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Journal of Human Evolution 130 (2019) 61e71

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Journal of Human Evolution

journal homepage: www.elsevier .com/locate/ jhevol

The mechanical origins of arm-swinging

Michael C. Granatosky a, *, Daniel Schmitt b

a Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USAb Department of Evolutionary Anthropology, Duke University, Durham, NC, USA

a r t i c l e i n f o

Article history:Received 9 July 2018Accepted 2 February 2019

Keywords:Arboreal locomotionBrachiationPrimatesSlothsBatsSuspensory locomotion

* Corresponding author.E-mail address: mgranatosky@uchicago.edu (M.C.

https://doi.org/10.1016/j.jhevol.2019.02.0010047-2484/© 2019 Elsevier Ltd. All rights reserved.

a b s t r a c t

Arm-swinging is a locomotor mode observed only in primates, in which the hindlimbs no longer have aweight bearing function and the forelimbs must propel the body forward and support the entirety of theanimal's mass. It has been suggested that the evolution of arm-swinging was preceded by a shift toinverted quadrupedal walking for purposes of feeding and balance, yet little is known about the me-chanics of limb use during inverted quadrupedal walking. In this study, we test whether the mechanics ofinverted quadrupedal walking make sense as precursors to arm-swinging and whether there arefundamental differences in inverted quadrupedal walking in primates compared to non-primate mam-mals that would explain the evolution of arm-swinging in primates only. Based on kinetic limb-loadingdata collected during inverted quadrupedal walking in primates (seven species) and non-primatemammals (three species), we observe that in primates the forelimb serves as the primary propulsiveand weight bearing limb. Additionally, heavier individuals tend to support a greater distribution of bodyweight on their forelimbs than lighter ones. These kinetic patterns are not observed in non-primatemammals. Based on these findings, we propose that the ability to adopt arm-swinging is fairly simplefor relatively large-bodied primates and merely requires the animal to release its grasping foot from thesubstrate. This study fills an important gap concerning the origins of arm-swinging and illuminatespreviously unknown patterns of primate locomotor evolution.

© 2019 Elsevier Ltd. All rights reserved.

1. Introduction

Arm-swinging is a form of suspensory locomotion unique toprimates among mammals inwhich only the forelimbs are used forweight-support and forward propulsion. This dynamic and me-chanically challenging form of locomotion has evolved multipletimes within primates: at least once in atelines (Jones, 2008;Rosenberger et al., 2008), once in Pygathrix (Byron and Covert,2004; Granatosky, 2015; Byron et al., 2017), and once, if not moretimes, in hominoids (Avis, 1962; Lewis, 1971; Tuttle, 1975; Larson,1998). Furthermore, even anatomically non-specialized primateshave been observed occasionally arm-swinging (SupplementaryOnline Material [SOM] Table S1). It should be noted that,although arm-swinging is often used synonymously with brachia-tion (e.g., Avis, 1962; Tuttle, 1975; Byron and Covert, 2004; Jones,2008), in this manuscript we reserve the term brachiation todescribe the ricochetal suspensory movements of extant gibbons

Granatosky).

(Hunt et al., 1996; Usherwood et al., 2003). Despite the funda-mental importance of arm-swinging to the evolutionary history ofprimates, its origins remain unknown. While the adaptive advan-tages of suspensory locomotion have been discussed in great detail(see Grand, 1972; Cartmill and Milton, 1977; Cartmill, 1985;Granatosky, 2016), no hypothesis has yet to be proposed for whyprimates utilize arm-swinging while all other mammals arerestricted to inverted quadrupedal walking.

From a paleontological perspective, investigating the origins ofarm-swinging is difficult. Much of these challenges arise from thefact that, although there are many anatomical modifications pre-sent within the postcranial skeleton of specialized arm-swingingprimates (e.g., Johnson and Shapiro, 1998; Larson, 1998; Reinet al., 2015; see list below), these features are not required toadopt arm-swinging behavior. It is easy to recognize habitual arm-swingers among extant and extinct taxa with their long forelimbsand long manual digits. But the earliest instances of arm-swingingas a critical adaptive behavior may have involved a functionaltransition in the role of the forelimb without major anatomicalchange. The number of anatomically non-specialized primatesobserved occasionally arm-swinging (SOM Table S1) supports the

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e7162

notion that the ability to adopt arm-swinging locomotion does notrequire any particular anatomical necessity beyond a mobileshoulder joint and the ability to flex the digits of the hand into afunctional hook (Granatosky, 2016). Such features are consideredsynapomorphic for primates (Larson, 1998; Bloch and Boyer, 2002;Schmitt and Lemelin, 2002; Boyer et al., 2013); thus, all primateshave the potential to move by arm-swinging. Additionally, Byronet al. (2017) demonstrated that there are limited mechanical solu-tions to arm-swinging, and as such anatomical convergence andparallelism are to be expected, an idea that reflects argumentsmade by Larson (1998). Such evolutionary processes make accuratereconstructions of phylogenetic relatedness and trait evolutiontenuous. It should also be noted that many derived postcranialfeatures of extant hominoids are suitable for both suspensory be-haviors and vertical climbing, so it is uncertain whether theyevolved first as an adaptation of one of these behaviors and weresubsequently co-opted for the other, or whether the two special-ized behaviors evolved simultaneously (for a relevant example, seeMoy�a-Sol�a et al., 2004; Alba et al., 2010; Alba, 2012). Takentogether, a purely paleontological approach to investigating theorigins of arm-swinging is problematic because without cleardiagnostic anatomical features linked with specific behaviors, it isimpossible to accurately reconstruct the locomotor repertoire ofthe earliest supposed arm-swinging primates.

As complement to paleontological analysis, an experimentalapproach using extant animals has proven greatly informative inreconstructing patterns in locomotor evolution across tetrapods(Schmitt and Lemelin, 2002; Reilly et al., 2006; Grossi et al., 2014;Nyakatura et al., 2014; Karantanis et al., 2015). Mechanically, theevolution of arm-swinging must have required a functional reor-ganization of the forelimb to become the primary propulsive andload-bearing limb (Fleagle et al., 1981; Granatosky, 2016; Byronet al., 2017). This arrangement presents an especially difficultbiomechanical challenge for primates, which predominantly relyon the hindlimb for both weight support and propulsion duringarboreal quadrupedal walking, climbing, and leaping (Kimura et al.,1979; Reynolds,1985; Hirasaki et al., 1993; Hanna et al., 2017). Thus,the origin of arm-swinging in primates, and not other animals, issimultaneously central to understanding the evolution of our orderand profoundly difficult to explain.

One locomotor mode seen as a potential precursor to arm-swinging is inverted quadrupedal walking; a form of suspensorymovement where animals walk quadrupedally upside down andutilize all four limbs for support and progression (Cartmill andMilton, 1977; Mendel, 1979; Granatosky et al., 2016; Byron et al.,2017). Switching between arboreal quadrupedal walking abovebranches and inverted quadrupedal walking below branches isthought to require very little anatomical and neuromuscular reor-ganization, and as a result has evolved numerous times amongvarying mammalian clades (Demes et al., 1990; Ishida et al., 1990;Fujiwara et al., 2011; Nyakatura, 2012). Slow, deliberately movingarboreal quadrupeds, like the lorises and sloths, that commonlyadopt inverted quadrupedal walking exhibit considerableanatomical similarities with arm-swinging primates (e.g., highlymobile wrist and ankle with and deep carpal and tarsal tunnels;Grand, 1967; Cartmill and Milton, 1977; Mendel, 1979; Jenkins,1981; Read, 2001), degree of phalangeal curvature in the handsand feet (Jungers et al., 1997), elongation of limbs (Mendel, 1981;Preuschoft and Demes, 1984; Swartz, 1989), medially compressedscapula (Green et al., 2016), globular humeral head and capitulum(Miller, 1935; Ashton and Oxnard, 1964; Jenkins et al., 1978; Rose,1988), short olecranon process (Rein et al., 2015), longer femoralneck and greater trochanter that lies inferior to the femoral head(Simons et al., 1992; Godfrey and Jungers, 2003; Gebo, 2014),

craniocaudally elongated and dorsoventrally short spinous pro-cesses, dorsally oriented transverse processes, and dorsoventrallyand mediolaterally elongated vertebral bodies (Johnson andShapiro, 1998; Granatosky et al., 2014). Such profound anatomicalsimilarities have led to the as yet untested proposition that theevolution of arm-swinging could be associated with an increase inbody size in arboreal primates that commonly adopt invertedquadrupedal walking (Grand, 1972; Cartmill and Milton, 1977;Cartmill, 1985).

In support of this notion, it is worth noting that the relativeimportance of suspensory locomotion and posture in arborealmammals' behavioral repertoires varies as a function of its bodyweight; for larger animals it is mechanically easier to hang below arelatively small branch rather than balancing atop it (Grand, 1972;Cartmill, 1985). In this light, it is possible to hypothesize that theevolution of arm-swinging in primates proceeds from arborealquadrupedal walking to inverted quadrupedal walking and then toarm-swinging, with changes in hindlimb and forelimb function ateach stage. That explanation, which is intuitively appealing, re-mains untested and is not a sufficient explanation in light ofavailable data. Other mammals use inverted quadrupedal walkingin their normal locomotor repertoire (Fujiwara et al., 2011;Granatosky, 2016), but arm-swinging has only evolved in pri-mates. Moreover, the fact that multiple lineages of primatesevolved arm-swinging independently suggests the presence ofsome shared mechanical precursor to arm-swinging present in allprimate lineages and not observed in other mammals (Byron et al.,2017). The questions that arise then are: do the mechanics ofinverted quadrupedal walking make sense as precursors to arm-swinging and are there fundamental differences in invertedquadrupedal walking in primates compared to non-primatemammals that would explain the evolution of arm-swinging inprimates only?

Data on limb-loading patterns of primates during invertedquadrupedal walking are currently limited to three closely-relatedstrepsirrhine species. During inverted quadrupedal walking forthese species, the forelimbs carry more body weight than thehindlimbs and serve as the primary propulsive limb, while thehindlimbs serve primarily braking functions (Ishida et al., 1990;Granatosky et al., 2016), a pattern opposite to what they exhibitduring above-branch walking. Unfortunately, due to the narrowtaxonomic breadth of this data it remains unclear whether thepatterns observed during inverted quadrupedal walking in pri-mates reflect strepsirrhine-specific patterns, primate-specific pat-terns, or mechanical requirements of below branch quadrupedallocomotion for all mammals.

The goal of this study is to test the hypothesis that invertedquadrupedal walking in primates is characterized by forelimb-dominated features of weight support and propulsion that wouldmake this form of locomotion a potential precursor to arm-swinging. To address this, we collected measures of weight sup-port distributiondi.e., peak vertical force (Vpk) and vertical im-pulse (VI)dand whether a limb applies a net propulsive or brakingforce (net fore-aft force impulse) on the forelimbs and hindlimbsduring arboreal quadrupedal walking and inverted quadrupedalwalking for seven primate species across awide range of bodymass(0.47e5.09 kg). Limb-loading datawere collected as animalsmovedat self-selected speeds across a stimulated arboreal runway inte-gratedwith force plates (Granatosky et al., 2016). In addition, and asan essential test of this model, these data were compared to pat-terns of inverted quadrupedal walking we collected on three spe-cies of non-primate mammal (bats and sloths) across a range inbody mass (0.03e7.25 kg) moving on similar instrumented run-ways (SOM Table S2).

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e71 63

2. Methods

2.1. Experimental design

Kinetic gait data were collected from animals housed at theDuke Lemur Center (Durham, NC, USA), North Carolina ZoologicalPark (Asheboro, NC, USA), Central Florida Zoo and Botanical Gar-dens (Sanford, FL, USA), Lubee Bat Conservancy (Gainesville, FL,USA), and Monkey Jungle Dumont Conservancy (Miami, FL, USA).All animal use was approved by the Duke Lemur Center (DLCResearch Project #MO-10-11-3) and Duke's Institutional AnimalCare and Use Committee (IACUC protocol # A270-11-10 and A245-14-10). All animals were adults and were clear of any pathologies orgait abnormalities (SOM Table S2).

Prior to the first trial, animals wereweighed by animal care staff.Forces for each day of trials were normalized to the weight recor-ded from that first day of data collection. The total sampling periodfor any individual lasted no longer than two weeks, so fluctuationsin body weight between the first and last day of sampling werelikely low. Forelimb and hindlimb single-limb forces were collectedwhile animals walked above [ruffed lemur (Varecia variegata), ring-tailed lemur (Lemur catta), Coquerel's sifaka (Propithecus coquereli),aye-aye (Daubentonia madagascariensis), common squirrel monkey(Saimiri sciureus), Nancy Ma's night monkey (Aotus nancymaae),and white-faced capuchin (Cebus capucinus)] and below[(V. variegata, L. catta, P. coquereli, D. madagascariensis, S. sciureus,A. nancymaae, C. capucinus), large flying fox (Pteropus vampyrus),Linnaeus's two-toed sloth (Choloepus didactylus), and commonvampire bat (Desmodus rotundus)] instrumented runways. Theinstrumented portion of the runways consisted of two Kistler forceplates (model 9317B; Kistler, Amherst, NY, USA). Force plate outputwas sampled at 12,000 Hz, and imported, summed, and processedusing BioWare™ v. 5.1 software (Kistler, Amherst, NY, USA), andthen filtered (Butterworth, 60 Hz) and analyzed using MATLAB(MathWorks, Natick, MA, USA).

Locomotor data on below branch quadrupedal locomotion inDe. rotundus was collected in a custom-made plexiglass enclosure(0.48 m � 0.15 m � 0.11 m) with an instrumented ceiling followingthe runway design outlined in previous studies (Riskin andHermanson, 2005; Riskin et al., 2006; Granatosky, 2018b). Theuse of this enclosure was required to prevent De. rotundus fromflying away during trials. Animals were encouraged to walk backand forth on the ceiling by lightly blowing on them through a straw(Riskin and Hermanson, 2005). The material makeup of the ceilingconsisted of a wire mesh, in which animals were able to grasp withtheir claws. The force plates were secured to section of stiff wiremesh (0.025 m � 0.15 m).

For all other species, locomotor data was collected on aninstrumented pole measuring 3.66 m in length and 3.10 cm indiameter that was positioned in their home enclosures. A smallsection of dowel was secured on one end of each force platemeasuring the same diameter as the rest of the runway and largeenough to accommodate the fore-aft length of the entire hand orfoot (~10 cm). These instrumented sections were mounted in themiddle of the runway flush with, but separated by a small gap from,the rest of the runway.

The animals were video-recorded during trials from a lateralview using a GoPro camera (Hero 3 þ Black Edition; GoPro, SanMateo, CA, USA) modified with a Back-Bone Ribcage (Ribcage v1.0;Back-Bone Gear Inc, Ottawa, ON, Canada), which allows the GoProcameras to be outfitted with interchangeable lenses and eliminatesimage distortion inherent to the camera (Granatosky, 2015;Granatosky et al., 2016; Byron et al., 2017). All videos were recor-ded at 120 frames/s. For each step, the subject's speed was calcu-lated by digitizing a point on the subject's head at each field over

the entire stride and calculating instantaneous speed at each in-terval based on a known distance marked on the runway used tocalibrate the image space. Only walking steps (i.e., duty factor over50%) in which the animal was traveling in a straight path and notaccelerating or decelerating (i.e., steady-state locomotion) wereselected for analysis. Steady-state locomotion was determined bycalculating the instantaneous velocity between subsequent videoframes throughout the entire stride, and then using regressionanalysis to determine whether velocity changed throughout thestride (Granatosky, 2015; Granatosky et al., 2016). Only strides withno detectable change in speed (i.e., slope not significantly differentfrom zero) were analyzed. Additionally, only steps with single-limbcontacts on the plate or those steps in which the forelimb andhindlimb forces were clearly differentiated were analyzed.

From these data, three variables were calculated for each step:(1) peak vertical (Vpk) force; (2) vertical impulse (VI); and (3) netfore-aft force impulse. The Vpk force was measured as the highestmagnitude point measured on the vertical force component of thesubstrate reaction force. The VI and net fore-aft force impulse weremeasured as the area under the force-time curve in the vertical andhorizontal component of the substrate reaction force, respectively.The net fore-aft force impulse provides a means for differentiatingthe overall braking or propulsive role of the limb during particularlocomotor behaviors (Demes et al., 1994). The net fore-aft forceimpulse for each limb was calculated by subtracting the brakingimpulse from the propulsive impulse. Positive values indicate a netpropulsive limb, while negative values indicate a net braking limb.Values approximating zero represent single limb contact forceswere braking and propulsive impulses are approximately equal.

All force data were normalized for the direction of travel,differing body mass, and orientation. This resulted in comparableforce curves that all displayed vertical force as positive value onthe vertical axis, braking force as a negative value on the fore-aftaxis, and propulsive force as a positive value on the fore-aft axis.In order to make comparisons between subjects of differing bodymasses, Vpk force was compared in multiples of body weight (%bw), and VI and net fore-aft force impulse in body weight seconds(%bws).

2.2. Statistical analyses

All statistical tests were conducted using MATLAB. Shapiro-Wilkand Levene's test were used to determine normality and homo-scedasticity within the data (Sokal and Rohlf, 2012). Prior to anystatistical comparisons, body weight-normalized Vpk, VI, and netfore-aft force impulse for each limb, species, and orientation werecompared with speed (m/s) and contact time (s) using a regressionanalysis to determine whether the variables of interest wereinfluenced by variation in speed or contact time within the sample.The magnitude of substrate reaction forces is thought to be influ-enced by speed and contact time (Demes et al., 1994). In order toaccount for the effect of speed and contact time, all Vpk, VI, and netfore-aft force impulse data that demonstrated a significant corre-lation were examined using an analysis of covariance (ANCOVA)with speed and contact time as the covariate to compare acrosslimbs and orientation (Olejnik and Algina, 1984; Vickers, 2005). Forthose variables that showed no association with speed or contacttime, we used a Kruskal-Wallis test, a non-parametric ANOVA, todetermine whether there were statistically significant differencesacross limbs and orientation. No interspecific comparisons wereconducted.

To assess whether variation in body size between species couldinfluence the tendency for forelimb-biased weight support, weconducted a regression analysis comparing weight distribution onthe forelimbs (R) during inverted quadrupedal walking in primate

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e7164

and non-primate mammals to body weight. We calculated R foreach individual as:

R ¼ VIFL=VItotal

where VIFL is the mean VI in the forelimb for each individual, andVItotal is the sum of the mean VI in the forelimb and hindlimb foreach individual (Raichlen et al., 2009; Larson and Demes, 2011;Granatosky et al., 2018). Values equal to 0.5 represent equalweight distribution between the limbs. Values lower than 0.5indicate greater weight distribution borne by the hindlimbs, andvalues greater than 0.5 indicate greater weight distribution borneby the forelimbs. In this study, R was calculated based onmean VI inthe forelimb and hindlimb for each individual. This calculation of Rwas necessary, because animals in this study tended to walk with adiagonal sequence gait (i.e., each hindlimb footfall is followed by acontralateral forelimb footfall) and placed the hindlimb in closeproximity to the forelimb. Therefore, likelihood of getting singlelimb forces from both the forelimb and the hindlimb during a singlestride was low.We also assessed whether R varied with the averageof speed and contact time of the individual during invertedquadrupedal walking using a regression analysis to determine ifthis association could confound our interpretations. No significantrelationship was observed between R and speed or contact time.

Data reported in this paper are provided as SOM Table S3.

3. Results

During arboreal quadrupedal walking, all primates displayedlower values for weight supportdi.e., lower Vpk (Fig. 1) and VI(Fig. 2)don the forelimbs compared to the hindlimbs (Tables 1 and2). Furthermore, during arboreal quadrupedal walking in all

Figure 1. Mean and standard deviation values of peak vertical forces in the forelimbs (yelloinverted quadrupedal walking in primates and non-primate mammals. All data presented asfigure legend, the reader is referred to the Web version of this article.)

primates the forelimb served a net braking function, while thehindlimb was net propulsive (Fig. 3). In sharp contrast, duringinverted quadrupedal walking all primate species in this studydemonstrated higher values for weight support on the forelimbscompared to the hindlimbs. In addition, the forelimb now served asthe primary propulsive limb, while the hindlimb had a net brakingfunction (Table 1; Fig. 3). This pattern, which is a profound reversalfrom the arboreal quadrupedalwalking condition, is independent ofphylogenetic relationships, or the relative frequency at which eachspecies utilizes suspensory locomotor behaviors during theirnormal locomotor repertoires (SOM Table S1). All non-primatemammals demonstrated the same pattern of a primarily propul-sive forelimb and braking hindlimb during inverted quadrupedalwalking, but none of the non-primate species demonstratedforelimb-biasedweight support. Both bat species and sloths showedequal contributions weight support between the forelimb andhindlimb, or a tendency for the hindlimb to bear a majority of bodyweight.

Additionally, during inverted quadrupedal walking in primatesthe proportion of weight distribution on the forelimbs (R) increasedsignificantly (y ¼ 0.031x þ 0.522; R2 ¼ 0.546; p � 0.001) with bodymass (Fig. 4). While all primates demonstrated forelimb-biasedweight support (SOM Fig. S1), heavier individuals tended to supporta greater distribution of body weight on their forelimbs than lighterindividuals. No such relationship (y ¼ 0.009x þ 0.394; R2 ¼ 0.177;p ¼ 0.197) was observed in the non-primate mammals in this study.

4. Discussion

Arm-swinging is a form of locomotion observed only in pri-mates, in which the forelimbs alone must serve to both propel the

w) and hindlimbs (blue) during above branch quadrupedal locomotion in primates anda percentage of body weight (%bw). (For interpretation of the references to color in this

Figure 2. Mean and standard deviation values of vertical impulse in the forelimbs (yellow) and hindlimbs (blue) during above branch quadrupedal locomotion in primates andinverted quadrupedal walking in primates and non-primate mammals. All data presented as a percentage of body weight seconds (%bws). (For interpretation of the references tocolor in this figure legend, the reader is referred to the Web version of this article.)

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e71 65

body forward and support the animal's mass. Yet it is unknownhow this form of locomotion evolved. The data here show aparsimonious mechanical pathway for the evolution of arm-swinging. In stark contrast to the well-reported pattern seen dur-ing arboreal quadrupedal walking, climbing, and leaping (Kimuraet al., 1979; Reynolds, 1985; Hirasaki et al., 1993; Hanna et al.,2017), when walking quadrupedally below branches all of the pri-mate species sampled so far rely primarily on the forelimb for bothweight support and propulsion. This finding indicates that thefundamental reorganization of forelimb function, which is neces-sary for the evolution of arm-swinging (Byron et al., 2017), occursduring the adoption of inverted quadrupedal walking. In contrast,non-primate mammals do not show forelimb-biased loading pat-terns during inverted quadrupedal walking and rely much moreheavily on the hindlimb for support. This suggests that non-primatemammals are faced with a mechanical constraint that makes themless likely to adopt arm-swinging behavior. It should be noted thatour sample of non-primate mammals was limited to only threespecies. Therefore, we propose caution in interpreting the patternsobserved in non-primate mammal until data from a greater taxo-nomic breadth can be collected.

4.1. Body size and the origins of arm-swinging

There are two non-mutually exclusive hypotheses as to whyanimals may adopt suspensory positional behaviors. From anecological perspective, suspensory movement allows an animal toeffectively double its feeding sphere (i.e., animals are able to ac-cess resources both above and below the support; Grand, 1972). Asecond theory considers a biomechanical model that predicts theratio of body size to support varies inversely with the ability to

remain balanced above the support. As the body size to supportsize ratio increases, arboreal quadrupedal walking becomes per-ilous (Napier, 1967; Cartmill, 1985; Lammers and Gauntner, 2008).One solution to this balance problem may be for arboreal animalsto move their center of mass below the support, thereby adoptingsuspensory behaviors (Napier, 1967; Cartmill, 1985). While therelationship between suspensory locomotion and body mass and/or increasing the feeding sphere has been established in a numberof sources (Napier, 1967; Grand, 1972; Cartmill, 1985), the ques-tion remains: why do primates adopt arm-swinging instead ofsimply adopting inverted quadrupedal walking like all othermammalian taxa?

The most common answer to this question usually comes downto an argument of the energetically efficient movement associatedwith the pendular mechanics of arm-swinging (Erikson, 1963;Fleagle, 1974; Chang et al., 2000). However, as has been evi-denced by a number of studies, arm-swinging primates rarelyadopt kinematic and kinetic patterns consistent with pendularmechanics (Bertram et al., 1999; Chang et al., 2000; Usherwoodet al., 2003; Bertram, 2004; Byron et al., 2017). Furthermore,work by Parsons and Taylor (1977) demonstrated relatively highlocomotor costs of transport during arm-swinging compared toarboreal quadrupedal walking or inverted quadrupedal walking.Our data on the association between forelimb functional roles andbody weight in primates demonstrate that heavier individuals tendto support a greater proportion of their body weight on theirforelimbs. The mechanism for why this pattern occurs is beyondthe scope of this study and remains an area of active investigation,but these data suggest that for larger-bodied primates the hindlimbis contributing little to overall weight support during invertedquadrupedal walking. As such, we propose that the ability to adopt

Table 1Summary statistics (mean ± SD) for kinetic variables during above branch quadrupedal locomotion and inverted quadrupedal walking in primates and non-primatemammals.

Species Orientation Speed(m/s)

Limb n Contact time (s) Net fore-aftimpulse (%bws)

Peak verticalforce (%bw)

Vertical impulse(%bws)

Weight distributionon the

forelimbs (R)a

Varecia variegata Above 0.82 ± 0.17 FL 40 0.50 ± 0.13 �3.00 ± 0.96 56.37 ± 7.34 16.08 ± 4.31 0.39 ± 0.03HL 31 0.63 ± 0.15 2.31 ± 1.38 77.14 ± 8.96 25.96 ± 6.43

Below 0.69 ± 0.15 FL 38 0.60 ± 0.08 3.51 ± 1.81 82.54 ± 14.95 28.36 ± 4.57 0.59 ± 0.01HL 33 0.58 ± 0.07 �1.78 ± 1.35 59.64 ± 10.94 19.43 ± 3.92

Lemur catta Above 0.57 ± 0.15 FL 28 0.69 ± 0.13 �2.92 ± 1.05 44.28 ± 5.10 18.36 ± 3.86 0.36 ± 0.02HL 25 0.69 ± 0.12 2.58 ± 1.29 78.63 ± 9.86 31.89 ± 4.82

Below 0.55 ± 0.13 FL 52 0.49 ± 0.11 2.09 ± 2.23 70.12 ± 9.32 19.34 ± 4.62 0.61 ± 0.05HL 41 0.49 ± 0.11 �2.36 ± 1.75 43.79 ± 10.84 12.16 ± 5.75

Propithecus coquereli Above 0.64 ± 0.18 FL 14 0.47 ± 0.19 �3.07 ± 1.84 50.85 ± 13.77 14.09 ± 6.12 0.32 ± 0.08HL 15 0.57 ± 0.12 3.40 ± 1.60 83.81 ± 15.11 27.57 ± 8.76

Below 0.51 ± 0.07 FL 59 0.59 ± 0.12 2.71 ± 1.91 79.90 ± 10.71 28.52 ± 5.38 0.67 ± 0.08HL 51 0.65 ± 0.13 �2.74 ± 2.00 34.98 ± 7.80 13.48 ± 4.85

Daubentonia madagascariensis Above 0.61 ± 0.23 FL 46 0.47 ± 0.09 �2.79 ± 1.65 53.48 ± 9.11 14.91 ± 4.71 0.40 ± 0.01HL 28 0.59 ± 0.16 3.98 ± 2.42 73.54 ± 8.19 22.52 ± 6.62

Below 0.44 ± 0.14 FL 26 0.81 ± 0.26 4.32 ± 4.80 66.96 ± 8.33 31.09 ± 9.03 0.61 ± 0.05HL 22 0.73 ± 0.20 �2.98 ± 2.55 49.04 ± 10.14 19.18 ± 7.10

Cebus capucinus Above 0.80 ± 0.20 FL 15 0.44 ± 0.21 �2.15 ± 1.50 53.13 ± 16.09 14.88 ± 9.79 0.32 ± 0.05HL 14 0.59 ± 0.20 2.22 ± 1.47 82.37 ± 14.33 28.16 ± 11.02

Below 0.57 ± 0.11 FL 16 0.62 ± 0.17 3.14 ± 2.91 83.05 ± 9.04 32.95 ± 9.97 0.65 ± 0.05HL 16 0.63 ± 0.21 �2.40 ± 2.68 59.24 ± 12.80 20.15 ± 7.12

Aotus nancymaae Above 0.63 ± 0.08 FL 13 0.68 ± 0.19 �1.88 ± 1.17 39.73 ± 11.37 14.73 ± 6.01 0.26 ± 0.03HL 16 0.88 ± 0.30 2.10 ± 1.32 76.58 ± 7.94 42.51 ± 16.76

Below 0.71 ± 0.16 FL 16 0.68 ± 0.25 1.83 ± 1.79 69.10 ± 11.86 28.62 ± 9.99 0.56 ± 0.02HL 14 0.74 ± 0.29 �2.55 ± 1.65 48.21 ± 12.52 22.93 ± 13.12

Saimiri sciureus Above 0.59 ± 0.13 FL 79 0.21 ± 0.09 �0.80 ± 0.64 47.82 ± 7.29 5.49 ± 2.46 0.38 ± 0.04HL 52 0.23 ± 0.08 1.32 ± 0.82 65.41 ± 7.30 8.85 ± 3.43

Below 0.56 ± 0.07 FL 19 0.42 ± 0.19 2.46 ± 2.11 59.29 ± 8.78 11.80 ± 3.84 0.54 ± 0.04HL 14 0.52 ± 0.26 �2.10 ± 1.19 45.92 ± 4.46 9.67 ± 3.09

Choloepus didactylus Below 0.10 ± 0.03 FL 25 5.10 ± 1.73 14.53 ± 10.90 61.64 ± 15.74 130.72 ± 23.19 0.47 ± 0.00HL 18 5.17 ± 1.99 �13.49 ± 21.12 59.75 ± 15.41 146.40 ± 46.04

Pteropus vampyrus Below 0.17 ± 0.04 FL 16 1.77 ± 0.89 3.79 ± 9.54 43.07 ± 12.26 34.81 ± 17.20 0.38 ± 0.07HL 25 1.94 ± 0.79 �4.23 ± 8.09 65.81 ± 19.14 56.63 ± 22.74

Desmodus rotundus Below 0.18 ± 0.05 FL 22 0.93 ± 0.37 5.92 ± 10.87 61.32 ± 13.76 36.51 ± 18.69 0.41 ± 0.05HL 27 0.82 ± 0.36 �5.33 ± 9.70 68.59 ± 13.33 48.31 ± 16.55

Abbreviations: FL ¼ forelimb; HL ¼ hindlimb.a Weight distribution on the forelimbs (R) calculated as R ¼ VIFL/VItotal, where VIFL is the mean VI in the forelimb for each individual, and VItotal is the sum of the mean VI in

the forelimb and hindlimb for each individual.

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arm-swinging is fairly simple for relatively large-bodied primates,and merely requires the animal to release its grasping foot from thesubstrate. This view is reinforced by the finding that the twolargest-bodied primate species analyzed in this study (i.e.,C. capucinus and P. coquereli) both occasionally used arm-swingingto cross the runway (SOM Fig. S2), and have been observed arm-swinging in the wild (SOM Table S1).

As appealing as the relationship between body size andforelimb-biased loading may appear, important issues remain. Wehave thrown around the phrase ‘relatively large-bodied primates’as if these animals could be categorized as distinct from otherspecies. Unfortunately, we cannot provide an exact body weight atwhich primates should switch from inverted quadrupedal walkingto arm-swinging. If one was to rely solely on our regression equa-tion (see Results) then 100% of body weight should be supported bythe forelimbs at ~ 15 kg. Obviously, this is a gross overestimate asmuch smaller bodied primates, such as gibbons (~5.5 kg), spidermonkeys (~7.5 kg), and douc langurs (~9.5 kg), all frequently utilizearm-swinging as part of their locomotor repertoire (Granatosky,2018a). Interestingly, despite our attempts to collect data duringinverted quadrupedal walking in these taxa, the only form of sus-pensory locomotion that could be elicited was arm-swinging (seeByron et al., 2017). Understanding why primates tend to favor arm-swinging versus inverted quadrupedal walking at ~5 kg remains anopen and important question.

To make this discussion even more difficult, there are somerelatively large-bodied primates (e.g., chimpanzees, orangutans,and some colobus monkeys; see SOM Table S1) that are capable of

utilizing both arboreal quadrupedal walking and invertedquadrupedal walking during arboreal movement (Doran, 1996;Thorpe and Crompton, 2006; Granatosky, 2018a). In regards tothe continued use of arboreal quadrupedal walking at large bodysizes, this can easily be explained as a function of substratediameter. As has been shown in a number of studies, evenlyhighly specialized arm-swinging primates commonly utilizearboreal quadrupedal walking on relatively large diameter sub-strates (Cant, 1986; Doran, 1992, 1996; Doran and Hunt, 1996;Workman and Covert, 2005; Thorpe and Crompton, 2006). Asillustrated by Cartmill (1985), balancing on top of substrates onlybecomes a problem when the diameter of the body is greater thanthe diameter of the substrate. Even then, arboreal animals mayutilize other mechanisms to maintain upright postures (i.e.,powerful grasping extremities and muscular compensation oftoppling torques) rather than switching to suspensory locomotion(Cartmill, 1985; Lammers and Gauntner, 2008). As for thecontinued use of inverted quadrupedal walking in large-bodiedtaxa, we see no mechanical reason to suggest this is notpossible or that this pattern negates our hypothesis. It may be thecase that these animals maintain hindlimb support primarily as ameans of increased security rather than weight support. Alter-natively, models by Nyakatura and Andrada (2013) propose thatduring inverted quadrupedal walking some cautious arborealquadrupeds, such as sloths, utilize the hindlimb to slow down andcontrol the pendular movement of the center of mass. Datacollected during inverted quadrupedal walking from an orangutanwould allow one to address these hypotheses.

Table 2Statistical comparisons between forelimb and hindlimb fore-aft impulse, vertical peak force, and vertical impulse.a

Species Orientation Forelimb/hindlimb net fore-aft impulse statisticalcomparison (F; p)

Forelimb/hindlimb vertical peak force statisticalcomparison (F; p)

Forelimb/hindlimb vertical impulse statistical comparison(F; p)

Nocovariateobserved

Adjusted for covariatewith contact time (s)

Adjusted forcovariate with speed

(m/s)

Nocovariateobserved

Adjusted for covariatewith contact time (s)

Adjusted forcovariate with speed

(m/s)

Nocovariateobserved

Adjusted for covariatewith contact time (s)

Adjusted forcovariate with speed

(m/s)

Varecia variegata Above e 267.30; <0.001 304.70; <0.001 e 167.70; <0.001 148.50; <0.001 e 64.35; <0.001 61.08; <0.001Below 186.00;

<0.001e e e e 49.99; <0.001 e 76.69; <0.001 e

Lemur catta Above e 290.00; <0.001 e e 288.40; <0.001 298.00; <0.001 e 322.40; <0.001 193.60; <0.001Below e 109.80; <0.001 e e e 161.20; <0.001 e 118.5; <0.001 52.45; <0.001

Propithecus coquereli Above e 157.60; <0.001 e e e 36.22; <0.001 e 29.45; <0.001 30.05; <0.001Below e 203.00; <0.001 213.30; <0.001 e 587.60; <0.001 607.6; <0.001 e 630.00; <0.001 250.50; <0.001

Daubentoniamadagascariensis

Above e 167.60; <0.001 207.90; <0.001 e 94.70; <0.001 e e 15.66; <0.001 e

Below e 40.7; <0.001 e e e 48.96; <0.001 e 43.85; <0.001 28.58; <0.001Cebus capucinus Above e 30.7; <0.001 e e e 24.94; <0.001 e 13.59; <0.001 15.32; <0.001

Below e 69.51; <0.001 e 36.95;<0.001

e e 17.48;<0.001

e e

Aotus nancymaae Above 72.11;<0.001

e e 105.30;<0.001

e e e 52.26; <0.001 42.39; <0.001

Below 48.02;<0.001

e e e e 19.97; <0.001 e 5.34; 0.029 2.23; 0.147

Saimiri sciureus Above e 264.60; <0.001 e e 183.50; <0.001 184.80; <0.001 e 111.80; <0.001 50.32; <0.001Below e 51.37; <0.001 e e e 26.91; <0.001 e 7.63; <0.001 e

Choloepus didactylus Below 32.31;<0.001

e e e 0.24; 0.630 e e 3.12; 0.085 e

Pteropus vampyrus Below e e 7.60; 0.009 e 21.03; <0.001 e 10.75;0.003

e e

Desmodus rotundus Below 14.61;<0.001

e e 3.50; 0.068 e e e 6.77; 0.012 e

a There is one degree of freedom for all statistical tests.

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Figure 3. Mean and standard deviation values of fore-aft force impulse in the forelimbs (yellow) and hindlimbs (blue) during above branch quadrupedal locomotion in primates andinverted quadrupedal walking in primates and non-primate mammals. All data presented as a percentage of body weight seconds (%bws). Positive values indicate a net propulsivelimb, while negative values indicate a net braking limb. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e7168

4.2. Evolutionary implications and paleontological evidence

Based on data collected in this study, we propose that theforelimb loading patterns observed during inverted quadrupedalwalking in primates would have promoted the eventual adoption ofarm-swinging. In our sample, all primate species, regardless ofbody size and taxonomic affiliation, rely primarily on the forelimbfor weight support and propulsion. As such, we argue that all pri-mate lineages that commonly utilize inverted quadrupedal walkingas part of their behavioral repertoire would have the tendency toevolve arm-swinging locomotion. Furthermore, based on the rela-tionship between body size and the degree of forelimb-biasedweight support during inverted quadrupedal walking (discussedabove) it is likely that arboreal lineages characterized by relativelylarge body size would be especially likely to adopt arm-swinging.Paleontological evidence for this hypothesis is supported bytrends in body size evolution of the three primate lineagesdi.e.,hominoids (Fleagle, 1978; Grabowski and Jungers, 2017), atelines(Rosenberger and Strier, 1989; Jones, 2008; Rosenberger et al.,2008), and Pygathrix (Delson et al., 2000)dwhere arm-swingingrepresents the dominant form of suspensory locomotion.

While the tendency for large body size and arm-swinging to beassociated has been inferred from evidence in the fossil record, adirect paleontological link between inverted quadrupedal walkingand arm-swinging is more tenuous. However, a closer look atevolutionary history of atelids and hominids reveals that both lin-eages have taxa that appear to have experimented with fore- andhindlimb suspensory positional behaviors prior to evolving morespecialized anatomy associated with arm-swinging.

Jones (2008) conducted a phylogenetic study that incorporatedthe fossil genera Caipora (~10 ka) and Protopithecus (~600 ka) to

generate hypotheses about the evolutionary history of arm-swinging in the atelines. Based on ancestral state reconstructions,Jones (2008) proposed that the last common ancestor of the ate-lines was an animal with several traits intermediate betweenAlouatta and Lagothrix (e.g., biceps lever arm, humeral bituberosityindex, humeral head shape), but not yet anatomically specializedfor arm-swinging. This suggests that this ancestor was primarily anarboreal quadruped, but likely had had some suspensory abilitiesintermediate between Alouatta and Lagothrix.

The catarrhine fossil record provides a much more indirect viewof the evolution and specialization of suspensory behaviors. Suchcomplexity arises from rampant parallelism between lineages(Tuttle, 1975; Larson, 1998; Alba, 2012; Alba et al., 2015), and anattempt to reconstruct trait evolution and phylogenetic relation-ships between these lineages is beyond the scope of this study.There are, however, a few fossils that are promising candidates forlinking inverted quadrupedal walking and arm-swinging. Epi-pliopithecus vindobonensis is a middle Miocene catarrhine that ischaracterized by a mix of anatomical features that have madereconstructing its positional behavior difficult (Zapfe, 1958; Fleagle,1975; Pina Miguel, 2016). Features of both the forelimbs (e.g., aglobular articular surface of the humeral head and a degree ofhumeral torsion paired with relatively long olecranon process ofthe ulna and relatively large tubercles of the humerus relative to thearticular surface) and hindlimbs (e.g., a femoral head extendingabove the greater trochanter on a slender staff-like femoral shaftpaired with a long facet for the sustentaculum and a basin-shapedconcave facet for the tibial malleolus on the talus) do not match asingular locomotor behavior (Zapfe, 1958; Fleagle, 1975; Arias-Martorell et al., 2015; Rein et al., 2015; Pina Miguel, 2016).Instead, this odd combination of features suggests an animal

Figure 4. The relationship between the proportion of body weight on the forelimb (R) and body mass for primates (stars) and non-primate mammals (circles) during invertedquadrupedal walking. Across primates the proportion of weight distribution on the forelimbs increased significantly (y ¼ 0.031x þ 0.522; R2 ¼ 0.546; p < 0.001) with body mass. Nosuch relationship (p ¼ 0.197) was observed in the non-primate mammals. Values lower than 0.5 indicate greater weight distribution borne by the hindlimbs, and values greater than0.5 indicate greater weight distribution borne by the forelimbs.

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e71 69

capable of generalized arboreal (or even terrestrial) quadrupedallocomotion, combined with climbing, fore- and hindlimb suspen-sory locomotion, and perhaps arm-swinging to some extent(Fleagle, 1975; Arias-Martorell et al., 2015; Rein et al., 2015; PinaMiguel, 2016).

A similar mix of mosaic features are present in the partialskeleton of the extinct dryopithecine Hispanopithecus laietanus(Alm�ecija et al., 2007; Alba, 2012; Alba et al., 2012; Pina Miguel,2016). In the forelimb, the highly curved phalanges (Alm�ecijaet al., 2007) and an elbow complex suitable for enabling consid-erable pronation and supination (Alba et al., 2012) are consistentwith suspensory positional behaviors. However, H. laietanus alsodemonstrates an ulnar olecranon morphology consistent witharboreal quadrupedal walking (Alba, 2012; Alba et al., 2012).Similarly, the femora and tibia are indicative of a locomotorrepertoire combining suspensory locomotion (e.g., femoral neck-shaft angle and relative width of the tibial medial malleolus) witharboreal quadrupedal walking (e.g., the shape of the tibial articularsurface; Tallman et al., 2013; Pina Miguel, 2016). Taken together,H. laietanus supports the hypothesis that an animal capable ofadopting inverted quadrupedal walking may have represented anintermediate locomotor stage during the transition from a gener-alized arboreal quadruped locomotion to arm-swinging.

5. Conclusion

In this study, we demonstrate that when primates adoptinverted quadrupedal walking the forelimb becomes the primary

weight-support and propulsive limb. Furthermore, our datademonstrate that heavier individuals tend to support a greaterproportion of their body weight on their forelimbs. These patternsare not observed in non-primate mammals. As such, we proposethat the ability to adopt arm-swinging is fairly simple for relativelylarge-bodied primates, andmerely requires the animal to release itsgrasping foot from the substrate. These data provide a testablehypothesis to explain why arm-swinging locomotion is observedonly in primates, and how it evolved convergently across primates.We hope that these findings will inspire future works, and we seeample opportunities to explore the: (1) relationship between bodysize and the use of arm-swinging and inverted quadrupedalwalking in extant primates; (2) anatomical correlates of invertedquadrupedal walking and whether these can be separated fromarm-swinging; and (3) paleontological record for concrete linksbetween inverted quadrupedal walking and arm-swinging.

Author contributions

M.C.G. and D.S. designed the initial experiment. M.C.G. collectedand analyzed the data. M.C.G. and D.S. wrote the manuscript.

Acknowledgments

We thank all those that helped with animal care and use.Without their help, we would not have been able to complete thisstudy. We thank Pierre Lemelin, Christine Wall, Jandy Hanna, Cal-lum Ross, Zeray Alemseged, Gabriel Yapuncich, David Green, Angel

M.C. Granatosky, D. Schmitt / Journal of Human Evolution 130 (2019) 61e7170

Zeininger, Zhe-Xi Luo, David Alba, and the anonymous three re-viewers and associate editor for their comments and inspirationthat improved the overall quality of this work. We also thankAmanda Carr for providing illustrations. This research was fundedin part by the Leakey Foundation, Force and Motion Foundation,and National Science Foundation's Graduate Fellowship Program.

Appendix A. Supplementary Online Material

Supplementary online material related to this article can befound at https://doi.org/10.1016/j.jhevol.2019.02.001.

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