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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709
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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LARSON
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
716
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LARSON
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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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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