Nonhuman Primate Locomotion - Wiley Online Library

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ondary osteon formation at the midshaft of the femur was correlated with locomotor differences among primates. Rafferty and Ruff (1994) used radiographs to ...
Received: 28 July 2017

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Revised: 9 November 2017

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Accepted: 10 November 2017

DOI: 10.1002/ajpa.23368

CENTENNIAL PERSPECTIVE

Nonhuman Primate Locomotion Susan G. Larson Department of Anatomical Sciences, Stony Brook University School of Medicine, Stony Brook, New York 11794-8081 Correspondence Susan G. Larson, Department of Anatomical Sciences, Stony Brook University School of Medicine, Stony Brook, NY 11794-8081 Email: [email protected]

1 | INTRODUCTION

world. There was little mention of nonhuman primates in the issues of AJPA from the 1920s other than in the context of understanding the

As an arboreal radiation of mammals, primates1 have access to a rich

origins of our species. Then as is the case now, analysis and interpreta-

set of resources including fruits, seeds, flowers, leaves, insects and the

tion of fossil material began with comparisons to our “simian” relations,

occasional lizard. To reach them they must navigate narrow diameter,

often with the viewpoint of an evolutionary progression beginning with

discontinuous supports that are oriented at angles ranging from hori-

primitive lemurs and culminating in the appearance of human beings.

zontal to vertical, and do so by engaging in a wide variety of locomotor

This perspective meant that the course of human evolution could be

behaviors. In addition to the quadrupedal walking, running and bound-

studied through comparative anatomy, as Dudley Morton attempted to

ing commonly observed among non-marine mammals, primates occa-

do through a series of comparative studies on human foot evolution

sionally walk bipedally, display jumping, leaping, and hopping behaviors,

(Morton, 1922, 1924, 1927). Although it is often said that early theo-

suspend themselves from their forelimbs, hind limbs, as well as all four

ries about human evolution emphasized brain size and tool use, on the

limbs, climb up and down vertical and inclined supports, utilize cantilev-

basis of his research on the foot, Morton concluded that, “The course

ered bridging between supports, and engage in a variety of non-

of human evolution was evidently characterized by progressive adapta-

stereotypical limb motions in order to scramble along small branches/

tions for erect terrestrial bipedism [sic], showing first in the feet and

lianas etc. Occupying an arboreal habitat, however, doesn’t necessarily

gradually extending upward to involve the entire body frame” (Morton,

lead to the diversity in locomotor behaviors observed among primates.

1927, p. 202; see also Ruff, this volume). He believed that bipedalism

A variety of other mammals like many rodents, carnivores, scandentians

in turn led to freeing of the upper limbs and the subsequent expansion

and marsupials also live in the trees but retain basic quadrupedal walk-

of the brain and the evolution of intelligence. This was long before the

ing, running, and bounding habits. The difference appears to be that

discovery and descriptions of australopithecine postcranial material in

while other mammals rely on claws to interlock with tree bark to avoid

the mid-twentieth century that established that a shift to upright pos-

falling, primates encircle narrow arboreal substrates with grasping

ture and bipedalism marked the earliest beginnings of the human line-

hands and feet tipped with flattened nails rather than claws. When,

age (also see Trinkaus, this volume).

how and why primates developed a dependence on grasping clawless

Of the limited research on nonhuman primates appearing in AJPA

extremities is a matter of continuing debate, but arguably underlies

in the 1920s and 1930s, that related to locomotion consisted of ana-

much of the locomotor diversity observed in the primate Order. Much

tomical descriptions of the musculoskeletal system (e.g., Schultz, 1924,

of the research establishing these generalization has appeared in the

1938; Ashley-Montagu, 1931; Midlo, 1934; Stewart, 1936). Other than

pages of the American Journal of Physical Anthropology (AJPA) and in

occasional references to positional behavior such as comments by Wei-

this review I will attempt to trace the development of many of these

denreich (1923) that most nonhuman primates walk with more ele-

ideas.

vated heels (digitigrade foot posture) than do humans, or that the primate foot is extremely supinated during climbing in the context of his study of human foot evolution, locomotor behavior was not a topic

2 | EARLY HISTORY

of research in AJPA, and attempts to link form and function were very Most of the research published in the early issues of the AJPA was on

general and vague. However, there were a few remarkable exceptions.

the attributes of modern human populations including the identification

One was Ruth Miller’s “Evolution of the Pectoral Girdle and Fore Limb

of the origins and interrelationships of different “races” across the

in the Primates” (1932). Although the focus was still on descriptive morphology, the study included a section summarizing the locomotor

1

Throughout this article, primates refers to nonhuman primates

Am J Phys Anthropol. 2018;165:705–725.

habits of different primate species mentioning among other things the

wileyonlinelibrary.com/journal/ajpa

C 2018 Wiley Periodicals, Inc. V

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F I G U R E 1 Reproduction of Plate 1 from Miller (1932)—Comparisons of the trapezius in a (1) dog, (2) lemur, (3) Old-World monkey, (4) gibbon, (5) gorilla, and (6) human

almost exclusive arboreality of New World monkeys, the secondarily

break.” Elftman and Manter (1935) also noted that in contrast to stand-

terrestrial locomotor habits of baboons, and the remarkable conver-

ing humans who are able to position their centers of gravity almost ver-

gence between gibbons and spider monkeys in locomotor behavior and

tically over their extended lower limb joints and thus maintain this

appearance. Following descriptions of pectoral girdle muscular anatomy

posture with minimal muscular effort, the position of the center of

across primate taxa with correlations to osteological features (Figure 1),

gravity of a chimpanzee standing bipedally necessitates using flexed

Miller went on to categorize complexes of features related to the

hip and knee joints and a much higher level of muscular effort to

mechanics of specific modes of locomotion. She noted that brachiating

remain stable.

primates exhibited enhanced development of the muscles associated

In the 1940s descriptions of new fossil hominins were becoming

with upper limb elevation such as trapezius, levator scapulae, deltoid

more common in the journal, and though most concerned skulls and

and supraspinatus, and also emphasized the important role of muscles

teeth, those on postcranial material often contained a rich supply of

like pectoralis, latissimus dorsi, infraspinatus, and teres major in sus-

comparative metrics on nonhuman primate postcrania (e.g., Straus,

pending the trunk below their supporting upper limbs. The study is

1948). Otherwise, the few papers on nonhuman primates that

remarkable in its breadth and depth, and remains an important resource

appeared mainly concerned descriptions of anatomical features unre-

today for those of us interested in primate forelimb function.

lated to locomotion. A notable exception is a study by Straus (1940)

Another pioneering paper on primate locomotion appearing in the 1930s was the study by Elftman and Manter (1935) comparing the feet of humans and chimpanzees during bipedal walking (see also Ruff, this volume). This is one of the first lab-based investigations of the locomotor characteristics of a living nonhuman primate, and included comparative information on the distribution of pressure on human and chimpanzee feet, and qualitative descriptions of foot kinematics during a bipedal step (Figure 2). Elftman and Manter (1935) related their observations to the anatomy of chimpanzee and human feet noting the existence of a transverse arch but no longitudinal arch in chimpanzees, and drawing attention to the mobility of their transverse tarsal joint and the occurrence of what has come to be known as the “mid-tarsal

Reproduction of figure 3 from Elftman and Manter (1935)—Fulcra of the human and chimpanzee feet in the course of a step

FIGURE 2

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707

that explored hand posture in great apes in an effort to determine why

of great apes. His paper included data on the sizes of both intrinsic and

they supported their weight on their knuckles (middle phalanges) rather

extrinsic chimpanzee hand muscles based on dissections of a large

that assuming a palmigrade hand posture as do most other primates.

series of chimpanzee cadavers (Figure 3), as well as descriptions of

He concluded that great apes have limited dorsiflexion capability due

osteological correlates of various aspects of the knuckle-walking hand

to the shortness of their long digital flexors and the particular osseoli-

posture. In addition, Tuttle offered detailed observations and support-

gamentous characteristics of their wrist joints, and interpreted their

ing photographs of hand postures in living great ape zoo subjects, and

condition as being functionally related to the habit of brachiation.

summarized what was known about great ape behavior from the field.

In 1943, Washburn and Detwiler issued a call for physical anthro-

Tuttle completed this tour de force with a review of the fossil evidence

pology to move beyond pure descriptive research by embracing the

documenting hand evolution among hominoids and for early human

utility of experimentation and hypothesis testing, a sentiment more

ancestors. Based on his many observations, Tuttle concluded that the

well-known from Washburn’s contribution to the Cold Spring Harbor

ancestors of humans were probably arboreal apes, but without the

symposium on “The Analysis of Primate Evolution with Particular Ref-

extreme specializations for manual suspension seen in gibbons or

erence to the Origin of Man” (Washburn, 1951). Whether in response

orangutans. They also did not pass through a knuckle-walking stage,

to the Washburn and Detwiler (1943) paper, or because interest in

instead utilizing palmigrade hand postures prior to the evolution of

experimental methods was “in the air”, studies testing functional

bipedalism. Tuttle’s suggestion that early human ancestors retained

hypotheses began to appear in AJPA. Among them was a study by

more primitive hand morphology inherited from a Miocene ancestor is

Wolffson (1950) that explored the degree to which scapular shape is

cija, Moya-Sola, a view that is gaining wide acceptance today (e.g., Alme

governed by genetic factors vs. muscle function. Through a series of

& Alba, 2010).

experimental manipulations of infant rats involving detaching, removing

Although perhaps less wide-ranging than Tuttle’s paper, the contri-

or deinnervating scapular muscles, the study demonstrated that while

bution to the “Evolution of Primate Locomotor Systems” issue of AJPA

the basic form of a bone is likely controlled by genetics, the fact that

by Grand (1967) similarly offered a detailed functional examination of

many characteristics were altered in the absence of muscular forces

musculoskeletal anatomy, in this case, the foot and ankle of the slow

confirmed that function also plays a critical role in the determination of

loris (Figure 4). Grand systematically analyzed each joint complex,

bone shape.

describing bony articulations, the attachments, positions and relative

Research on primates related to locomotion continued to be rare

sizes of associated muscles, and ranges of motion exhibited. Like Tuttle

in AJPA in the 1950s and early 1960s. For the occasional papers that

(1967), Grand (1967) drew on observations of living loris subjects to

appeared, the focus was still comparative morphology (e.g., Schultz,

formulate his functional interpretations.

1953), but studies were becoming more hypothesis-driven rather that

The following year Grand offered a similarly comprehensive study

purely descriptive. Whether human ancestors were brachiators or

of the hind limb of the howler monkey (Alouatta caraya). He prefaced

quadrupeds was a current topic of debate, and Tappen (1955) and Zie-

his detailed descriptions of muscular anatomy with an overview of the

gler (1964) both explored ape musculature to shed light on the locomo-

challenges presented by travel through an arboreal environment includ-

tor mode that may have preceded human bipedalism. However, a

ing the discontinuity of supports and the variability in substrate size

major turning point occurred in the March 1967 issue that was devoted

and stability. To meet these challenges, arboreal primates must utilize

to papers stemming from a 1965 Wenner-Gren supported conference

motor skills beyond the limb flexion and extension adequate for terres-

on the “Evolution of Primate Locomotor Systems”. The conference

trial habitats, to include opposition of digits, wrist pronation/supination,

organizer, Warren Kinzey, argued in the issue’s preface that detailed

ankle inversion/eversion, as well as abductory and rotational capabil-

knowledge of evolutionary trends among nonhuman primate taxa as

ities at various limb joints. Grand (1968) noted that since the limbs of

well as for nonprimates such as marsupials and insectivores was essen-

arboreal primates could not take advantage of the columnar arrange-

tial if we were to understand our own origins. The emphasis at the con-

ment of the limb elements of terrestrial mammals, they must heavily

ference was on methods and approaches to studying primate

rely on musculotendinous reinforcement for joint stabilization.

locomotion, and brought together researchers from diverse back-

The tradition of detailed description and functional analysis of

grounds and perspectives. Whether by design or accident, this collec-

nonhuman primate morphology continued in the years following the

tion of papers in large part identified a series of “themes” that define

“Evolution of Primate Locomotor Systems” issue of AJPA. Excellent

the modern study of primate locomotion, and I will return to it repeat-

examples include the paper by Cartmill and Milton (1977), which

edly in the more topical review that follows.

offered a new perspective for the interpretation of distinctive hominoid wrist characteristics by highlighting parallels observed in the wrists of

3 | FUNCTIONAL ANALYSIS OF PRIMATE LOCOMOTOR MORPHOLOGY

cautious climbing lorisines. They suggested that this and the resemblance between apes and lorises in other characteristics of the shoulder and thorax, as well as in tail reduction, implied that these characteristics

The papers by Tuttle (1967) and Grand (1967) in the “Evolution of Pri-

in apes are functionally related to climbing habits rather than brachia-

mate Locomotor Systems” issue of AJPA continued the journal’s tradi-

tion as they were typically interpreted. Another example is the study

tion of detailed anatomical study. Tuttle (1967) presented an in-depth

by Hunt (1991) on the mechanics of chimpanzee positional behavior.

exploration of the functional correlates of knuckle-walking in the hands

Drawing on his field observations of the selective importance of

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Reproduction of figure 1 from Tuttle (1967)—Fresh dissection of Chimpanzee Hand. (a) Adductor pollicis has a tendon (t) which inserts into the ventromedial aspect of the distal phalanx of the thumb. Flexor pollicis brevis (f) and abductor pollicis brevis (a), which insert into the ventrolateral aspect of the proximal phalanx of the thumb, assist adductor pollicis during fine manipulation. Note large size of lumbrical muscles (1). (b) The deep muscles of the palm, the well differentiated heads of adductor pollicis (transverse and oblique), and the first palmar interosseous muscle of the thumb (p)

FIGURE 3

manual suspension and vertical climbing, Hunt evaluated diverse

hand (Cartmill, 1979; Hamrick, 1996, 1997; Lemelin & Schmitt, 1998;

aspects of chimpanzee musculoskeletal anatomy and concluded that

Lewis, 1969, 1972a; Marzke, 1971; O’Connor, 1975; Susman, 1979;

most osseoligamentous specializations of the trunk and forelimb can be

Young & Heard-Booth, 2016), the pelvis, hip and hind limb (Anapol &

related to arm-hanging, while muscular specializations are more closely

Barry, 1996; Anapol & Jungers, 1986; Anemone, 1990; Gebo, 2011;

associated with climbing. Additional examples include the papers on

Hammond, 2014; Hammond, Plavcan, & Ward, 2016; Hammond, John-

foot morphology by Gebo (1985, 1992). Based on an array of myologi-

son, & Higham, 2017; Hamrick, 1998; Lewton, 2015; McHenry & Cor-

cal and skeletal observations of the feet of prosimian primates, he con-

ruccini, 1978; Oxnard, German, Jouffroy, & Lessertisseur, 1981a;

cluded that the I–II adductor grasp of lemurids and indriids is a derived

Oxnard, German, & McArdle, 1981b), the ankle and foot (DeSilva,

characteristic associated with large-bodied vertically clinging and leap-

2010; Gebo, 1987; Goodenberger et al., 2015; Lewis, 1972b; Lisowski,

ing species, whereas the I–V opposable grasp is the primitive grasp

Albrecht, & Oxnard, 1974; Meldrum, Dagosto, & White, 1997; Nowak,

type maintained by most other primates (Gebo, 1985). In his analysis of

Carlson, & Patel, 2010), and the trunk and vertebral column (Curtis,

foot adaptions in apes, Gebo (1992) concluded that plantigrady is asso-

1995; German, 1982; Johnson & Shapiro, 1998; Russo, 2010; Shapiro,

ciated with terrestriality, and both are uniquely shared by African apes

1995).

and humans. On the basis of foot anatomy, he suggested that hominin

In the 1980s, analyses of skeletal elements began to consider

evolution likely passed through a quadrupedal terrestrial phase before

internal and microscopic characteristics in addition to external features

the adoption of bipedality.

(For a more detailed discussion of studies of bone biology and mechan-

These are but a few of the studies of primate functional locomotor

ical properties in the AJPA, see Ruff, this volume.). Noting that cortical

morphology appearing in AJPA in the years following the 1967 Evolu-

bone undergoes remodeling in part in response to mechanical stimuli,

tion of Primate Locomotor Systems issue, and there have been too

Schaffler and Burr (1984) undertook a study to determine whether sec-

many to attempt summarizing them all. Like the studies by Grand

ondary osteon formation at the midshaft of the femur was correlated

(1967) and Tuttle (1967), many offered detailed analyses of specific

with locomotor differences among primates. Rafferty and Ruff (1994)

regions or joint complexes: the shoulder and forelimb (Anapol & Gray,

used radiographs to document internal trabecular structure of the fem-

2003; Chan, 2008; Green, 2013; Green, Sugiura, Seitelman, & Gunz,

oral and humeral heads of a suspensory primate, an arboreal quadru-

2015; Holliday & Friedl, 2013; Kimes, Siegel, & Sadler, 1981; Larson,

ped, and a terrestrial quadruped. They compared trabecular mass and

€ schel & Sellers, 2016; Selby & Lovejoy, 2017; Shea, 1986; 1995; Pu

density to measures of articular surface area and to overall body size.

Squyres & DeLeon, 2015; Swartz, 1990; Turnquist 1983), the wrist and

Fajardo

and

€ller Mu

(2001)

introduced

using

micro-computed

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Burgess et al. (2016) have explored the relationships between limb bone cross-sectional geometry, limb joint posture and ontogeny in vervet monkeys and baboons. Analysis of long bone cross-sectional properties, of joint surface area, and of characteristics of subchondral bone and subarticular trabecular bone continue to be common tools for physical anthropologists interested in identifying functional correlates of locomotor mode in nonhuman primates (e.g., Gebo & Sargis, 1994; Godfrey et al., 1995; Ishida, Yamanaka, & Gunji, 2005; Lieberman, Polk, & Demes, 2004; Ruff, 2002; Ryan & van Rietbergen, 2005; Sarringhaus, MacLatchy, & Mitani, 2016; Shaw & Ryan, 2012) (see also Ruff, this volume). In the 1967 issue of AJPA on “Evolution of Primate Locomotor Systems,” Oxnard (1967) presented an overview of his research with colleagues Ashton, Healy, and others using quantitative methods to explore shape differences among primate scapulae (Figure 5). This series of studies were highly influential in popularizing the use of multivariate morphometric methods to analyze complex shape variation across taxa, and have been applied to a number of different anatomical regions (e.g., Anemone, 1990; Corruccini & Ciochon, 1976, 1978; Lisowski et al., 1974; Manaster, 1979; Oxnard et al. 1981a, 1981b; Steudel, 1981). This methodology offers a means of quantifying and comparing complex shapes to identify commonalities as well as the Reproduction of figure 2 from Grand (1967)—Phantom drawing of the foot (slow loris)

FIGURE 4

basis of differences across taxa. The distribution of taxa within the morphometric “space” is interpreted in regard to whether phylogeny or function best accounts for the observed patterns. If the clustering of

tomography into the comparative analysis of primate trabecular architecture. The higher resolution offered by this imaging technique made it possible to examine a variety of trabecular bone characteristics beyond simply 2D orientations and radiographic density including bone volume fraction, trabecular number, thickness and separation, and the degree of uniformity in trabecular orientation (anisotropic—uniform, isotropic—nonuniform). In a follow-up study, Fajardo, Ryan, and Kap-

taxa largely follows taxonomic groupings then their shared appearance is thought to mainly reflect their shared ancestry. If, however, unrelated taxa that share similarities in locomotor behavior cluster together, and/ or closely related species that display distinctive locomotor profiles occupy separate regions in the morphometric space, then the influence of function is considered to be evident. In recent years, use of 3D landmark data has replaced the 2D caliper measurements of early morpho-

pelman (2002) further explored the accuracy of high-resolution X-ray

metric studies (e.g., Green, 2013; Green et al., 2015; Holliday & Friedl,

CT in quantifying the structural properties of primate trabecular bone.

2013; Squyres & DeLeon, 2015; Young, 2008) and this approach con-

CT scanning has also been used to analyze the apparent density of sub-

tinues to be a valuable tool in quantifying osteological correlates of

chondral bone to gain insight into the loading history of joint surfaces.

locomotor differences among primates.

Focusing on the medial femoral condyle, Polk, Williams, and Peterson (2009) examined the patterns of subchondral bone apparent density in a sample of 28 primate species to explore the relationship between

4 | FIELD RESEARCH RELATED TO PRIMATE LOCOMOTION

body size and joint posture. Nowak et al. (2010) used the distribution of subchondral bone apparent density at the primate calcaneo-cuboid

In the 1967 issue of AJPA on “Evolution of Primate Locomotor Sys-

joint to explore the influence of differences in locomotor mode and

tems,” Ripley (1967) argued that while morphometric research like that

foot posture on joint loading.

summarized by Oxnard (1967) can successfully demonstrate correla-

In addition to determining the number of osteons in a long bone

tions between morphological features and locomotor habits among pri-

cross-section, the shape of that cross-section has also been a topic of

mates, the approach oversimplifies the nature of primate locomotion as

study, such as the paper by Burr, Ruff, and Johnson (1989) comparing

observed in the wild. Ripley (1967) noted that morphologists are typi-

the cross-sectional shape of the humerus to that of the femur in three

cally interested in identifying an animal’s “primary” locomotor pattern

species of macaque. They observed that the structural rigidity of the

as a means of determining the key mechanical stressors that have influ-

femur was a better reflection of locomotor differences than was the

enced the adaptive evolution of an anatomical region within a lineage.

humerus. Demes, Jungers, and Selpien (1991) also observed greater

Primary might be defined as the type of locomotion having high sur-

structural rigidity in the femur than in the humerus among indriid pri-

vival value in critical contexts such as escape from predators, or it can

mates with greater a-p reinforcement of the femur presumably related

refer to the locomotor behavior that is used most often. This has led to

to increased bending strength for leaping behaviors. More recently,

the creation of somewhat artificial locomotor categories often defined

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Reproduction of figure 5 from Oxnard (1967)—Bivariate plot of locomotor discriminant Functions 1 and 2

by extreme types that could be misleading in regard to the behavior of intermediate groups. According to Ripley (1967), actual locomotor behavior among free-ranging primates is a much more diverse and complex phenomenon influenced by details of diet, habitat, ecology and social interactions as well as morphology. She advocated an approach to studying locomotor behavior based on identifying the types of locomotion utilized for the various tasks involved in day-today life (Figure 6). Only once the behavior of individuals of both sexes at all life stages in a variety of circumstances, both routine and urgent, was determined could these behaviors be interpreted within an evolutionary perspective. The utility of one such morphologically defined locomotor category, semibrachiation, was investigated by Mittermeier and Fleagle (1976) by comparing the locomotion and postural habits of two primate species both classified as semibrachiators: the red spider monkey (Ateles geoffroyi) and black and white colobus monkey (Colobus guereza). They observed little to no overlap in actual locomotor behavior in these two species, and concluded that the category was not useful since

Reproduction of figure 12 from Ripley (1967)—Two alternative modes of leaving a tree via peripheral branches are (1) dropping off while suspended by the forelimbs, and (2) walking off a low-lying end of a branch

FIGURE 6

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there is no behavior or set of behaviors that can be identified as semi-

711

undertook a comparative study of locomotion and habitat use among

brachiation, and the diversity of locomotor and postural behaviors dis-

six monkey species living in the Ivory Coast’s Tai Forest. He found that

played by taxa included in this category is much greater than the

if the context of the locomotor behavior was considered, there was

similarities.

less disagreement between the two earlier studies than it appeared.

The strategy of using pairwise comparisons of primate species to

For example, in Surinam, Kibale, and Tai, climbing was more common

investigate morphological correlates of habitat and behavioral differen-

during foraging, and leaping more common during travel, and all of the

ces has proven to be a valuable research tool for studies of primate

monkeys tended to use larger supports during travel than during forag-

locomotion. Grand (1976) compared the terrestrial velocity of a maca-

ing. Like Fleagle and Mittermeier (1980), McGraw (1998) reported that

que and two langur species looking for correlates to morphology as

larger monkeys used the largest supports, but he noted that smaller

well as “psychosocial” context. Fleagle (1977) compared the naturalistic

species displayed a more complicated relationship to small and

behavior of two sympatric leaf-monkey species following the approach

medium-sized supports and were influenced by species-specific travel

recommended by Ripley (1967) of observing their locomotor patterns

and foraging strategies. In general, smaller monkey species faced fewer

during daily activities. Although one species typically moved quadrupe-

limitations in terms of substrate size or forest layer, and were therefore

dally along large diameter supports, the other preferred smaller sup-

able to choose among a more diverse set of locomotor and canopy use

ports and more frequently engaged in leaping and forelimb suspension.

patterns. In addition, comparisons of behavioral profiles among small

Comparison of the muscular anatomy of the two species revealed

branches for large-bodied species are complicated by whether or not

numerous differences related to the specific biomechanical demands of

they possess specializations for manual or tail-assisted suspension.

their contrasting locomotor habits. Rodman (1979) compared the skele-

Hunt (1992) also emphasized the importance of context when doc-

tal anatomy of the primarily arboreal Macaca fascicularis to that of

umenting chimpanzee positional behavior. Based on his observations in

Macaca nemestrina, which frequently travels terrestrially to utilize

the Mahale Mountain and Gombe Stream National parks, he reported

widely dispersed resources. He predicted that M. fascicularis should be

that overall, manual suspension is infrequent among chimpanzees.

built like a powerful climber and leaper, while M. nemestrina should dis-

However, it is commonly used during feeding, particularly among small

play cursorial features. By and large skeletal differences between these

branches. Hunt (1992) argued that when attempting to determine the

two species matched those predictions. Ward and Sussman (1979) sim-

adaptive advantage of morphology, it is essential to consider not only

ilarly compared two sympatric lemur species, one of which preferred

frequency, but the stresses that a postural/locomotor behavior gener-

the lowest levels of the forest and the ground (Lemur catta), and the

ates as well as the distinctiveness of that behavior.

other which used the upper levels of the forest canopy (Eulemur fulvus).

In light of the complex interactions between locomotion and habi-

They observed several differences in hind limb musculoskeletal anat-

tat variables that have been reported, Cannon and Leighton (1994) sug-

omy correlated with these differences in habitat and substrate use.

gest that crossing gaps in the forest canopy can serve as a useful

Fontaine (1990) studied Saimiri boliviensis and A. geoffroyi in the field to

organizing principle. Based on their comparison of the locomotor

determine how well their naturalistic behavior matched predictions

behaviors of long-tailed macaques (M. fascicularis) and agile gibbons

based on locomotor categories, morphometric studies and the conse-

(Hylobates agilis), the frequency with which gaps are encountered per

quences of body size. Although his results were in general agreement

unit distance, the length of continuous pathways, and the availability of

with predictions based on morphological characteristics, there were

easily crossable gaps strongly influenced the choice of forest stratum.

discrepancies, particularly in regard to the frequency of leaping and

They constructed a “Perceived Continuity Index” that correlated well

climbing.

to the strata utilized by macaques and gibbons, suggesting that each

Fleagle and Mittermeier (1980) undertook comparisons of seven

species travels in forest layers that offer it the greatest travel effi-

Surinam monkey species to explore how body size, diet, and ecological

ciency. For gibbons, their ability to brachiate and leap allowed them to

parameters such as forest stratification and forest type are related to

cross larger gaps than could macaques, which was reflected in their

locomotor behavior. They reported that larger species tended to climb

preference for the emergent canopy layer and higher strata than used

more and use larger supports, and that leaping is frequent among

by the macaques.

smaller taxa and when utilizing the forest understory. However, they

Evolutionary conclusions based on correlations between morphol-

found that diet did not display any consistent associations with either

ogy, locomotor behaviors and forest architectural preferences depend

locomotor behavior or forest utilization.

on the consistency of these relationships. To determine whether sub-

To further explore these issues, Gebo and Chapman (1995b) stud-

strate selection is simply a matter of availability or is instead a reflec-

ied the relationships between body size, forest structure and locomo-

tion of a functional relationship, McGraw (1996) compared the

tion in five cercopithecid monkey species in Uganda’s Kibale Forest. In

locomotor behavior of five cercopithecids in two structurally distinct

contrast to the results of Fleagle and Mittermeier (1980), Gebo and

forest areas of the Tai Forest of the Ivory Coast. He observed that the

Chapman (1995b) reported that smaller species climbed more and

locomotor profiles of the five monkey species were remarkably consist-

leaped less than larger ones, most leaping occurred in mid- to upper

ent despite differences in the structural properties of the two habitats.

canopy strata rather than the understory, and there was no consistent

By and large the monkeys displayed similar frequencies of different

relationship between body size and sizes of utilized supports. In order

locomotor modes and consistent support type use independent of their

to try and reconcile some of these conflicting results, McGraw (1998)

relative abundance in the two forest types. The fact that each monkey

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species uses a specific subset of support types despite the fact that they are all capable of using all kinds of supports suggested to McGraw (1996) that primate locomotor behavior is highly conservative and that some underlying set of factors operates to limit or in some way determine that behavior. Isbell, Pruetz, Lewis, and Young (1998) compared the locomotor activities of patas monkeys (Erythrocebus patas) and vervet monkeys (Cholorcebus aethiops) to test hypothesized selective advantages of long limbs that have been proposed to explain the elongation of lower limb length in Homo erectus. They compared home range size, travel distances, and the context of different locomotor modes including in response to predator threats. They concluded that the long limbs and correlated long strides of patas monkeys are related to increased foraging efficiency to exploit widely distributed food resources. Although these features may also increase speed, high speed running was less important than walking efficiency, and they suggested that similar considerations could explain lower limb elongation in H. erectus. The comparative studies summarized earlier are of course only a subset of primate field research that has appeared in the pages of AJPA following Ripley’s call for careful documentation of the spectrum of locomotor behaviors of a taxon related to its natural habitat and ecology. Due to their close relationship to humans, the great apes have been a frequent focus of study (e.g., Cant, 1992; Doran, 1992, 1993a, 1993b; Manduell, Morrogh-Bernard, & Thorpe, 2011; Remis, 1995; Stanford, 2006; Susman, Badrian, & Badrian, 1980; Thorpe & Cromp-

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5.1 | Electromyography Tuttle teamed up with the human electromyographer Basmajian to undertake a series of studies on muscle recruitment patterns among great apes. The focus of their first study was the activity of the forearm muscles of a gorilla during knuckle-walking (Tuttle, Basmajian, Regenos, & Shine, 1972). They were surprised by the relative inactivity of many of the muscles such as flexor digitorum profundus, and concluded that close-packed positioning mechanisms may be mainly responsible for stability of the gorilla’s wrist and metacarpophalangeal joints. Tuttle and Basmajian (1974) next studied the brachial muscles of the gorilla, and their most surprising result was again the absence of activity, in this case, of all of the brachial muscles during manual suspension by the gorilla. In a follow-up study, Tuttle, Velte, and Basmajian (1983) reported similar patterns of brachial muscle recruitment in chimpanzees and orangutans. Tuttle and Basmajian (1978a) next turned their attention to the recruitment patterns of the shoulder muscles of chimpanzees, orangutans and gorillas. During arm-raising behaviors, they observed EMG activity in the deltoid, rhomboids and members of the rotator cuff that were generally consistent with those reported for humans. Contrary to predictions based on morphology (e.g., Roberts, 1974), these shoulder muscles were inactive during pendant suspension, leading Tuttle and Basmajian (1978a) to conclude that like the wrist and elbow, joint integrity of the great ape shoulder was maintained mainly by osseoligamentous mechanisms. This led them to suggest that detailed examina-

ton, 2005, 2006; Videan & McGrew, 2002). Investigations of New

tion of the bony, tendinous, and ligamentous components of ape

World monkey locomotor behavior include Bezanson (2009), Menzel

shoulder joints could provide new clues regarding their suspensory

€n Ybarra (1984), and Walker and Ayres (1996), that of Old (1986), Scho

adaptations. In a companion paper, Tuttle and Basmajian (1978b)

World monkeys include Bitty and McGraw (2007), Cant (1988), Dun-

reported on the activity patterns of great ape shoulder muscles during

ham, Kane, and McGraw (2017), Gebo and Chapman (1995a), Rose

quadrupedal postures and locomotion. They reported that quiet quad-

(1976), and Workman and Covert (2005), and that of prosimians

rupedal standing elicited minimal muscular activity, while quadrupedal

include Blanchard, Furnell, Sellers, & Crompton (2015), Dagosto (1994),

walking elicited modest to high levels of activity. Tuttle and Basmajian

Dykyj (1980), and Warren and Crompton (1997).

(1978b) concluded that overall there were few major differences in the muscle recruitment patterns of the three great ape species, despite differences in hand postures (knuckle-walking in the African apes vs. fistwalking in the orangutan), nor did the suspensory adaptations evident in their shoulder complexes appear to compromise their abilities to

5 | EXPERIMENTAL METHODS FOR STUDYING PRIMATE LOCOMOTION

engage in quadrupedal behaviors with only moderate muscular effort. To explore the functional interpretation of prominent markings for the insertions of flexor digitorum profundus and flexor digitorum

Although none of the papers included in the 1967 issue of AJPA on

superficialis in the hand of fossils hominins, Susman and Stern (1979)

“Evolution of Primate Locomotor Systems” concerned the application

investigated the EMG activity of these two muscles in chimpanzees.

of experimental approaches to the study of primate locomotion, in his

They reported that the two digital flexors are largely inactive during

preface Kinsey noted the importance of developing methodologies

quadrupedal postures or the support phase of quadrupedal walking,

whereby techniques such as electromyography (a means of document-

but displayed maximum activity during manual suspension. Susman and

ing muscle activation patterns) or cineradiography (the combination of

Stern (1979) concluded that the prominent insertions for these digital

cinephotography and radiography for motion analysis) could be utilized

flexors observed in the O.H. 7 hand suggested the importance of arbo-

to enhance our understanding of primate locomotion, a sentiment ech-

real behaviors in the fossil hominin.

oed by conference participants Prost, Snyder, and Tuttle. In the 1970s

Stern, Wells, Jungers, and Vangor (1980b) examined the EMG

such papers began to appear in the pages of AJPA and have become

activity patterns of caudal serratus anterior during posture and locomo-

almost as frequent as more descriptive studies of primate locomotor

tion in Ateles, Lagothrix, and Alouatta. Since Ateles displays similar modi-

morphology.

fications in the muscle’s size and configuration as are seen apes

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713

including the cranio-caudal orientation of the lowest digitiations, this

Although the general consensus was that the dorsal position of the

comparison offered the opportunity to investigate the functional impli-

scapula and lateral orientation of the glenoid fossa necessitated a high

cations of these specializations. Contrary to the inactivity in caudal ser-

degree of humeral torsion in apes (and humans), Larson (1988) noted

ratus anterior during arm-raising behaviors in great apes reported by

that torsion in gibbons was actually quite modest. She concluded that

Tuttle and Basmajian (1977), Stern, Wells, Jungers, Vangor, and Fleagle

gibbons tolerated the resulting lateral set to their elbows in order to

(1980b) observed significant activity during arm-raising in most of cau-

take advantage of the extreme lateral rotation of the elbow joint it con-

dal serratus anterior, except for the most extreme caudal bundles. The

ferred during arm-swinging.

latter instead were used to aid in transmitting the weight of the trunk to

In addition to those summarized earlier, other EMG studies of pri-

the supporting forelimb during suspensory postures and locomotion. In a

mate muscle function appearing in AJPA include the studies by Tuttle,

follow-up study, Larson, Stern, and Jungers (1991) re-examined the

Basmajian, and Ishida (1979) on the EMG activity of great ape thigh

activity of caudal serratus anterior as well as trapezius in chimpanzees.

muscles during bipedal standing and walking; Stern et al. (1980a), who

They reported similar functional differentiation within caudal serratus

used EMG to investigate to evolution of a clavicular head of the pec-

anterior as observed by Stern et al. (1980b) for spider monkeys. How-

toralis major muscle, which is infrequent in primates; Shapiro and

ever, they confirmed the report by Tuttle and Basmajian (1977) of inac-

Jungers (1988, 1994), who explored how the evolution of erect posture

tivity in cranial trapezius during arm-raising, suggesting instead that its

and locomotion might have necessitated changes in deep back muscle

recruitment was more closely related to head position.

function; Larson and Stern (1989, 1992) on the relationship between

In one of perhaps the most influential EMG studies to date, Stern

supraspinatus recruitment during quadrupedal locomotion and size and

and Susman (1981) studied the recruitment of the gluteal muscles in

projection of the humeral greater tubercle; Kumakura (1989), who

Hylobates, Pongo, and Pan with an eye to understanding the evolution-

compared the morphology and activity patterns of biceps femoris in

ary changes of the hominin pelvis associated with bipedalism. In mod-

four different primate species during a variety of locomotor behaviors;

ern humans, the iliac blades approach a sagittal orientation and the

Larson and Stern (2006), Stern and Larson (2001), and Tuttle, Hol-

lesser gluteals (gluteus medius and minimus) are hip abductors enabling

lowed, and Basmajian (1992), all of whom explored the complex

them to control side-to-side balance of the pelvis by resisting hip

recruitment patterns of forearm pronators and supinators during loco-

adduction during single limb support of bipedal walking. In apes and

motion in apes and monkeys; Larson and Stern (2009) on the contribu-

monkeys, however, the iliac blades face dorsally and the lesser gluteal

tion of hip extensor muscle force to fore-/hind limb weight support

muscles were assumed to act as hip extensors. This implied that the

asymmetry in primate quadrupeds; and Patel, Larson, and Stern (2015),

functional role of the lesser gluteals had to change in the course of

who confirmed that peroneal process size is not indicative of a contri-

early human evolution. Based on its pattern of recruitment in a variety

bution of peroneus longus to hallucal grasping.

of behaviors, Stern and Susman (1981) deduced that gluteus medius is not primarily a thigh extensor in apes, but rather is a medial rotator of

5.2 | Motion analysis

the hip in orthograde postures when the hip is slightly flexed. During bipedality, this action allowed it to provide side-to-side balance of the

Documenting the movement profiles of limb elements (aka kinematics

trunk at the hip, thus performing the same functional role as in humans.

or motion analysis) is a central component in the study of primate loco-

The transition to habitual bipedalism with a more extended thigh in

motor mechanics. Since many aspects occur too quickly to be followed

human evolution could then be viewed as mainly involving osteological

by the human eye, studies of locomotor movements depend on use of

changes in the iliac blades, altering the line of action of the lesser glu-

motion pictures, initially recorded on film (e.g., Hurov, 1985; Prost,

teals, but preserving their functional contribution to gait.

1965; Vilensky, 1980, 1983), but quickly replaced by videotape record-

Although Tuttle and Basmajian (1978a) had reported similar pro-

ings, and most recently by digital video. Rosenberger and Stafford

files of recruitment for all members of the rotator cuff in apes during

(1994) compared locomotor profile data collected by direct observation

arm-raising and pendant suspension, Larson and Stern (1986) observed

to that obtained from video analysis in their study on the locomotion

more individualistic activity patterns for each of the four muscles in the

of captive Leontopithecus and Callimico. They reported being able to

chimpanzee, with subscapularis displaying the most distinctive recruit-

record more bouts from the video than through direct visual scanning,

ment pattern. Larson (1988) compared the activity profile of subscapu-

in part due to the need to stop and enter data for the latter. The video

laris in gibbons to that of chimpanzees to determine whether the

also made it possible to identify subtleties of locomotion behavior not

distinctive recruitment pattern observed in the latter was common to

detectable by the human eye.

all apes. As had been reported for chimpanzees (Larson & Stern, 1986),

Lemelin and Schmitt (1998) explored hand positioning on arboreal

the maximum levels of EMG activity in the gibbon occurred during the

supports of a large and diverse sample of primate quadrupeds by vid-

support phase of vertical climbing. However, unlike the chimpanzee,

eotaping subjects in zoos, research centers as well as in a lab setting.

the gibbon displayed subscapularis activity during the support phase of

Morphological studies had suggested that primates with ectaxonic

arm-swinging and it was more active during free arm motions (Larson,

hands (longer fourth ray, found in most strepsirhines) should use more

1988). Larson (1988) related the observed differences in subscapularis

oblique hand positions on an arboreal support, while those with mesax-

recruitment to greater demands for medial rotatory force at the

onic hand (longer third ray, found in most haplorhines) should use more

shoulder in gibbons due to their low degree of humeral torsion.

neutral hand positions. However, hand positioning was quite variable,

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and many primates were able to adopt both neutral and deviated hand

primates can increase running speed. Patel (2009) showed that digiti-

positions regardless of their hand type. Lemelin and Schmitt (1998)

grady did indeed increase effective forelimb length, but contrary to pre-

concluded that primates adjust their hand posture to accommodate the

dictions, he observed that his subjects used more palmigrade hand

substrate and are not strongly constrained by morphology. Larson,

postures at faster speeds. In agreement with the field study by Isbell

Schmitt, Lemelin, and Hamrick (2000) and Larney and Larson (2004)

et al. (1998), Patel (2009) concluded that longer effective limb length

also took advantage of the portability of videotape recording to docu-

associated with digitigrade hand posture in terrestrial primates was

ment aspects of forelimb posture in diverse samples of primates and

more likely associated with foraging efficiency and longer day ranges

nonprimates in zoos, research centers and lab settings.

that speed of locomotion (see also Patel, 2010).

Tardieu, Aurengo, and Tardieu (1993) offered one of the first

Cineradiography refers to a method of film or video recording of

attempts to document the 3D motions of a primate. The subjects of

animal motion that substitutes an X-ray source for the light source of a

the study (an adult woman, 12-year-old girl, 9-year-old boy, and 6-

movie camera. Jenkins, Dombrowski, and Gordon (1978) pioneered its

year-old female chimpanzee) wore a single-piece dance suit marked

use in studies of primate locomotion documenting shoulder motion in

with points corresponding to the nodes of a volumetric 3D finite-

brachiating spider monkeys. They reported that in contrast to the cau-

element model to be used to represent the quantified body motion.

dal and ventral motion of the scapula during a stride of a quadrupedal

The subject’s motion was recorded by four synchronized movie cam-

monkey, the excursion of the scapula is reversed in brachiators to

eras, and Cartesian coordinates of the points on the body suits were

move more dorsally during support phase. This motion brings the

hand digitized on each set of the four synchronized images to inform

shoulder joint closer to the median plane thus positioning the body

the model. Tardieu et al. (1993) reported that human bipedal gait was

center of gravity under the supporting hand. Dorsal scapular motion is

characterized by synchronized transverse and vertical displacements of

facilitated by the increased thoracic breadth of brachiators, and by

the body center of mass. The bipedal gait of the chimpanzee was char-

alterations in the length and shape of the clavicle. Schmidt and Fischer

acterized by modest center of mass motion but without any simple pat-

(2000) also used cineradiography to study shoulder and forelimb

tern of periodic movement, and was accompanied by large limb

motion but in a quadrupedal walking brown lemur (E. fulvus). In contrast

motions apparently to continuously adjust balance.

to the assumed parasagittal planar motion of the scapula of a quadru-

^t Aerts, Van Damme, Van Elsacker, and Duchene (2000) and D’Aou

ped, they reported an unexpected degree of scapular mobility in the

Aerts, De Clercq, De Meester, and Van Elsacker (2002) have helped

brown lemur including ante-/retroversion, adduction/abduction, and

address a paucity of data on the locomotion of bonobos by forging a

rotation around its long axis. They noted that the motion referred to as

working relationship with Wild Animal Park of Planckendael, Belgium.

shoulder abduction did not occur at the shoulder joint as in apes or

Aerts et al. (2000) documented spatio-temporal variables during bipedal

humans, but rather was produced by internal rotation of the scapula

and quadrupedal walking and reported that despite differences in body

around its long axis coupled with flexion at the shoulder joint. Schmidt

proportions and the distributions of mass between bonobos, chimpan-

and Fischer (2000) suggested that this method of achieving humeral

zees and humans, overall the dynamics of their oscillating legs were

abduction was probably typical of small mammals. In order to explore

^t et al. (2002) recorded hind limb segsimilar in the three species. D’Aou

the contributions of individual tarsal joints to the “midtarsal break”,

ment and joint angles of bipedal and quadrupedal walking bonobos and

Thompson, Holowka, O’Neill, and Larson (2014) employed cineradiog-

noted high levels of variability in bonobos compared with humans.

raphy to document tarsal motion in chimpanzee feet during passive

Although the hip is more flexed during quadrupedal walking, they

manipulation. They reported that the talonavicular joint exhibited a

observed general similarities in limb angle profiles for bonobo bipedal-

larger range of motion that the calcaneocuboid joint, indicating that the

ism and quadrupedalism, which in turn were similar to those reported

medial side of the transverse tarsal joint contributes more to midfoot

for chimpanzees. Comparisons to humans indicated similar hip–knee coordination, but distinctive knee–ankle coordination in bonobos. Incorporation of 3D motion capture computer software and digital

mobility in chimpanzees. In addition, they note that the transverse tarsal joint undergoes considerable frontal plane (inversion/eversion) rotation.

video recording has greatly facilitated our ability to document the complex limb motions of primate subjects. Isler (2005) used these methods to compare the 3D limb joint motions of zoo-housed gorillas, bonobos,

5.3 | Substrate reaction forces, energetics

orangutans, and gibbons during vertical climbing. She observed that

Studies of limb postures and motions during locomotion often also

gibbons displayed greater agility, utilized larger ranges of motion at the

include force plate recordings to collect kinetic data on the substrate

shoulder and elbow, and horizontally abducted their upper arm more

reaction forces (SRFs) generated by those movements. Demes and

than the great apes. The climbing movements of the gorilla and bonobo

Carlson (2009) used this combination to explore the degree of align-

were roughly similar, while the orangutan used larger ranges of joint

ment between SRF vectors and distal limb segments in capuchin mon-

motion and longer stride lengths than the African apes. Patel (2009)

keys (Cebus apella) during arboreal and terrestrial walking, and while

used 3D motion capture to explore the functional significance of digiti-

turning. Good alignment between the SRF and the forearm or leg loads

grade hand posture in three cercopithecine monkey species. Since digi-

the limb in axial compression, whereas nonalignment will cause bending

tigrady increases the effective length of the limb, this hand posture has

moments and higher peak stresses. They reported that the SRF is rarely

long been assumed to be a means by which terrestrial/semiterrestrial

well-aligned with the leg and forearm and is quite variable when

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715

walking on arboreal supports. They concluded that arboreal locomotion

reported that leaping generates exceptionally high peak forces, with

subjects the limbs to frequent unpredictable bending stresses.

higher take-off forces due to the fact that some of the impulse gener-

Schmidt (2005) combined cineradiographic motion analysis with

ated deforms the compliant substrate requiring greater effort to

SRF recordings to investigate the limb kinematics and kinetics of squir-

achieve the leap. During landing, however, substrate compliance damp-

rel monkeys. The ability to visualize scapular motion allowed her to

ens landing forces. The fact that their results differed from those col-

estimate the contribution of each forelimb segment to stance length.

lected with rigidly mounted force plates highlighted the importance of

She reported that scapular retraction contributes to over half of stance

creating as realistic as possible simulated substrates for lab-based loco-

length, while humeral retraction contributes a little over a third, with

motor research.

successively less motion contributed by each remaining segment. As

In order to compare the climbing biomechanics a spider monkey to

she observed in the brown lemur, the motion of the scapula is not

that of a Japanese macaque, Hirasaki, Kumakura, and Matano (2000)

strictly parasagittal, but rather follows the contour of the thorax. Like

undertook an inverse dynamics analysis using kinetic data collected

other quadrupedal primates, the squirrel monkeys displayed higher

from a specially designed instrumented climbing pole combined with

peak SRF on their hind limbs than on their forelimbs, and Schmidt

kinematic and morphological data. They reported that the spider mon-

(2005) noted that maximum forces on the hind limb coincided with the

key relies more on its hind limb for propulsive force and mainly uses its

moment of forelimb touchdown, thus reducing compressive loads on

forelimb to keep its body close to the substrate. The macaques, on the

the forelimb joints when it is most extended.

other hand, displayed less differentiation in fore-/hind limb function

Demes, Franz, and Carlson (2005) used force plates to determine

using both for propulsion.

the magnitude of SRF during jumping in L. catta and E. fulvus that

Chang, Bertram, and Lee (2000) and Usherwood, Larson, and Ber-

unlike standing leaps, involve a run up before and a run out afterward.

tram (2003) used overhead mounted instrumented handholds to gather

Vertical forces and impulses were large during take-off and landing but

data on SRF during brachiation in a gibbon. Studying slow speed con-

not substantially different from those observed during quadrupedal

tinuous contact brachiation, Chang et al. (2000) reported that the gait

gaits, in contrast to the very high SRF characteristic of specialized verti-

was in many ways analogous to bipedal walking in permitting

€ nther, D’Aou ^ t, and cal clingers and leapers. Channon, Crompton, Gu

pendulum-like exchange of potential and kinetic energy. SRF at the

Vereecke (2010) investigated SRF and leaping mechanics in gibbons

hand resembled ground reaction forces during human bipedalism

highlighting the importance of their hind limbs to their overall locomo-

except for the reversal of the order of horizontal braking and propul-

tor repertoire despite the dominance of manual suspensory

sive forces. Usherwood et al. (2003) focused on higher speed gait

locomotion.

known as “ricochetal brachiation” that is characterized by a ballistic

Demes and colleagues utilized SRF data to analyze the center of

flight phase. They reported that by changing the timing of hand release

mass mechanics in bipedal capuchin monkeys (Demes & O’Neill, 2013)

gibbons are able to alter their net horizontal impulse. Rotation at the

and bipedal chimpanzees (Demes et al., 2015), both of which walk with

shoulder to alter trunk orientation in addition to the swing beneath the

bent-hip, bent-knee gaits. They reported that the bipedalism of the

hand produces a whip-like double pendulum incorporating rotational

capuchins was a “grounded run” and not governed by the pendulum

kinetic energy. Additional mechanisms for controlling the energy of

mechanics that are characteristic of human walking. In contrast, the

brachiation include lifting or dropping the legs and elbow flexion. Other

center of mass of the chimpanzee did oscillate allowing some energy

studies of brachiation mechanics include Bertram and Chang (2001),

recovery through the exchange of kinetic and potential energy as

^ t, and Aerts (2011), and Oka, Hirasaki, Hirokawa, Michilsens, D’Aou

humans do, but the amount of recovery was less and more variable.

Nakano, and Kumakura, (2010).

Importantly, the oscillating chimpanzee center of mass did not match

Functional interpretation of many characteristics of bone such as

the flat center of mass trajectory reported for humans walking with

cross-sectional properties are based on assumptions about patterns of

bent hips and knees, which has been used to attempt to model early

limb loading, and a common goal of kinematic and kinetic data collec-

hominin bipedal locomotion. Demes et al. (2015) concluded that

tion in locomotion studies is to be able to make predictions about these

humans walking with flexed lower limbs have limited utility for testing

loading patterns. Demes et al. (1998, 2001) undertook analyses of

hypotheses about early hominin gait.

bone strain distributions in the ulna and tibia of macaques to determine

Collection of SRF data in the studies cited earlier involved the

how well these predictions align with apparent limb loading. In both

research subjects moving over the force plates, either directly as in ter-

cases, the measured distributions of bone strain indicated that bending

restrial travel, or on horizontal poles attached to the plate to simulate

was the predominant loading regime but not in the planes displaying

arboreal locomotion. However, a few studies have been undertaken to

maximum reinforcement. Although their study subjects were sheep,

document the forces generated during nonhorizontal locomotion.

the strain gauge study by Lieberman et al. (2004) also called into ques-

Demes, Jungers, Gross, and Fleagle (1995) constructed an instru-

tion some of the conventional wisdom regarding the interpretation of

mented vertical force pole to explore take-off and landing forces during

primate long bone cross-sectional geometry. In response to these and

vertical leaping by Propithecus and Hapalemur. Their observations of

other issues that have been raised regarding the functional interpreta-

leaping behavior in the field indicated that tree sway was a frequent

tion of bone morphology, Ruff, Holt, and Trinkaus (2006) argued that

component of leaping dynamics, and they therefore incorporated a

bone strain data collected in a lab setting can only approximate the

level of compliance in the design of the force pole. Demes et al. (1995)

diverse strain environment likely experienced by any bone in the

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Reproduction of figure 5 from Hildebrand (1967)—Sketches of Pan (top) and Pongo (bottom) showing slight asymmetry (contrast length of step by arms on right and left), the passage of both hind feet to the same side of the respective hands, and differences in the manner of placing the hands on the ground

FIGURE 7

course of an animal’s spectrum of behaviors. They concluded that as

were small as many have suggested, this similarity in costs of horizontal

long as the multitude of factors influencing bone morphology are con-

and vertical locomotion would have facilitated their successful occupa-

sidered, traditional analytical methods of characterizing cross-sectional

tion of the small branch arboreal niche.

properties still offer the best insight in interpreting bone functional adaptation (see Ruff, this volume for further discussion of these issues). Recording the pressure distribution on the hands and/or feet is a

6 | DISTINCTIVE ASPECTS OF PRIMATE QUADRUPEDALISM

relatively new approach to assessing force generation during locomotion. Plantar pressures during bipedal and quadrupedal walking were

Putting aside for the moment some of the truly unique locomotor

^t, De Clercq, Van Elsacker, compared for bonobos by Vereecke, D’Aou

modes observed in primates like leaping between vertical supports or

and Aerts (2003), and for Japanese macaques by Hirasaki, Higurashi,

arm-swinging, even the form of quadrupedal walking and running

and Kumakura (2010). Wunderlich and Jungers (2009) analyzed manual

exhibited by most primates is distinctive from that typically displayed

digital pressure among young and older chimpanzees walking both on

by other mammals. In fact, the very first paper in the 1967 “Evolution

^ t, the ground and on simulated arboreal substrates. Vereecke, D’Aou

of Primate Locomotor Systems” issue of AJPA was by Hildebrand

Van Elsacker, De Clercq, and Aerts (2006) combined plantar pressure

(1967) on primate quadrupedal gait. The paper offered a systematic

recordings with collection of SRF in their functional analysis of the gib-

overview of the gaits exhibited by each family of nonhuman primate as

bon foot during terrestrial bipedal walking.

well as for Tupaiidae, then thought to approximate the primate ances-

Studies of primate locomotion often allude to the possible advan-

tral condition. He noted that nearly all primate quadrupeds display a

tages of particular characteristics in terms of greater efficiency or in

preference for diagonal-sequence, diagonal-couplets walks (left hind,

reduction of locomotor costs. Measurement of the rate of oxygen con-

right fore, right hind, left fore, with the diagonal pair moving together),

sumption during locomotion offers a means to determine the actual

a gait pattern that is rare among nonprimates. At the same time, Hilde-

energetic costs entailed by that activity. O’Neill (2012) investigated the

brand (1967) emphasized the high levels of variability in primate gait

metabolic costs of walking, cantering and galloping in ring-tailed lemurs

characteristics (see also Prost, 1965, 1969). Although gait variability

(L. catta), and reported that the lemurs have relatively low costs com-

was easy to relate to the need for versatility in discontinuous arboreal

pared with predictions based on scaling trends for terrestrial birds and

habitats, the almost unique preference for diagonal-sequence, diago-

mammals, suggesting that their locomotion is relatively economical. He

nal-couplets walks was more difficult to explain. Moving diagonal pairs

also noted that their gait choice corresponds to locomotor cost minima.

of limbs in sequence means that a foot will touch down while the hand

Hanna and Schmitt (2011) compared the energetic costs of climbing to

on the same side is still in contact with the substrate, and with their

that of horizontal locomotion in five species of primates. They reported

long limbs, primate quadrupeds often have to “over-stride”, that is, pass

that the energetic costs of climbing and horizontal locomotion were

their foot to one side or the other of the ipsilateral hand to touch

similar for small primates, but climbing was much more energy costly

down beside or ahead of it (Figure 7). This potential for limb interfer-

for larger-bodied species. They suggested that if the earliest primates

ence coupled with the fact that diagonal-sequence, diagonal-couplets

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717

walks did not offer any obvious biomechanical advantage over the

distinctive nature of primate forelimb posture was most directly related

more commonly observed lateral sequence walks of nonprimates,

to reaching out with clawless grasping hands to gain a secure grip on a

made their preference among primate quadrupeds something of a mys-

particular support in a small-branch environment. This also necessitated

tery. Thus, how the form of quadrupedal locomotion displayed by non-

nonstereotypical forelimb motions, which in turn required flexibility in

human primates is similar to or different from that of other mammals

neural control of motion and perhaps the higher level of supraspinal

has become a topic of much research.

input that Vilensky and Patrick (1985) alluded to. More precise control

To better place primate quadrupedalism into context, Vilensky

of forelimb positioning would lead to the ability to use the forelimb in

undertook several studies in the 1980s and 1990s of primate quadru-

more versatile ways for foraging and manipulation and concomitant

pedal behavior applying analytical methods developed for nonprimates.

increases in ranges of motion at the forelimb joints. The resulting

Heglund, Taylor, and McMahon (1974) had demonstrated that parame-

reduced stability at those joints could only be tolerated if mechanisms

ters such as stride rate, stride length, and speed at the trot-gallop tran-

were developed to attenuate disruptive forces to the forelimb gener-

sition could be predicted from body size in a variety of quadrupedal

ated by locomotion. Larson et al. (2000) suggested that this need to

mammals. Vilensky (1980) tested the utility of those predictions for M.

spare the forelimb might explain other distinctive characteristics of pri-

mulatta and observed that their stride length was almost double the

mate quadrupedal locomotion such as the observation that peak verti-

predicted value, while stride rate was almost half that of the nonpri-

cal SRFs in primates are higher on their hind limbs than their forelimbs,

mates studied by Heglund et al. (1974). In addition, he reported that

in contrast to the nearly universal opposite pattern in nonprimates

the macaques didn’t actually use a running trot like other quadrupeds,

(Carlson & Demes, 2010; Demes et al., 1994; Hanna, Polk, & Schmitt,

instead transitioning from a fast walk to a gallop. In a later study, Vilen-

2006; Kimura, 1985; Kimura, Okada, & Ishida, 1979; Reynolds, 1985b;

sky observed that macaques do not display symmetry in timing of fore-

Schmidt, 2005).

and hind limb motion characteristics, which he related to the greater

Although higher hind than fore-peak SRF was initially attributed to

role that the hind limb plays in support and propulsion in primates

a more posteriorly positioned center of mass in primates, there is little

(Vilensky, 1983). Noting that neither the distinctive use of diagonal

evidence supporting this explanation (Vilensky, 1979; Wells & DeMen-

sequence gaits nor the absence of a running trot in primates had ready

thon, 1987). How exactly primates accomplish this asymmetry has

explanations in terms of physical characteristics or locomotor mechan-

been a matter of some debate. Theoretically, if an animal walks in such

ics, Vilensky and Patrick (1985) drew attention to the fact that unlike

a way that their fore- and/or hind limbs oscillate around a protracted

most mammals, stepping movements cannot be elicited following spinal

average limb angle, more weight would be distributed to their hind

transection in primates (Eidelberg, Walden, & Nguyen, 1981), and sug-

limbs than their forelimbs (Reynolds, 1985a). The fact that primates

gested that motor control in primates may require more supraspinal

begin a step with protracted limbs raises the possibility that this could

input than other animals.

contribute to higher hind limb weight support in primates. Larson and

Vilensky and Gankiewicz (1990) documented the angular displace-

Stern (2009) explored this possibility by comparing average limb angles

ments of the forelimb joints in vervet monkeys (Chlorocebus aethiops)

across a broad sample of primate and nonprimate quadrupeds, but

across different speeds, but noted a paucity of comparative data with

found that primate forelimbs oscillate about a nearly vertical axis, and

which to evaluate the patterns they observed. In part to address this

while the average hind limb angle is protracted, the deviation from ver-

limitation, Larson et al. (2000) undertook a broad study of forelimb pos-

tical is likely too small to have a major impact on weight distribution in

ture across a large sample of quadrupedal primates and nonprimates.

most primates. However, the large-bodied great apes may be an excep-

They reported that primates begin a step with a uniquely protracted

tion in taking advantage of protracted average hind limb angles to dis-

humerus compared with the either vertical or retracted initial humeral

tribute more weight to their hind limbs (see Raichlen, Pontzer, Shapiro,

posture in nonprimates. Primates also utilize larger humeral and overall

& Sockol, 2009; Larson and Demes, 2011).

forelimb angular excursions than nonprimates. They noted that the

Reynolds (1985a) suggested that primates can reduce the percent-

resulting greater alignment of the scapula and humerus increases effec-

age of body weight supported by their forelimbs by actively shifting

tive limb length, augmenting the relatively long limb bone lengths that

weight onto their hind limbs using muscular effort. He noted that the

have been reported for primates (Alexander et al., 1979). The combina-

force of an extrinsic limb muscle will both alter the SRF at the foot and

tion of long limbs and large limb excursions accounted for the relatively

how the trunk balances on the limb. Since the effect of a limb retractor

long stride lengths that had been documented by Vilensky (1980) and

will be to shift weight onto the hind limb, he proposed that by recruit-

others (Alexander & Maloiy, 1984; Reynolds, 1987). One advantage of

ing their hind limb retractors during the early part of support phase of

long strides could be as a way of maintaining speed while keeping

a step, quadrupedal primates could increase the proportion of weight

stride rates low thus avoiding a “bouncy” running gait (such as a run-

borne by their hind limbs without unduly increasing the propulsive

ning trot) that could cause dangerous and energy costly branch sway

force applied to the foot. Larson and Stern (2009) examined the activity

(Demes, Jungers, & Nieschalk, 1990). Larson et al. (2000) noted that

patterns of potential hind limb retractors (hip extensors) in nine species

unlike other mammals with elongated limbs, primates have maintained

of primates to test Reynolds’ proposal. The long head of biceps femoris

grasping hands and feet, which has been related to travel and foraging

was active during the first half of support phase in all species, poten-

in a small-branch setting (Cartmill, 1972, 1974; Garber, 1980; Hamrick,

tially contributing to active weight shift onto the hind limb. In addition,

1998; Rasmussen, 1990; Sussman, 1991). They suggested that the

the species that display the most marked fore/hind limb weight support

718

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LARSON

asymmetry displayed more intensive hip extensor recruitment with

primate infants to test a proposal by Cartmill, Lemelin, and Schmitt

more muscles active and at higher amplitudes.

(2002) that use of a diagonal sequence/diagonal couplet gait was

Schmitt (1998, 1999) has noted that beginning a step with a highly

related to the position of the hind limb at the moment of contralateral

protracted forelimb and allowing it to pass through a large angular

forelimb touchdown. They reported that the ability to position the hind

excursion increases step length and contact time, which when coupled

limb more nearly under the body’s center of mass at forelimb touch-

with substantial elbow yield, are the main components of a compliant

down was not due to gait choice as Cartmill et al. (2002) contended,

gait. Limb compliance not only lowers the body center of mass and

but more a reflection of the angular excursion of the hind limb in pri-

reduces its vertical oscillations, all of which improve stability on narrow

mates. Infant baboons could achieve this posture using either diagonal

supports, it also reduces peak stresses acting on the limb by increasing

sequence/diagonal couplet gaits or lateral sequence/lateral couple

the time over which they develop. Thus, greater compliance in the

gaits. In a reply to Shapiro and Raichlen (2005), Cartmill, Lemelin, and

forelimb than the hind limb might be another way in which primates

Schmitt (2007) acknowledged that both gait patterns enhance stability

are able to spare their forelimbs from disruptive locomotor stresses,

at the point of forelimb touchdown, but argue that an equally impor-

and Schmitt (1998, 1999) argues that the advantages of a compliant

tant consideration is the long interval during a step cycle when the

gait were major contributors in the successful exploitation of the arbo-

body is supported by one fore- and one hind limb. For a diagonal

real habitat by the primate order.

sequence, diagonal couplet gait this will be a diagonal pair of limbs,

It can be argued, then, that the increased mobility and range of motion of the forelimb necessitated by reliance on clawless grasping extremities and facilitated by reduced peak locomotor forces, afforded ever more diverse and versatile forelimb use, which in turn contributed to other distinctive aspects of primate behavior. Although this explanation for the observed functional differentiation between the fore- and hind limbs of primates seems plausible, is there evidence that this characteristic is indeed related to locomotion and not itself a by-product of dependence on the forelimb for feeding, foraging and manipulation? Noting that the South American wooly opossum (Caluromys philander) occupies a small branch niche and uses grasping hands and feet like many primates (although they retain claws on their digits), Schmitt and Lemelin (2002) and Schmitt, Gruss, and Lemelin (2010) explored their footfall patterns, forelimb kinematics, and distribution of SRF to determine if their shared ecology and behavior has led to convergent locomotor characteristics. They reported that unlike other opossums, wooly opossums use diagonal sequence/diagonal couplet gaits, a more protracted arm, and display higher peak vertical SRF on their hind limbs as observed in quadrupedal primates, offering strong evidence supporting the link between primate locomotor characteristics and exploitation of the small branch niche. While the wooly opossum converges on primates in regard to habitat and locomotion, the common marmoset (Callithrix jacchus) in some ways converges on nonprimate arborealists like squirrels in preferring large vertical tree trunks where they use claw-

whereas in a lateral sequence, lateral couplet gait it will be an ipsilateral pair. Since the latter tends to cause the body to lurch from one side to the other, while the former keeps the body more centered over the narrow support, primates prefer the diagonal sequence, diagonal couplet combination (Cartmill et al., 2002, 2007). Young (2009) noted that primate asymmetric gaits, which are frequently used for higher speed locomotion, particularly in small-bodied primates, have received comparatively little attention. He explored the asymmetrical gait dynamics of marmosets and squirrel monkeys moving on terrestrial and arboreal substrates, and reported that the monkeys were able to alter aspects of their gait, such as peak vertical forces and center of mass movements, to increase stability on the arboreal supports. Higursashi, Hirasaki, and Kumakura (2009) and Nyakatura, Fischer, and Schmidt (2008) both noted that most research on the characteristics of primate quadrupedal gait have focused on horizontal motion over continuous supports, whereas in reality, the arboreal habitat is discontinuous and supports vary in orientation. Nyakatura et al. (2008) observed that cotton-top tamarins (Saguinus oedipus) dramatically altered the kinematics and phasing of limb motions depending on whether they were traveling up or down an incline. Higursashi et al. (2009) similarly found that Japanese macaques (M. fuscata) moving over discontinuous supports simulated by horizontal ladders, altered

like nails to cling and climb in order to feed on exudates. They are

footfall sequencing and/or limb coupling in response to varying rung

small-bodied, have short limbs and a reduced hallux that is less oppos-

intervals. In both studies, the authors were able to identify biomechani-

able than other primates. Schmitt (2003) has shown that their locomo-

cal advantages of particular combinations of gait parameters in specific

tion is also atypical for a primate: they use lateral sequence gaits when

circumstances, but both agreed that the behavioral plasticity exhibited

they walk, do not highly protract their arm during a step and display

by primate quadrupeds that make these adjustments possible is more

high peak forelimb SRF. However, Callithrix appears to be an outlier in

significant than was the use of any particular gait type, as did Hilde-

this regard as other callitrichids that also possess claw-like nails but uti-

brand in 1967.

lize small branches with greater regularity exhibit more typical primate locomotor characteristics (Schmitt, 2003).

7 | CONCLUSIONS

Although there is ample evidence that the distinctive use of diagonal sequence/diagonal couplet gaits by primates is correlated with use

The pages of AJPA offer a rich history of primate locomotor research,

of a small branch environment, a functional explanation for why it is

and this overview is far from complete. There are many fine papers,

advantageous has been a matter of debate. Shapiro and Raichlen

not to mention whole areas of research, like studies of size and scaling,

(2005) took advantage of the wider range of gait patterns exhibited by

that I couldn’t fit in, and I apologize to anyone who I may have

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LARSON

unintentionally slighted in this way. Papers on primate locomotor morphology enjoy the longest tradition of appearance in the journal and continue to be the most frequent type of contribution today, with experimental studies a not too distant second on both counts. However, primate locomotor research as a whole is not a large component of publications in AJPA, averaging roughly four or five papers a year; and it is not a recognized category in the editor’s annual reports or in the list of topics sorting contributed presentations and posters at the AAPA meetings. This could simply be due to history or to the fact that many of the papers I have included in this review could be logically placed in other categories such as primate or human paleontology, primate behavior or osteology. It seems likely that in the future, studies of morphology will continue to be the most frequent type of primate locomotor research to appear in AJPA. For a number of reasons, lab-based experimental research is gradually being replaced by zoo and sanctuary-based studies, and by studies that bring the lab equipment into the field. Although this will curtail some types of research, such as electromyographic studies, it offers the potential to expand the taxonomic diversity of research subjects and with it a more complete understanding of the full range of the locomotor characteristics of nonhuman primates.

AC KNOW LE DGME NT S I wish to thank the editors for offering me the opportunity to undertake this overview of nonhuman primate locomotor research in the pages of AJPA, and also thank Chris Ruff and Kevin Hunt for very

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OR CID

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How to cite this article: Larson SG. Nonhuman Primate Loco-

Workman, C., & Covert, H. H. (2005). Learning the ropes: The ontogeny of locomotion in red-shanked douc (Pygathrix nemaeus) Delacour’s

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