were 5 or moremeters from the camera, minimizing paral-lax problems (Plagenhoef, 1979; Winter,1990). Video analysis was performed on aPanasonic AG-6300 VCR, using frame-by-frame playback (30 frames/sec) to identifysteps in which the subject was traveling in arelatively straight path, approximately per-pendicular to the line of sight of the camera.Only walking gaits were analyzed of stepson substrates inclined no more than 20° tothe horizontal.

Video images were imported into a 486microcomputer with a PC-Vision1 videoframe grabber board, and digitized forquantitative analysis with Java Video Anal-ysis computer software from Jandel Scien-tific (Sausalito, CA). The orientation of thearm (shoulder to elbow) and the entire fore-limb (shoulder to contact point) relative tothe trunk (shoulder to hip) at hand touch-down and liftoff were digitized, as well asthe inclination of the trunk relative to hor-izontal and the orientation of the substrate.The angles of the humerus and forelimb rel-ative to a line perpendicular to the sub-strate passing through the shoulder joint athand touchdown and lift-off were later com-puted trigonometrically. As no significantdifferences were found between steps onhorizontal substrates compared to theslightly inclined or declined substrates (20°or less), all steps for a species were pooledand limb angles are described as being rel-ative to a vertical line passing through theshoulder joint.

Given the nature of the data source, itwas not possible to control for speed or sub-strate type, or to correct for any out-of-planemotion. In addition, it should be empha-sized that none of the zoo subjects wereshaved to help identify joint centers. Whilebony landmarks indicating joint positions

can in most cases be easily identified onlarger animals, the fur of very small sub-jects tends to obscure such landmarks.These data, then, are at best approxima-tions of limb posture kinematics. However,as an indication of the accuracy of thesemethods, arm angle data at hand touch-down and liftoff collected here for two pri-mate species, Chlorocebus aethiops andSaimiri sciureus, were compared to infor-mation published by Vilensky and Gan-kiewicz (1990) and Vilensky et al. (1994)1

acquired under more controlled laboratoryconditions. In all cases, the published val-ues fell within one standard deviation of ourspecies means.

Video data were collected on 95 quadru-pedal mammalian species. Data on an addi-tional 7 species of nonprimate mammalswere derived from the literature (see Table1) to yield a total of 102 species, including 53primates and 49 nonprimates. The nonpri-mate sample included 4 marsupials, 7 ro-dents, 23 carnivores, 13 ungulates, 1 hyrax,and 1 tupiid. Since the latter two were thesole representatives of their orders, for sim-plicity of comparisons, they were groupedwith the rodents because of their similarbody size and form. The primate sampleincluded 10 lorisoids, 7 lemuroids, 14 ceboidspecies, 18 cercopithecoids, and 4 homi-noids. All nonprimate species were withinthe size range of nonhuman primates (60g–160 kg).

An effort was made to digitize at least10 steps from every species, but this wasnot always possible.2 Mean values for limbangles for each species were grouped intoorders. Since limb excursion angles arepotentially correlated to body size (McMa-hon, 1975, 1984), differences betweenmammalian orders were analyzed withANCOVAs, using the General Linear Mod-els Procedure of SAS (SAS Institute, Cary,NC, 1988), with the angle of interest beingthe dependent y-variable, and body sizebeing the independent x-variable (Sokaland Rohlf, 1981). The procedure computed

1In both cases, published values were estimated from graphs.2The number of steps analyzed from the videotapes is

included in Table 1.

88 S.G. LARSON ET AL.

TABLE 1. List of species studied

Species Common name Body size (kg)1 No. of steps analyzed

Primates2

CheirogaleidsCheirogaleus major Greater dwarf lemur 0.40 31Cheirogaleus medius Fat-tailed dwarf lemur 0.28 22Microcebus murinus Gray mouse lemur 0.12 27Mirza coquereli Coquerel’s dwarf lemur 0.31 18

GalagidsGalago senegalensis Senegal bushbaby 0.19 9Otolemur garnetti Small-eared greater bushbaby 0.76 66

LorisidsLoris tardigradus Slender loris 0.19 31Nycticebus coucang Slow loris 0.65 21Nycticebus pygmaeus Pygmy slow loris 0.42 30Perodicticus potto Potto 1.10 23

LemuridsEulemur coronatus Crowned lemur 1.65 7Eulemur fulvus Brown lemur 2.21 39Eulemur macaco Black lemur 2.44 62Eulemur mongoz Mongoose lemur 1.62 26Hapalemur griseus Gentle lemur 0.94 40Lemur catta Ring-tailed lemur 2.21 28Varecia variegata Ruffed lemur 3.49 38

CebidsAotus trivirgatus Owl monkey 0.77 21Cebuella pygmaea Pygmy marmoset 0.12 3Cebus albifrons White-fronted capuchin 2.73 10Cebus apella Tufted capuchin 3.08 15Saguinus geoffroyi Geoffroy’s tamarin 0.49 3Saguinus midas Golden-handed tamarin 0.54 5Saimiri sciureus Squirrel monkey 0.72 12

AtelidsAlouatta caraya Black howler monkey 5.37 3Alouatta seniculus Red howler monkey 5.95 26Aletes belzebuth Long-haired spider monkey 8.07 11Ateles paniscus Black spider monkey 8.77 14Callicebus moloch Dusky titi monkey 0.99 5Lagothrix lagothricha Woolly monkey 7.15 14Pithecia pithecia White-faced saki 1.76 15

CercopithecinesCercocebus galeritus Tana River mangabey 7.40 18Cercopithecus ascanius Red-tailed monkey 3.31 5Cercopithecus diana Diana monkey 4.55 19Cercopithecus lhoesti L’Hoest’s monkey 4.71 2Cercopithecus mitis Blue monkey 6.09 26Cercopithecus neglectus De Brazza’s monkey 5.74 1Chlorocebus aethiops Vervet monkey 3.62 27Erythrocebus patas Patas monkey 9.45 23Macaca fascicularis Long-tailed macaque 4.48 17Macaca mulatta Rhesus macaque 9.90 26Mandrillus sphinx Mandrill 22.25 29Miopithecus talapoin Talapoin monkey 1.25 13Papio anubis Olive baboon 19.20 20

ColobinesColobus angolens Angolan colobus monkey 8.62 7Nasalis lavartus Proboscis monkey 20.40 7Pygathrix nemaeus Douc langur 9.72 9Trachypithecus cristata Silvered leaf monkey 6.18 4Trachypithecus francoisi Francois’ leaf monkey 7.52 3

PongidsGorilla gorilla Lowland gorilla 121.00 21Pan paniscus Bonobo 38.20 4Pan troglodytes Chimpanzee 53.00 21Pongo pygmaeus Orangutan 57.00 18

FORELIMB POSTURE IN QUADRUPEDAL PRIMATES 89

(continued)

an adjusted mean (least squares mean) foreach order, in which the effect of body sizehas been accounted for. In addition, thestandard errors of the adjusted means,

and pairwise comparisons of statisticaldifferences between means, were calcu-lated. A similar procedure was performedon primate species grouped into families

TABLE 1. Continued

Species Common name Body size (kg)1 No. of steps analyzed

CarnivoresAcinonyx jubatus Cheetah 53.50 10Ailuris fulgens Red panda 4.00 11Arctictis binturong Binturong 11.50 8Canis familiaris3 Domestic dog 11.25Cryptoprocta ferox Fossa 9.50 6Eira barbara Grey-headed tayra 4.50 9Felis caracal Caracal 16.00 26Felis catus4 Domestic cat 3.50Felis silvestris Wild cat 5.50 3Felis wiedii Margay 6.50 2Hyaena hyaena Striped hyaena 40.00 15Martes flavigula Yellow-throated marten 2.50 2Mephitis mephitis Striped skunk 1.75 1Mungos mungo Banded mongoose 1.60 11Mustela putorius5 European polecat 0.90Nasua nasua Brown coati 4.00 5Neofelis nebulosa Clouded leopard 19.50 3Panthera onca Jaguar 85.00 12Panthera pardus Leopard 60.00 11Procyon lotor Racoon 6.50 2Suricata suricatta Meerkat 0.79 10Tremarctos ornatus Spectacled bear 100.00 24Vulpes corsac Corsac fox 5.50 7

MarsupialsCaluromys philander Woolly opossum 0.30 10Dendrolagus matschiei Tree kangaroo 7.20 9Didelphis virginiana6 Virginia opossum 2.31Phascolarctos cinereus Koala 9.30 10

RodentsDasyprocta aguti Orange-rumped agouti 2.65 15Dinomys branickii Pacarana 12.50 2Dolichotis patagonum Patagonian cavy 12.50 6Heterohyrax brucei5,7 Gray hyrax 1.20Hydrochaeris hydrochaeris Capybara 50.50 1Mesocricetus auratus5 Golden hamster 0.10Myoprocta acouchy Acouchy 0.95 3Rattus norvegicus5 Brown rat 0.50Tupaia glis7 Tree shrew 0.17 3

UngulatesCapricornis crispus Japanese serow 75.00 5Damaliscus dorcas Blesbok 91.50 6Gazella dama Mhorr’s gazelle 57.50 7Gazella dorcas Dorcas gazelle 17.50 9Gazella soemmerringi Soemmering’s gazelle 42.00 1Madoqua guentheri Guenther’s dik dik 4.60 5Muntiacus muntjac Muntjac 16.00 2Neotragus moschatus Suni 6.50 5Odocoileus virginianus Deer 150.00 4Ovis vignei Transcapian urial 50.00 10Rangifer tarandus Reindeer 95.50 4Saiga tatarica Saiga antelope 47.00 10Sylvicapra grimmia Gray duiker 18.50 2

1 Mean body sizes for species taken from the literature (average of male and female if reported separately). Sources: Macdonald(1984a,b); Nowak (1991); Smith and Jungers (1997).2 Taxonomy after Fleagle (1999).3 Data from Nomura et al. (1966) and Tokuriki (1973).4 Data from Miller and Van der Meche (1975) and English (1978a,b).5 Data from Jenkins (1971).6 Data from Jenkins and Weijs (1979).7 Hyraxes and tree shrews are not rodents but members of the orders Hyracoidea and Scandentia, respectively. However, to simplifycomparisons, they were grouped with the rodents because of their similar size and body form.


or subfamilies to explore for differencesacross the order.

RESULTS

Figure 1 shows the angle of the humerusat touchdown relative to body size acrossthe sample. The angles are expressed rela-tive to a vertical line through the shoulder:positive values reflect a humerus that isahead of vertical, and negative numbers re-flect a humerus that is positioned behindvertical. It is clear that at any body size,nonhuman primates have a more protractedhumerus than any nonprimate mammal,with the interesting exception, Caluromysphilander, being an arboreal marsupial.The koala (Phascolarctos cinereus), anotherarboreal marsupial, also approaches the pri-mate range.

For ease of comparison, Figure 2 presentsa graph of just the group means for protrac-

tion angle at touchdown, retraction angle atliftoff, and total angular excursion of thehumerus and of the entire forelimb for eachof the mammalian groups. The positivetouchdown angle of the humerus of pri-mates stands in marked contrast and is sig-nificantly different from those of the othermammalian groups (Table 2). Primate hu-meri are also less retracted at liftoff thanthose of other mammalian groups, andagain this difference is statistically signifi-cant. Even though primates do not retracttheir humeri as far as other mammaliangroups during a step, the total excursion ofthe arm is still significantly greater thanthat of all other mammalian groups exceptthe marsupials.

The excursion angles of the forelimb re-flect how these differences in humeral ex-cursion affect the motion of the entire limb.Although all mammals display a protracted

Fig. 1. Mean humeral touchdown angle plottedagainst mean body size (see Table 1) for each species.Angles are described relative to a vertical line passingthrough the shoulder to the substrate. Positive valuesdenote a humerus positioned in front of the vertical;negative values reflect a position behind the vertical.Primates are represented by circles, marsupials bystars, carnivores by triangles, rodents (including thehyrax and tree shrew) by squares, and ungulates by

diamonds. Primates display larger humeral protractionangles than almost any other mammal. The notableexceptions are the woolly opossum, Caluromys philan-der, which is an arboreal, small-bodied species showingother convergences with primates in hand and foot pro-portions (Lemelin, 1996, 1999), and the koala, Phasco-larctos cinereus, which also occupies an arboreal habi-tat.


forelimb at touchdown since the forefootmust land ahead of the shoulder to preventthe animal from falling forward, the degreeof forelimb protraction at touchdown isagain significantly greater in primates.There are no significant differences betweenany of the groups in the degree of forelimbretraction at liftoff; however, the total angu-lar excursion of the forelimb is still larger inprimates compared to the other mammaliangroups (statistically different for all exceptthe marsupials).

Figure 3 displays a schematic representa-tion of these differences in limb postureacross mammals. The cartoons are drawn asif the animals are all the same size andshare equal total limb lengths (humerus 1forearm length). However, the relative pro-portions of the proximal to distal limb seg-ment lengths have been adjusted to morerealistically portray the limbs of cursorilyadapted species (carnivores and ungulates)and noncursorial species (marsupials and

rodents). In each case, the small dark trian-gle represents humeral excursion, and thelighter triangle is total forelimb excursion.The distal limb segment was simply drawnto connect the distal end of the humerus tothe line representing the forelimb angle,and therefore, elbow angles should not betaken as necessarily accurate. The positionof the liftoff foot above the substrate is likelydue to unaccounted-for scapular motion,which unfortunately could not be docu-mented in this study. As illustrated in Fig-ure 3, not only do primates utilize largerhumeral and forelimb excursion angles, buttheir limb excursion is more nearly symmet-ric around a vertical line from the shoulderto the substrate.

Having shown that primates as a groupdiffer from other mammalian groups, it isalso important to consider whether there isvariation in these postural characteristicswithin primates. Figure 4 displays meanhumeral and forelimb angles for the pri-

Fig. 2. Raw mean humeral and forelimb excursionangles for all mammalian groups sampled. Angles areexpressed relative to a vertical line passing through theshoulder. Total humeral excursion angle (TOTAL-HUM) equals humeral touchdown angle (TD-HUM)

plus the absolute value of humeral liftoff angle (LO-HUM). Similarly, total forelimb excursion angle(TOTAL-LIMB) equals forelimb touchdown angle (TD-LIMB) plus the absolute value of forelimb liftoff angle(LO-LIMB). See text for further discussion.


mate sample sorted by families (with thetwo subfamilies of cercopithecoids also sep-arated). The families are arranged fromsmallest to largest average body size,3 sug-gesting some influence of overall size on hu-meral excursion, with a pattern of decreas-

ing degree of protraction and retraction ofthe humerus at touchdown and liftoff lead-ing to smaller total humeral excursion asaverage body size increases. However, it isclear that in all primate families, the hu-merus touches down in a protracted position(see Table 3). Despite these differences inhumeral excursion angles, forelimb excur-sion angles appear fairly uniform across pri-mates, especially limb angle at touchdown.While there is some indication of decreasing

3Average body size for the lemurids actually exceeds that ofthe cebids sampled here, but they were put in reverse order inFigure 4 so that the lemurids could be more directly comparedwith the other prosimian families, and the cebids could be com-pared to the atelids.

TABLE 2. Raw and least square means for sample species grouped into orders

TD-HUM MEAN LSMEANStd err

LSMEANProbability level for H0: LSMEAN(i) 5 LSMEAN(j )

Marsupials Rodents Ungulates Primates

Primate 28.07 28.06 1.44Carnivores 27.08 27.08 2.12 Carnivores 0.2281 0.0039 0.0001 0.0001Marsupials 20.34 20.37 5.10 Marsupials 0.0026 0.0001 0.0001Rodents 220.05 220.06 3.84 Rodents 0.0010 0.0001Ungulates 237.30 237.23 3.15 Ungulates 0.0001

LO-HUM MEAN LSMEANStd err



Primates 256.82 255.08 1.67Carnivores 266.25 266.78 2.45 Carnivores 0.5743 0.1577 0.0783 0.0002Marsupials 273.13 270.39 5.91 Marsupials 0.6232 0.5606 0.0138Rodents 275.30 274.03 4.45 Rodents 0.9318 0.0001Ungulates 267.04 274.53 3.65 Ungulates 0.0001

TOTAL-HUM MEAN LSMEANStd err

















limb retraction angle and decreasing totalexcursion with increasing body size, the dif-ferences are small, and most are not statis-tically significant.

DISCUSSION

The video data analyzed here were col-lected under less than ideal conditions.Nonetheless, the results suggest that thedifferences between primates and nonpri-mate mammals are so large that even theseinexact techniques reveal meaningful infor-mation. All quadrupedal primates begin awalking step with a protracted humerusand retract the limb through a large angu-lar excursion as the step proceeds. This con-trasts sharply with the either vertical orretracted position of the humerus at touch-down and smaller excursion angles of mostother quadrupedal mammals. While thesestatements are broadly true across pri-mates, there is some variability within the

order, and these differences certainly meritfurther study. However, analysis of moresubtle kinematic differences requiresgreater uniformity in variables such as sub-strate type and speed, and are thereforeprobably best pursued in a more controlledlaboratory setting.

The protracted position of the humerus inprimates results in a more obtuse glenohu-meral joint angle, and thus a more verticallyaligned scapula and humerus. This is incontrast to a more acute glenohumeral an-gle and more crouched posture of most othernoncursorial mammals. Scapular and hu-meral alignment increases the effectivelength of the limb and augments the alreadyrelatively long limb bone segments (femur,tibia, humerus, and ulna) of primates (Alex-ander et al., 1979). Since limb length andlimb angular excursion are directly relatedto stride length, one might propose that thecombination of a long forelimb with large

Fig. 3. Schematic representations of limb posturesin different mammalian groups constructed from meanhumeral and forelimb excursion angles. In all cartoons,body size and total forelimb length (proximal 1 distalsegments) are equal. However, the relative proportionsof the proximal and distal segments have been adjustedto better reflect typical limb proportions in different

mammalian groups. Larger, lightly shaded trianglesrepresent total forelimb excursion, i.e., the differencebetween forelimb touchdown angle and forelimb liftoffangle. Smaller, darkly shaded triangles similarly rep-resent total humeral excursion. See text for furtherdiscussion.


Fig. 4. Raw mean humeral and forelimb excursion angles for primates sorted into families, with thecercopithecoids separated into subfamilies Cercopithecinae and Colobinae (taxonomic sorting taken fromFleagle, 1999). Groups are arranged from smallest to largest average body size with the exception of thelemurids and cebids, which are switched in order to make more direct comparisons with other membersof their superfamilies. See text for discussion.


TABLE 3. Raw and least square means for primate families or subfamilies



Gala Loris Lem Ceb Atel Cerco Col Pon

Cheirogaleids 38.00 38.24 2.84 Chei 0.5858 0.3862 0.1619 0.0087 0.0015 0.0001 0.0017 0.0091Galagids 40.62 40.85 3.95 Gala 0.2131 0.0953 0.0088 0.0022 0.0001 0.0022 0.0060Lorisids 34.61 34.83 2.84 Loris 0.6654 0.0847 0.0190 0.0003 0.0185 0.0313Lemurids 33.14 33.33 2.15 Lem 0.1268 0.0236 0.0001 0.0234 0.0407Cebids 28.54 28.75 2.18 Ceb 0.3959 0.0147 0.3442 0.1783Atelids 26.02 26.10 2.26 Atel 0.1436 0.8783 0.3260Cercopithecines 22.02 22.06 1.53 Cerco 0.2300 0.7318Colobines 25.62 25.59 2.46 Col 0.3535Pongids 21.55 20.08 5.40









TD-LIMB MEAN LSMEANStd err




LO-LIMB MEAN LSMEANStd err




TOTAL-LIMB MEAN LSMEANStd err




angular excursion is for the purpose of in-creasing relative stride length, which has1indeed been documented for nonhumanprimates(Vilensky,1980;AlexanderandMa-loiy, 1984; Reynolds, 1987). However, whatadvantage long stride length offers pri-mates has remained unclear.

Stride length times the rate of strideequals speed, and therefore, animals pre-sumably may change either or both toachieve different speeds. Since primates userelatively low stride frequencies (Alexanderet al., 1979; Reynolds, 1987), long stridelength may be a compensation to maintainspeed. Indeed, Demes et al. (1990) arguedthat at least in lorisids, long stride length isa more effective way of achieving higherwalking speeds in an arboreal habitat pre-cisely because it does not entail high stridefrequency. Fast, high-frequency gaits pro-duce steeply rising, relatively high peakforces that could cause significant branchsway, which is both dangerous and energy-costly. In addition, lorisids search for preyand avoid predators by being cryptic; thus,long, low-frequency strides that minimizebranch swaying motions also avoid alertingeither predator or prey.

However, most primates are not cryptic,and while there is continuing debate aboutwhether the locomotor mode of the ancestraleuprimate emphasized “grasp-leaping” (e.g.,Martin, 1972; Szalay and Delson, 1979; Sza-lay and Dagosto, 1980; Dagosto, 1988; Gebo,1989), vertical clinging and leaping (Napierand Walker, 1967), or arboreal, quadrupe-dal walking and running (e.g., Godinot andJouffroy, 1984; Ford, 1988), there is littlethat suggests a form of cautious quadrupe-dalism as in lorisids. In this context, whatadvantage do forelimb protraction, large an-gular excursion, and limb elongation offerbesides increased stride length?

Limb elongation, at least, is seen in othermammals such as many carnivores and un-gulates. The elongation observed in theseforms, usually grouped together as cursors,has been brought about by lengthening thedistal elements of the limb, including thefingers (Alexander et al., 1979). Distal elon-gation is generally viewed as a means ofreducing the inertial properties of the limbby concentrating mass proximally, thereby

making it easier to swing the limb forwardand increasing running efficiency (Smithand Savage, 1956; Hildebrand, 1988). How-ever, in so doing, these animals have sacri-ficed any ability to grasp with their hands orfeet. Alternatively, those mammalian spe-cies that have retained more grasping ex-tremities tend to have relatively shorterlimbs.

By lengthening the proximal and inter-mediate limb segments, primates haveevolved the unique combination of relativelylong limbs with grasping extremities. Ac-cording to most proposals that have beenoffered to explain the origins of primates,the evolution of clawless grasping extremi-ties is related to travel and foraging in asmall-branch arboreal setting (Cartmill,1972, 1974, 1992; Garber, 1980; Rasmussen,1990; Sussman, 1991; Hamrick, 1998; for acontrary view, see Soligo and Muller, 1999).Is there any reason why elongated limbsand a more protracted forelimb postureshould also be associated with this environ-ment? We suggest that reaching out withclawless, grasping hands in a small-branchsetting forms the foundation for the distinc-tive primate forelimb posture during walk-ing. It is interesting to note in this contextthat one nonprimate species that displays adegree of humeral protraction within theprimate range, Caluromys philander, alsouses grasping extremities to travel and for-age in a small-branch setting, and showsother convergences in hand and foot propor-tions to cheirogaleid primates (Lemelin,1996, 1999). Similarly, the species display-ing the next closest forelimb protraction an-gle to that of primates is the koala (Phasco-larctos cinereus), also an arboreal, climbing-adapted marsupial.

To travel or forage in an arboreal small-branch habitat using clawless, graspinghands, an animal must be able to reach outprecisely to gain a secure grip on a particu-lar branch or object. This is especially trueof the climbing and scrambling forms of lo-comotion usually associated with the small-branch milieu. Nonstereotypical forelimbmotion demands versatility in the neuralcontrol of limb movement, and as Georgopo-lulos and Grillner (1989) have shown, thisentails a greater degree of supraspinal con-


https://www.researchgate.net/publication/13365349_Nails_and_Claws_in_Primate_Evolution?el=1_x_8&enrichId=rgreq-4dc9e7dc-5f43-4b8a-bf73-38e126384e94&enrichSource=Y292ZXJQYWdlOzEyNTQ5NTMwO0FTOjIwMDAzMTMzNzQ4ODM4NEAxNDI0NzAyNTk1MjEx

trol4 of forelimb movements. They also re-port that the corticospinal input involved incorrect positioning of the forelimbs duringlocomotion is the same as that involved inforelimb manipulatory movements. Geor-gopolulos and Grillner (1989) propose thatthe ability to use the forelimb for manipu-lation evolved from the ability to accuratelyposition the limb during locomotion.

It follows that as supraspinal control ofprecise locomotor forelimb positioning de-veloped, so did fine control of forelimb move-ment for foraging and manipulation. How-ever, use of the forelimb for foraging,manipulation, and nonstereotypical locomo-tor motions also depends on enhanced mo-bility at the forelimb joints to increase therange of motion of the limb. Larson (1998)pointed out that increasing the mobility ofjoints generally can only be accomplished atthe expense of stability, and cannot developif the forelimbs are subjected to large dis-ruptive locomotor forces. She suggested thatmany of the distinctive characteristics ofprimate quadrupedal locomotion can be re-lated to mechanisms that primates utilize toattenuate the disruptive forces to which theforelimbs are subjected. Among these mech-anisms are alteration of muscle recruitmentpatterns (Larson and Stern, 1989, Vilenskyand Larson, 1989; Larson, 1998), greaterreliance on the hind limbs than the fore-limbs for both support and propulsion(Kimura et al., 1979; Kimura, 1985; Reyn-olds, 1985; Demes et al., 1992, 1994), anduse of a more compliant gait (Schmitt, 1995,1998, 1999).

A compliant gait is characterized by sub-stantial limb yield (joint flexion duringstance phase) during a step, longer steplength, and longer contact time compared toa stiffer walk. The mechanics of compliantgait have been described in detail elsewhere(Alexander, 1977, 1992; Taylor, 1985; Mc-Mahon, 1985; McMahon et al., 1987; Blick-han, 1989; Farley et al., 1993; Schmitt,1995, 1998, 1999), and will only be brieflysummarized here. Long step length andlong contact time reduce peak stresses act-

ing on the limb by increasing the time overwhich they develop. While it has often beenpostulated that primates crouch when walk-ing on branches to lower their center ofmass to better maintain balance (e.g.,Napier, 1967; Grand, 1968a,b, 1984;Fleagle, 1978; Morbeck, 1979; Cartmill,1985), Schmitt (1995, 1998, 1999) has docu-mented that this crouch is brought about ina compliant manner by increasing elbowyield during support phase, which also in-creases contact time. In addition, elbowyield helps reduce vertical oscillations of thebody’s center of mass, giving it a lower, flat-ter trajectory (Schmitt, 1995, 1998). We sug-gest that initial limb protraction also lowersthe body’s center of mass at the beginning ofa step. More importantly, beginning a stepwith the forelimb in a protracted positionand then having it pass through a largeangular excursion has the effect of furtherincreasing step length and contact time.Thus the combination of elbow yield associ-ated with a compliant gait, and initial limbprotraction, work together to produce acrouching posture that is critical for main-taining balance and stability on a branch, aswell as reducing the tendency to causebranch sway. They thereby augment the in-creased stabilization brought about directlyby increased contact time (Cartmill, 1985;Demes et al., 1990; Schmitt, 1995, 1998,1999). Finally, it should be noted that somekinetic advantage may derive from initiallimb protraction alone. McMahon et al.(1987) have demonstrated that by changingthe “angle of attack” of a limb, a protractedlimb position at touchdown reduces verticallanding speed and vertical stiffness of thebody, which attenuates some of the forcesassociated with impact.

Thus the unique characteristics of pri-mate forelimb posture during walking ob-served here can be seen as integral compo-nents of several mechanisms that helpreduce disruptive locomotor forces on fore-limb joints, as well as increase security onsmall branches. However, current consen-sus suggests that the earliest primates werevery small, perhaps mouse size (Martin,1972; Cartmill, 1974; Dagosto and Ter-ranova, 1992; Rose, 1995; for a contraryview, see Soligo and Muller, 1999), and it is

4Uncomplicated locomotion on an even surface is believed tobe controlled largely by the spinal cord in most animals.


unclear just how disruptive locomotor forcesmight be on the forelimb joints of such smallanimals. Therefore, the development of suchthings as a compliant gait may have notoccurred until later in primate evolution,when larger species began to appear. Aslarger species evolved, however, adoption ofthese stabilizing and force reducing mecha-nisms would have been facilitated by preex-isting forelimb elongation and protractionthat had already evolved as functional ad-aptations to reaching out and securing gripsin the discontinuous small-branch habitat.

In order to determine the validity of theseproposals, it would be useful to know whena more protracted humeral posture andlarger angular excursion first appeared inthe evolution of primates. However, answer-ing this question depends on being able toidentify morphological correlates of thesepostural features. To this end, an investiga-tion is currently underway (by S.G.L.) toidentify traits of the scapula and proximalhumerus distinguishing primates from non-primates that could be indicative of use of amore protracted humerus in early eupri-mates. Documentation of the appearanceand distribution of such features in eupri-mate fossils will hopefully help us to betterunderstand the early evolution and radia-tion of primates.

CONCLUSIONS

Primates are distinguished from mostother mammals in displaying a more pro-tracted forelimb posture and greater fore-limb angular excursion during quadrupedalwalking. We propose that these uniquecharacteristics can be related to several in-terconnected selective factors that were in-volved in the successful occupation and ra-diation of primates in the arboreal small-branch niche.

In order to effectively travel and forage ina discontinuous, complex small-branch en-vironment, early primates needed to be ableto reach out and achieve a secure grip on abranch or a food object. This selected notonly for clawless grasping extremities, butalso for greater cortical control of forelimbmovements. Limb elongation might alsobeen advantageous in this context. As corti-cal control of the forelimb for locomotion

increased, so did forelimb manipulatoryabilities improve, thus enhancing manualforaging. The increasing versatility in fore-limb use would be augmented by greatermobility in forelimb joints to increase therange of motion. Greater joint mobility, inturn, would select for mechanisms that re-duced the disruptive forces experienced byforelimb joints during locomotion, especiallyas species with larger body sizes evolved.These mechanisms could take advantage ofthe somewhat increased limb length andforward range of motion of the forelimb as-sociated with reaching out for a secure grip,to begin a step with the limb in a moreprotracted position, and thereby increasinglimb excursion as well as augmenting steplength and contact time. These changes ingait would have the added advantages ofincreasing stability on small branches andreducing dangerous and energy-costlybranch sway. Further increases in the de-gree of forelimb protraction and limb elon-gation associated with these gait changesmight in turn improve the ability to reachout with the forelimb to move and forage inthe small-branch habitat.

ACKNOWLEDGMENTS

This study is based on videotape of ani-mals at the following institutions: Brook-field Zoo, Chicago, IL; Bronx Zoo, New York,NY; Cleveland Zoo, Cleveland, OH; Pitts-burgh Zoo, Pittsburgh, PA; San Diego Zoo,San Diego, CA; Duke Primate Center,Durham, NC; Primate Locomotion Labora-tory, Stony Brook, NY; and Laboratoired’Ecologie Generale, CNRS/Unite de Re-cherche 1183, Brunoy, France. P.L. thanksDrs. Martine Atramentowicz, Jean-PierreGasc, and Francoise K. Jouffroy, who as-sisted him in videotaping Caluromys phi-lander in France. This research was sup-ported by grants from the L.S.B. LeakeyFoundation to S.G.L. and M.H., and byNSF grants BCS 9806291 to S.G.L., SBR-9320237 to M.H., and SBR-9318750 to P.L.

LITERATURE CITED

Alexander RM. 1977. Mechanics and scaling of terres-trial locomotion. In: Pedley T, editor. Animal locomo-tion. London: Academic Press. p 93–110.


Alexander RM. 1992. A model of bipedal locomotion oncompliant legs. Philos Trans R Soc Lond [Biol] 338:189–198.

Alexander RM, Maloiy GMO. 1984. Stride lengths andstride frequencies of primates. J Zool Lond 202:577–582.

Alexander RM, Jayes AS, Maloiy GMO, Wathuta EM.1979. Allometry of the limb bones of mammals fromshrews (Sorex) to elephant (Loxodonta). J Zool Lond189:305–314.

Blickhan R. 1989. The spring-mass model for runningand hopping. J Biomech 22:1217–1227.

Cartmill M. 1972. Arboreal adaptations, and the originof the order Primates. In: Tuttle R, editor. The func-tional and evolutionary biology of primates. Chicago:Aldine. p 97–122.

Cartmill M. 1974. Pads and claws in arboreal locomo-tion. In: Jenkins FA Jr, editor. Primate locomotion.New York: Academic Press. p 45–83.

Cartmill M. 1985. Climbing. In: Hildebrand M, BrambleDM, Liem KF, Wake DB, editors. Functional verte-brate morphology. Cambridge: Belknap Press. p 73–88.

Cartmill M. 1992. New views on primate origins. EvolAnthropol 1:105–111.

Dagosto M. 1988. Implications of postcranial evidencefor the origin of euprimates. J Hum Evol 17:35–56.

Dagosto M, Terranova CJ. 1992. Estimating the bodysize of Eocene primates: a comparison of results fromdental and postcranial variables. Int J Primatol 13:307–344.

Demes B, Jungers WL, Nieschalk U. 1990. Size- andspeed-related aspects of quadrupedal walking in slen-der and slow lorises. In: Jouffroy FK, Stack MH,Niemitz C, editors. Gravity, posture and locomotionin primates. Florence: Il Sedicesimo. p 175–197.

Demes B, Larson SG, Stern JT Jr, Jungers WL. 1992.The hindlimb drive of primates—theoretical reconsid-eration and empirical examination of a widely heldconcept. Am J Phys Anthropol [Suppl] 14:69.

Demes B, Larson SG, Stern JT Jr, Jungers WL,Biknevicius AR, Schmitt D. 1994. The kinetics of“hind limb drive” reconsidered. J Hum Evol 26:353–374.

English AW. 1978a. An electromyographic analysis offorelimb muscles during overground stepping in thecat. J Exp Biol 76:105–122.

English AW. 1978b. Functional analysis of the shouldergirdle of cats during locomotion. J Morphol 156:279–292.

Farley CT, Glasheen J, McMahon TA. 1993. Runningsprings: speed and animal size. J Exp Biol 185:71–86.

Fleagle JG. 1978. Locomotion, posture and habitat useof two sympatric leaf-monkeys in West Malaysia. In:Chivers DJ, Herbert J, editors. Recent advances inprimatology, volume 1, behavior. New York: Aca-demic Press. p 331–336.

Fleagle JG. 1999. Primate adaptation and evolution.2nd ed. London: Academic Press.

Ford SM. 1988. Postcranial adaptations of the earliestplatyrrhine. J Hum Evol 17:155–192.

Garber P. 1980. Locomotor behavior and feeding ecologyof the Panamanian tamarin (Saguinus oedipus geof-froyi, Callitrichidae, Primates). Int J Primatol 1:185–201.

Gebo DL. 1989. Locomotor and phylogenetic consider-ations in anthropoid evolution. J Hum Evol 18:201–233.

Georgopoulos AP, Grillner S. 1989. Visuomotor coordi-nation in reaching and locomotion. Science 245:1209–1210.

Godinot M, Jouffroy FK. 1984. La main d’Adapis (Pri-mates, Adapidae). In: Buffetaut E, Mazin JM,Salmion E, editors. Actes du Symposium Paleon-tologique G. Cuvier. Paris: Montbeliard. p 221–242.

Grand T. 1968a. Functional anatomy of the lower limbof the howler monkey (Alouatta caraya). Am J PhysAnthropol 28:163–181.

Grand T. 1968b. Functional anatomy of the upper limb.In: Biology of the howler monkey (Alouatta caraya).Bibl Primatol 7:104–125.

Grand T. 1984. Motion economy within the canopy: fourstrategies for mobility. In: Rodman P, Cant J, editors.Adaptations for foraging in nonhuman primates: con-tributions to an organismal biology of prosimians,monkeys and apes. New York: Columbia UniversityPress. p 54–72.

Hamrick MW. 1998. Functional and adaptive signifi-cance of primate pads and claws: evidence from NewWorld anthropoids. Am J Phys Anthropol 106:113–127.

Hildebrand M. 1988. Analysis of vertebrate structure,3rd ed. New York: John Wiley and Sons.

Jenkins FA Jr. 1971. Limb posture and locomotion inthe Virginia opossum (Didelphis marsupialis) andother non-cursorial mammals. J Zool Lond 165:303–315.

Jenkins FA Jr, Weijs WA. 1979. The functional anat-omy of the shoulder in the Virginia opossum (Didel-phis virginiana). J Zool Lond 188:379–410.

Kimura T. 1985. Bipedal and quadrupedal walking ofprimates: comparative dynamics. In: Kondo S, editor.Primate morphophysiology, locomotor analyses andhuman bipedalism. Tokyo: University of Tokyo Press.p 81–104.

Kimura T, Okada M, Ishida H. 1979. Kinesiologicalcharacteristics of primate walking: its significance inhuman walking. In: Morbeck ME, Preuschoft H,Gomberg N, editors. Environment, behavior, andmorphology: dynamic interactions in primates. NewYork: Gustav Fischer. p 297–311.

Larson SG. 1998. Unique aspects of quadrupedal loco-motion in nonhuman primates. In: Strasser E,Fleagle J, Rosenberger A, McHenry H, editors. Pri-mate locomotion: recent advances. New York: PlenumPress. p 157–173.

Larson SG, Stern JT Jr. 1989. The role of propulsivemuscles of the shoulder during quadrupedalism invervet monkeys (Cercopithecus aethiops): implica-tions for neural control of locomotion in primates. JMotor Behav 21:457–472.

Lemelin P. 1996. The evolution of manual prehensilityin primates: a comparative and functional analysis inprosimian primates and didelphid marsupials. Ph.D.dissertation, University at Stony Brook.

Lemelin P. 1999. Morphological correlates of substrateuse in didelphid marsupials: implications for primateorigins. J Zool Lond 247:165–175.

Macdonald DW. 1984a. The encyclopedia of mammals.New York: Facts on File, Inc.

Macdonald DW. 1984b. All the world’s mammals: car-nivores. New York: Torstar Books, Inc.

Martin RD. 1972. Adaptive radiation and behavior ofthe Malagasy lemurs. Philos Trans R Soc Lond [Biol]264:295–352.

McMahon TA. 1975. Using body size to understand thestructural design of animals: quadrupedal locomo-tion. J Appl Physiol 39:619–627.

McMahon TA. 1984. Muscles, reflexes and locomotion.Princeton: Princeton University Press.

McMahon TA. 1985. The role of compliance in mamma-lian running gaits. J Exp Biol 115:263–282.


McMahon TA, Valiant G, Frederick EC. 1987. Grouchorunning. J Appl Physiol 62:2326–2337.

Miller S, Van der Meche FGA. 1975. Movements of theforelimbs of the cat during stepping on a treadmill.Brain Res 91:255–269.

Morbeck ME. 1979. Forelimb use and positional adap-tation in Colobus guereza: integration of behavioral,ecological and anatomical data. In: Morbeck M,Preuschoft H, Gomberg N, editors. Environment, be-havior, and morphology: dynamic interactions in pri-mates. New York: Gustav Fisher. p 95–118.

Napier JR. 1967. Evolutionary aspects of primate loco-motion. Am J Phys Anthropol 27:333–342.

Napier JR, Walker AC. 1967. Vertical clinging and leap-ing—a newly recognized category of locomotor behav-iour of primates. Folia Primatol (Basel) 6:204–219.

Nomura S, Sawazake H, Ibaraki T. 1966. Co-operatedmuscular action in postural adjustment and motionin dog, from the viewpoint of electromyographic kine-siology and joint mechanics. IV. About muscular ac-tivity in walking and trot. Jpn J Zootech Sci 37:221–229.

Nowak RM. 1991. Walker’s mammals of the world, 5thed. Baltimore: The Johns Hopkins University Press.

Plagenhoef S. 1979. Dynamics of human and animalmotion. In: Morbeck M, Preuschoft H, Gomberg N,editors. Environment, behavior, and morphology: dy-namic interactions in primates. New York: GustavFisher. p 95–118.

Rasmussen DT. 1990. Primate origins: lessons from aneotropical marsupial. Am J Primatol 22:263–277.

Reynolds TR. 1985. Stresses on the limbs of quadrupe-dal primates. Am J Phys Anthropol 67:351–362.

Reynolds TR. 1987. Stride length and its determinantsin humans, early hominids, primates, and mammals.Am J Phys Anthropol 72:101–116.

Rose KD. 1995. The earliest primates. Evol Anthropol5:159–173.

Schmitt D. 1995. A kinematic and kinetic analysis offorelimb use during arboreal and terrestrial quadru-pedalism in Old World monkeys. Ph.D. dissertation,University at Stony Brook.

Schmitt D. 1998. Forelimb mechanics during arborealand terrestrial quadrupedalism in Old World mon-keys. In: Strasser E, Fleagle J, Rosenberger A,McHenry H, editors. Primate locomotion: recent ad-vances. New York: Plenum Press, p 175–200.

Schmitt D. 1999. Compliant walking in primates. J ZoolLond 248:149–160.

Schmitt D, Larson SG, Stern JT Jr. 1994. Serratusventralis function in vervet monkeys (Cercopithecusaethiops): are primate quadrupeds unique? J ZoolLond 232:215–230.

Smith JM, Savage RJG. 1956. Some locomotor adapta-tions in mammals. J Linn Soc (Zool) 42:603–622.

Smith RJ, Jungers WL. 1997. Body mass in compara-tive primatology. J Hum Evol 32:523–559.

Sokal R, Rohlf J. 1981. Biometry. The principles andpractice of statistics in biological research. New York:Freeman.

Soligo C, Muller AE. 1999. Nails and claws in primateevolution. J Hum Evol 36:97–114.

Sussman RW. 1991. Primate origins and the evolutionof angiosperms. Am J Primatol 23:209–223.

Szalay FS, Dagosto M. 1980. Locomotor adaptations asreflected on the humerus of Paleogene primates. FoliaPrimatol (Basel) 34:1–45.

Szalay FS, Delson E. 1979. Evolutionary history of theprimates. New York: Academic Press.

Taylor CR. 1985. Force development during sustainedlocomotion: a determinant of gait, speed and meta-bolic power. J Exp Biol 115:253–262.

Tokuriki M. 1973. Electromyographic and joint-me-chanical studies in quadrupedal locomotion. I. Walk.Nippon Juigaku Zasshi [Jpn J Vet Sci] 35:433–448.

Vilensky JA. 1980. Trot-gallop transition in a macaque.Am J Phys Anthropol 53:347–348.

Vilensky JA. 1987. Locomotor behavior and controlin human and nonhuman primates: comparisonswith cats and dogs. Neurosci Biobehav Rev 11:263–274.

Vilensky JA. 1989. Primate quadrupedalism: how andwhy does it differ from that of typical quadrupeds?Brain Behav Evol 34:357–364.

Vilensky JA, Gankiewicz E. 1990. Effects of speed onforelimb joint angular displacement patterns invervet monkeys (Cercopithecus aethiops). Am J PhysAnthropol 83:203–210.

Vilensky JA, Larson SG. 1989. Primate locomotion: uti-lization and control of symmetrical gaits. Annu RevAnthropol 18:17–35.

Vilensky JA, Moore AM, Libii JN. 1994. Squirrel mon-key locomotion on an inclined treadmill: implicationsfor the evolution of gaits. J Hum Evol 26:275–386.

Winter DA. 1990. Biomechanics and motor control ofhuman movement. New York: John Wiley and Sons.


Uniqueness of primate forelimb posture during quadrupedal locomotion

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