Comparison of spatiotemporal gait characteristics betweenvertical climbing and horizontal walking in primatesMichael C. Granatosky1,*, Daniel Schmitt2 and Jandy Hanna3
ABSTRACTDuring quadrupedal walking, most primates utilize diagonal-sequence diagonal-couplet gaits, large limb excursions andhindlimb-biased limb loading. These gait characteristics are thoughtto be basal to primates, but the selective pressure underlying thesegait changes remains unknown. Some researchers have examinedthese characteristics during vertical climbing and propose thatprimate quadrupedal gait characteristics may have arisen due tothe mechanical challenges of moving on vertical supports.Unfortunately, these studies are usually limited in scope and do notaccount for varying strategies based on body size or phylogeny. Here,we test the hypothesis that the spatiotemporal gait characteristicsthat are used during horizontal walking in primates are alsopresent during vertical climbing irrespective of body size andphylogeny. We examined footfall patterns, diagonality, speed andstride length in eight species of primates across a range of bodymasses. We found that, during vertical climbing, primates slow down,keep more limbs in contact with the substrate at any one time,and increase the frequency of lateral-sequence gaits compared withhorizontal walking. Taken together, these characteristics areassumed to increase stability during locomotion. Phylogeneticrelatedness and body size differences have little influence onlocomotor patterns observed across species. These data reject theidea that the suite of spatiotemporal gait features observed inprimates during horizontal walking are in some way evolutionarilylinked to selective pressures associated with mechanicalrequirements of vertical climbing. These results also highlight theimportance of behavioral flexibility for negotiating the challenges oflocomotion in an arboreal environment.
INTRODUCTIONQuadrupedal walking in primates is differentiated from that of mostmammals by a suite of features (Cartmill et al., 2002; Demes et al.,1994; Granatosky et al., 2016b; Kimura et al., 1977; Reynolds,1985; Schmitt, 1994; Schmitt and Hanna, 2004). First, primatestend to utilize diagonal-sequence footfall patterns (i.e. eachhindlimb footfall is followed by a contralateral forelimb footfall)versus lateral-sequence footfall patterns (i.e. each hindlimb footfall
is followed by an ipsilateral forelimb footfall) (Cartmill et al., 2002,2007; Hildebrand, 1967; Rollinson and Martin, 1981; Shapiro andRaichlen, 2007; Vilensky and Larson, 1989). Second, quadrupedalprimates exhibit relatively larger limb excursions, resulting inrelatively long stride distances (Larson et al., 2000, 2001; Schmitt,1998). Finally, most primates exhibit functional differentiationbetween the forelimbs and hindlimbs, where the hindlimb serves asthe primary support and propulsive limb (Demes et al., 1994;Granatosky et al., 2018a; Hanna et al., 2017; Kimura et al., 1977;Schmitt and Hanna, 2004; Schmitt and Lemelin, 2002). It remainsunresolved what selective factors initially drove primates to adoptthese unusual locomotor characteristics.
One scenario that has received relatively little attention is that themechanical requirements of vertical climbing may be the selectivepressure for the evolution of certain aspects of the unusual pattern ofprimate quadrupedal walking (Hanna et al., 2017; Prost andSussman, 1969; Vilensky et al., 1994). Climbing, often on verticalsupports, is a critical and fundamental form of locomotion forarboreal animals during foraging, travel, escape or finding a saferesting place. As originally reported by Prost and Sussman (1969)and Vilensky and colleagues (1994), and later supported byNyakatura et al. (2008), increasing support inclination increasesthe presence of diagonal-sequence gaits over lateral-sequence gaitsin primates. This finding led Prost and Sussman (1969) andVilensky et al. (1994) to propose that, as climbing became moreimportant to the locomotor repertoire of early primates, thefrequency of diagonal-sequence-gait utilization also increased.Those previous studies focused on increased inclination, but notpure vertical supports, which raises the question of how limb phasewill vary with a 90 deg incline. Hirasaki et al. (1993) examinedfootfall patterns in Macaca fuscata and Ateles geoffroyi, and foundthat macaques showed mostly diagonal-sequence diagonal-couplet(DSDC) gaits (and trots), whereas spider monkeys tended moretoward a pace when climbing a vertical support. Data collected byHanna and Schmitt (2011) placesMacaca fasicularis solidly in withM. fuscata in the use of DSDC gaits and trots. However, neitherstudy compared explicitly to horizontal supports, although it isknown that all three species tend to use DSDC gaits on horizontalsupports. Macaques, therefore, retain the pattern seen on thehorizontal supports while spider monkeys deviate in a directiontoward laterally coordinated limb behavior. More recently, Hannaet al. (2017) reported that, during climbing, the forelimbexperiences primarily tensile loads, while hindlimb loading isprimarily compressive and propulsive, suggesting that functionaldifferentiation of the limbs could have evolved in association withclimbing and been maintained on level surfaces.
While evidence supporting Prost and Sussman (1969) andVilensky and colleagues’ (1994) original hypothesis has beenreported in a number of studies (Hanna et al., 2017; Nyakatura andHeymann, 2010; Nyakatura et al., 2008), direct comparisonsbetween vertical climbing and horizontal walking remain scarce.Received 29 May 2018; Accepted 27 November 2018
1Department of Organismal Biology and Anatomy, University of Chicago, Chicago,IL 60631, USA. 2Evolutionary Anthropology, Duke University, Durham, NC 27708,USA. 3Biomedical Sciences, West Virginia School of Osteopathic Medicine,Lewisburg, WV 24901, USA.
Furthermore, comparisons that have been conducted between thetwo locomotor modes are usually limited in terms of species andbody size range. Therefore, this study explores spatiotemporal gaitvariables of vertical climbing and horizontal walking in nine speciesof primarily arboreal primates across a range of body masses (0.18–9.77 kg) in order to test the hypothesis that the mechanicalrequirements associated with vertical climbing may represent aselective factor in the formation of certain aspects of the unusualpattern of primate quadrupedal locomotion.In an arboreal context, gait patterns may serve as a behavioral
mechanism to enhance stability and safety (Cartmill et al., 2002,2007; Hildebrand, 1967; Preuschoft, 2002; Rollinson and Martin,1981; Shapiro and Raichlen, 2007). Habitual use of DSDC gaits iscommon among primates, some marsupials and the carnivoranPotos flavus (Cartmill et al., 2002, 2007; Granatosky et al., 2016b;Hildebrand, 1967; Karantanis et al., 2015; Schmitt and Lemelin,2002). There are two primary hypotheses for the benefits of a DSDCgait in an arboreal context. First, DSDC gaits essentially minimizethe amount of time that the limbs are arranged as a unilateral bipod(Cartmill et al., 2002; Shapiro and Raichlen, 2007). This may beespecially important for arboreal quadrupedal primates while onarboreal supports because it reduces the chances of toppling off thesupport (Cartmill et al., 2007; Shapiro and Raichlen, 2007). Thesecond explanation is based on the distinct limb-loading patternobserved in primates that essentially allows them to support themajority of their body weight on the hindlimb rather than theforelimb (Reynolds, 1985; Schmitt and Lemelin, 2002). Byadopting a DSDC walking gait, the forelimb is able to testsupports before the animal commits the majority of its body weight(Cartmill et al., 2002; Schmitt and Lemelin, 2002). If the supportshould fail due to local weakness, then the animal is able to utilizethe horizontal lever effect to quickly pitch backwards onto thehindlimb and use its grasping hindfoot to secure a grasp, therebypreventing a fall (Larson and Demes, 2011; Larson and Stern, 2009;Reynolds, 1985; Young, 2012). It should be noted that thismechanism has only been addressed thoroughly during quadrupedalwalking, and it is unclear what, if any, benefits shifting weightbackwards to the hindlimbs would have during behaviors such asclimbing, running or leaping.While these explanations have been discussed in great detail in
reference to arboreal quadrupedal walking, it is likely that DSDCgaits would not confer the same biomechanical benefits whileanimals are vertically climbing. The concern of falling forward on aflexible or failing branch articulated by Cartmill et al. (2002) is notsignificant during vertical movement, nor would hindlimbdominance be a particular advantage over forelimb dominancewere a vertical support to bend or break. With this in mind, somehave argued that lateral-sequence diagonal-couplet (LSDC) gaitspromote stability, in relation to the location of the center of mass(COM) relative to the support polygon of the limbs (Cartmill et al.,2002, 2007; Lammers and Zurcher, 2011; Rollinson and Martin,1981; Shapiro and Raichlen, 2005, 2007). Of course, the polygon ofsupport model only applies when animals are walking on ahorizontal, or at least mostly horizontal, support (Cartmill et al.,2002; Preuschoft, 2002). LSDC gaits are more often exhibited byterrestrial mammals (Cartmill et al., 2002, 2007; Hildebrand, 1967;Muybridge, 1887; Preuschoft, 2002), but are also used by somearboreal specialists, such as sugar gliders (Shapiro and Young,2010), callitrichids (Nyakatura and Heymann, 2010; Nyakaturaet al., 2008) and scansorial rodents (Schmidt and Fischer, 2010).Thus, there are no unambiguous biomechanical grounds for usingdiagonal- versus lateral-sequence gaits when climbing vertically.
Beyond specific gait patterns, animals can increase securityand stability on arboreal substrates by altering the timing atwhich the limbs come into contact with and release the support(Cartmill, 1985; Dunbar and Badam, 2000; Isler, 2004; Islerand Thorpe, 2003; Karantanis et al., 2016; Preuschoft, 2002).For animals without claws, grasping hands and feet providemuscular support that prevent toppling off or rotating aroundarboreal supports (Cartmill, 1985; Congdon and Ravosa, 2016;Lammers and Gauntner, 2008). By maintaining longer contacttimes, animals are able to increase security and stability byassuring that they always have a powerful grasping hand or footin contact with the support to prevent falling (Cartmill et al.,2002; Karantanis et al., 2015; Patel et al., 2015) and increasethe total number of limbs in contact with the support at any onetime, resulting in a more stable base throughout the stride(Cartmill et al., 2002; Isler and Thorpe, 2003; Shapiro andRaichlen, 2007).
Although cost of transport is not measured in this study, somemight argue, based on studies of horizontal locomotion, that costsof force production would vary with stride length and contact timeduring climbing (Kram and Taylor, 1990; Pontzer, 2007a,b;Roberts et al., 1998). However, climbing costs do not appear to beassociated with changes in step length relative to horizontallocomotion (Hanna and Schmitt, 2011). This is likely because themetabolic cost of climbing by primates can be primarily explainedby the cost of performing muscular work against gravity, ratherthan the rate at which the force is produced (Hanna et al., 2008).Consequentially, vertical climbing results in relatively greaterenergetic costs compared with horizontal walking in primates atbody sizes greater than 1 kg (Hanna et al., 2008). One strategy thatlarge-bodied primates could theoretically use to reduce energeticcosts of vertical climbing would be to increase step distancecompared with horizontal walking. Thus, we were interested inhow stride length varied with climbing in awide sample of species,in respect to both climbing mechanics and energetic costs. It isworth noting in this context that primates typically take longerstrides compared with non-primate species during horizontallocomotion (Alexander and Maloiy, 1984; Larson et al., 2000),and some data (Nyakatura et al., 2008) suggest that, during verticalclimbing, primates may increase stride length even more so than inhorizontal locomotion. Therefore, this study specifically examinesstride length in climbing.
In this study, we have two primary goals: (1) to assessspatiotemporal patterns of vertical climbing in primates across arange of body sizes to determine general trends across species; and(2) to compare spatiotemporal patterns of vertical climbing tohorizontal walking to assess the hypothesis that selective pressuresassociated with vertical climbing may be responsible for certainaspects of the unusual pattern of primate quadrupedal walkingmechanics. To focus investigation, we will test the followinghypotheses:
Hypothesis 1: diagonal-sequences gaits are the most commonlyobserved gait type for primates during horizontal walking andvertical climbing, and are not affected by variation in body massbetween species.
Hypothesis 2: hindlimb and forelimb relative support durationand speed of movement are similar during vertical climbing andhorizontal walking, and are not affected by variation in body massbetween species.
Hypothesis 3: stride length, and the tendency to modulate it, aresimilar during vertical climbing and horizontal walking, and are notaffected by variation in body mass between species.
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RESEARCH ARTICLE Journal of Experimental Biology (2019) 222, jeb185702. doi:10.1242/jeb.185702
Journal
ofEx
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iology
MATERIALS AND METHODSSubjectsAdult Loris tardigradus (Linnaeus 1758), Nycticebus pygmaeusBonhote 1907, Cheirogaleus medius Geoffroy 1812, Eulemurmongoz Linnaeus 1766, Daubentonia madagascariensis Gmelin1788, Saimiri sciureus (Linnaeus 1758),Macaca fascicularis Raffles1821, Aotus nancymaae Hershkovitz 1983 and Aotus azarae(Humboldt 1811) were used in this study (Table S1). All speciesare primarily arboreal and commonly use both arboreal horizontalwalking and vertical climbing as part of their normal locomotorrepertoires (Cant, 1988; Curtis and Feistner, 1994; Fleagle, 2013;Fleagle and Mittermeier, 1980; Gebo, 1987; Glassman and Wells,1984; Goodenberger et al., 2015; Nekaris, 2001). All data wereobtained from animals housed at the Duke Lemur Center and DukeUniversity Vivarium (Durham, NC, USA), Monkey Jungle (Miami,FL, USA), Stony Brook University (Stony Brook, NY, USA), andMichale E. Keeling Center (Bastrop, TX, USA).
ProceduresAll procedures were approved by the appropriate InstitutionalAnimal Care and Use Committee (IACUC;West Virginia School ofOsteopathic Medicine: 2007-1, 2008-1, 2009-4; Duke University:A104-09-03; A130-07-05, A270-11-10; State University ofNew York: 91-94-0131). The data collection procedures havebeen described extensively elsewhere (Granatosky, 2018a;
Granatosky et al., 2016a, 2018; Hanna et al., 2017) and will besimply summarized here. Subjects were encouraged by food rewardto climb a pole attached to a wall (climbing trials) or the ground(walking trials). The pole varied in diameter between 1.27 and3.81 cm (Table S1). Pole diameters were chosen on the basis ofpreviously published studies (Granatosky et al., 2016a; Hanna et al.,2017), which generally attempt to use the smallest pole the animalswill utilize (Schmitt and Hanna, 2004). As the animals moved up/across the pole, they were video recorded (A601f; Basler AG,Ahrensburg, Germany, Sony Handycam, or GoPro Hero3+) at60–120 frames per second [see Granatosky et al. (2016a) forinformation on data collection with GoPro cameras]. Only trials inwhich the animal was traveling in a straight path and not acceleratingor decelerating (i.e. steady-state locomotion) throughout theclimbing or walking trial, in which a full forelimb and/orhindlimb contacted the pole, and which exhibited a symmetricfootfall sequencewere retained for analysis. For all data, steady-statelocomotion was determined by a combination of video, force andsymmetry data following previously established methods (Byronet al., 2017; Granatosky et al., 2016a, 2018a; Hanna et al., 2017).For all trials, symmetry was determined using the methods ofCartmill et al. (2002), with a ±10 criterion such that the timing ofopposite limb touchdown could vary between 40 and 60% of thestride cycle (50% indicates the timing of opposing limbs is exactly1/2 of the cycle).
Macaca fascicularis
Saimiri sciureus
Aotus sp.
Eulemur mongoz
Cheirogaleus medius
Daubentonia madagascariensis
Nycticebus pygmaeus
Loris tardigradus
0.19 7.33Average body mass (kg)
Fig. 1. Average body mass plotted onto the phylogeny for the primate species used in this study. The cladogram is assembled by pruning a recentsupertree (Hedges et al., 2015) to include only the species in our study.
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RESEARCH ARTICLE Journal of Experimental Biology (2019) 222, jeb185702. doi:10.1242/jeb.185702
Data processingFor single-camera recordings, calibration for distance was performedby using a known length in the view of the camera in the same plane asthe animal was moving. For data collected with two cameras (i.e. allvertical climbing data and horizontal walking data on L. tardigradus,C. medius, N. pygmaeus, A. azarae and E. mongoz), calibration wasaccomplished with a three-dimensional (3D) cube with knowncorners. Speed was determined from this calibration as the averagevelocity of the animal over the view of the camera, by the 3D positionof the head marker from the initial view in the cameras to the lastview in the camera [seeHanna andSchmitt (2011),Hanna et al. (2008)and Hanna et al. (2017) for details]. For data collected from asingle laterally positioned camera (i.e. horizontal walking data onD. madagascariensis, S. sciureus,M. fascicularis and A. nancymaae),the subject’s speedwas calculated by digitizing a point on the subject’shead over the entire stride based on a known distance on the runway[see Granatosky (2018a), Granatosky et al. (2016a) and Granatoskyet al. (2018) for details]. From video recordings, we considereddiagonality, gait type, percentage of limb support, stride duration,forelimb and hindlimb duty factor, stride length, speed, and stridefrequency (see Table S2 for information about variables). As some ofthese parameters are size dependent, we used the hindlimb length tocalculate the dimensionlessmeasures of stride length, speed, and stridefrequency. Hindlimb length was collected fromD. madagascariensis,S. sciureus, M. fascicularis and A. nancymaae while animals wereanesthetized. Hindlimb length from the remaining species weremeasured from space-calibrated video recordings.Due to low sample sizes, A. nancymaae and A. azarae were
grouped together and analyzed as Aotus sp.We tested for statisticallysignificant differences in the utilization of gait types and percentageof limb support between horizontal and vertical arboreal locomotionusing a χ2 test. We used a series of Mann–Whitney U-tests todetermine whether diagonality, dimensionless speed, dimensionlessstride length, and forelimb and hindlimb duty factor variedsignificantly between horizontal and vertical arboreal locomotion.Regression models were constructed to examine the impact of bothstride frequency and stride length on speed using their dimensionlesscounterparts. The impact of each parameter was compared using aFisher r-to-z transformation to test significance of the differencebetween two correlation coefficients. No statistical comparisons wereconducted on untransformed speed, stride frequency, stride durationor stride length between the two conditions, but means and standarddeviations are still reported as untransformed data.This study used a series of regression analyses to assess the
effects that variation in body masses between species may have onspatiotemporal gait variables (i.e. diagonality, forelimb andhindlimb duty factor, dimensionless stride length, speed, andstride frequency, and the correlation coefficients for dimensionlessspeed as a function of dimensionless stride length and stridefrequency) during horizontal walking and vertical climbing. Assome evidence suggests that branch diameter may influence gaitpatterns in primates (Stevens, 2008), an additional series ofregression analyses were used to assess the effects that variationin relative branch diameter [i.e. branch diameter/body mass1/3; seeStevens (2008)] may have on spatiotemporal gait variables duringhorizontal walking and vertical climbing. As phylogenetic historymay be an additional and relevant confounding factor on theassociation between spatiotemporal gait variables and body massand relative branch diameter, phylogenetically independentcontrasts were used for all intraspecific regression analyses. Thelogarithmic transformation of all variables was used for all analyses.All phylogeny-based analyses were performed in R (Ver. 3.4.2) Ta
ble1.
Sum
marystatistic
sfortheva
riab
lesof
interest
during
horizo
ntal
walking
andve
rtical
clim
bing
Spe
cies
Orie
ntation
NSpe
ed(m
s−1)
Dim
ension
less
spee
dForelim
bdu
tyfactor
Hindlim
bdu
tyfactor
Diago
nality
Stride
time(s)
Stridefreq
uenc
y(strides
s−1)
Dim
ension
less
strid
efreq
uenc
yStride
leng
th(m
)Dim
ension
less
strid
eleng
th
Loris
tardigradu
sHorizon
tal
330.37
±0.18
0.33
±0.16
0.66
±0.13
0.52
±0.07
0.56
±0.04
0.95
±0.36
1.22
±0.50
0.14
±0.06
0.30
±0.04
2.28
±0.33
Vertical
390.28
±0.18
0.25
±0.16
0.63
±0.07
0.59
±0.06
0.47
±0.07
1.49
±0.96
0.97
±0.56
0.11
±0.07
0.29
±0.06
2.16
±0.44
Che
iroga
leus
med
ius
Horizon
tal
320.59
±0.16
0.64
±0.17
0.51
±0.10
0.55
±0.08
0.55
±0.07
0.30
±0.08
3.49
±0.78
0.33
±0.07
0.17
±0.04
1.98
±0.44
Vertical
600.43
±0.22
0.47
±0.25
0.63
±0.11
0.62
±0.08
0.41
±0.14
0.49
±0.20
2.41
±0.97
0.22
±0.09
0.17
±0.03
2.02
±0.44
Nycticeb
uspy
gmae
usHorizon
tal
220.48
±0.20
0.45
±0.20
0.60
±0.09
0.54
±0.04
0.56
±0.10
0.78
±0.26
1.42
±0.44
0.16
±0.05
0.33
±0.06
2.79
±0.57
Vertical
760.28
±0.14
0.27
±0.14
0.60
±0.08
0.57
±0.08
0.48
±0.09
1.14
±0.59
1.10
±0.50
0.12
±0.05
0.25
±0.03
2.19
±0.33
Saimiri
sciureus
Horizon
tal
980.58
±0.13
0.40
±0.08
0.46
±0.10
0.54
±0.10
0.59
±0.20
0.48
±0.11
2.20
±0.45
0.33
±0.07
0.27
±0.07
1.25
±0.33
Vertical
251.03
±0.31
0.69
±0.21
0.61
±0.13
0.52
±0.10
0.55
±0.21
0.48
±0.13
2.23
±0.59
0.34
±0.09
0.46
±0.08
2.05
±0.36
Aotus
sp.
Horizon
tal
450.63
±0.14
0.40
±0.09
0.57
±0.10
0.60
±0.08
0.58
±0.08
1.10
±0.33
0.99
±0.31
0.16
±0.05
0.68
±0.20
2.68
±0.76
Vertical
300.49
±0.10
0.32
±0.07
0.62
±0.11
0.64
±0.07
0.44
±0.11
0.73
±0.18
1.44
±0.31
0.22
±0.04
0.35
±0.10
1.49
±0.39
Eulem
urmon
goz
Horizon
tal
290.96
±0.30
0.52
±0.16
0.51
±0.08
0.54
±0.08
0.62
±0.05
0.61
±0.16
1.77
±0.50
0.34
±0.10
0.54
±0.11
1.54
±0.34
Vertical
104
0.89
±0.25
0.47
±0.13
0.59
±0.09
0.48
±0.07
0.58
±0.10
0.57
±0.10
1.82
±0.36
0.35
±0.07
0.48
±0.07
1.35
±0.19
Dau
benton
iamad
agas
carie
nsis
Horizon
tal
500.66
±0.21
0.35
±0.11
0.51
±0.06
0.57
±0.04
0.66
±0.04
0.94
±0.25
1.13
±0.25
0.22
±0.05
0.59
±0.11
1.58
±0.30
Vertical
340.53
±0.25
0.28
±0.14
0.62
±0.08
0.67
±0.05
0.55
±0.11
1.25
±0.32
0.86
±0.28
0.17
±0.05
0.61
±0.10
1.68
±0.29
Mac
acafascicularis
Horizon
tal
601.00
±0.26
0.45
±0.12
0.62
±0.09
0.59
±0.06
0.64
±0.07
0.89
±0.13
1.15
±0.18
0.26
±0.04
0.86
±0.15
1.76
±0.31
Vertical
430.74
±0.25
0.33
±0.11
0.62
±0.10
0.64
±0.07
0.43
±0.12
0.92
±0.17
1.12
±0.20
0.25
±0.04
0.66
±0.24
1.32
±0.48
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RESEARCH ARTICLE Journal of Experimental Biology (2019) 222, jeb185702. doi:10.1242/jeb.185702
using phytools (Revell, 2012), ape (Paradis et al., 2004), nlme(https://CRAN.R-project.org/package=nlme) and geiger (Harmonet al., 2007). For all phylogenetic analyses, the phylogeny wasconstructed by pruning a recent super timetree (Hedges et al., 2015)to include only the species in our study (Fig. 1).
RESULTSThe sample consisted of 780 strides. Summary statistics for thevariables of interest are presented in Table 1. Frequency data for thegait type and percentage of limb support are presented in Tables 2and 3, respectively.For almost all species, diagonality was significantly lower during
vertical climbing compared with horizontal walking (P≤0.033;Table 1 and Figs 2 and 3). Only S. sciureus (hereafter referred to asSaimiri) demonstrated similar diagonality between the twolocomotor modes (P=0.254). Accordingly, this drop indiagonality was associated with a significant increase in walkingtrots and LSDC gaits for all species except Saimiri (Table 2).Patterns of forelimb and hindlimb duty factor between the two
locomotor modes also revealed significant differences for mostcomparisons, although the direction of the effects were lessconsistent (Fig. 4). As with diagonality, there was no significant
difference (P=0.452) in hindlimb duty factor observed in Saimiribetween vertical climbing and horizontal walking. Forelimb dutyfactor was significantly (P≤0.041) lower during horizontal walkingcompared with vertical climbing for almost all species exceptL. tardigradus (hereafter referred to as Loris),N. pygmaeus (hereafterreferred to asNycticebus) andM. fascicularis (hereafter referred to asMacaca). For these taxa, no significant differences (P≥0.289) wereobserved. Hindlimb duty factor was significantly (P<0.001) lowerfor E. mongoz (hereafter referred to as Eulemur) during verticalclimbing, but all other species demonstrated significantly lowerhindlimb duty factors during horizontal walking (P≤0.044).
When comparing limb support patterns between horizontalwalking and vertical climbing, it is clear that supporting the bodywith two contralaterally positioned limbs is the most commonarrangement for both locomotor modes. This is followed by havingthree limbs in contact with the support, followed by supporting thebody as pair of ipsilateral couplets. For half of the species [Loris;Nycticebus; A. nancymaae and A. azarae (hereafter referred tocollectively as Aotus); and Eulemur], no significant differenceswere observed between the frequency of limb support patternsbetween horizontal walking and vertical climbing. For the other halfof the sample, the proportion of stride that had all four limbs in
Table 2. Percentage of each gait type used during horizontal walking and vertical climbing
Species Orientation N PaceLateral sequencelateral couplet
contact with the support increased during vertical climbing.Additionally, C. medius (hereafter referred to as Cheirogaleus),Saimiri and D. madagascariensis (hereafter referred to as
Daubentonia) exhibited an increased proportion of the stride thathad all three limbs in contact with the support during verticalclimbing. In contrast,Macaca demonstrated a decrease in three-limb
1.0 A B
C D
E F
G H
Loris Cheirogaleus
Nycticebus Saimiri
Aotus Eulemur
Daubentonia Macaca
0.8
0.6
0.4
Dia
gona
lity
0.2
0
1.0
0.8
0.6
0.4
0.2
0
1.0
0.8
0.6
0.4
0.2
0
1.0
0.8
0.6
0.4
0.2
0
1.0
0.8
0.6
0.4
0.2
0
1.0
0.8
0.6
0.4
0.2
0
1.0
0.8
0.6
0.4
0.2
0
1.0
0.8
0.6
0.4
0.2
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Fig. 2. ‘Hildebrand’ plots displaying diagonalityagainst hindlimb duty factor collected duringhorizontal walking and vertical climbing. Values forhorizontal walking (‘H’) are shown in white and verticalclimbing (‘V’) in gray. Species are displayed in order ofincreasing body mass: (A) Loris tardigradus (NH=33strides; NV=39 strides); (B) Cheirogaleus medius(NH=32 strides; NV=60 strides); (C) Nycticebuspygmaeus (NH=22 strides; NV=76 strides); (D) Saimirisciureus (NH=98 strides; NV=25 strides); (E) Aotus sp.(NH=45 strides; NV=30 strides); (F) Eulemur mongoz(NH=29 strides; NV=104 strides); (G) Daubentoniamadagascariensis (NH=50 strides; NV=34 strides); and(H)Macaca fascicularis (NH=60 strides;NV=43 strides).
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contact and a rise in diagonal-couplet support when climbingvertical supports (Table 3).For most species, dimensionless speed tended to be significantly
(P≤0.034) lower during vertical climbing compared with horizontalwalking (Fig. 5A). There was no significant difference (P=0.163) indimensionless speed observed in Eulemur between verticalclimbing and horizontal walking. Dimensionless stride lengthfollowed a similar pattern. For most species, dimensionless stridelength tended to be significantly (P≤0.001) lower during verticalclimbing compared with horizontal walking. The opposite patternwas observed in Saimiri (P<0.001). There was no significantdifference (P≥0.133) in dimensionless stride length observed inLoris, Cheirogaleus or Daubentonia between vertical climbing andhorizontal walking (Fig. 5B).The construction of a stepwise regression model on the effects of
dimensionless stride frequency and length on dimensionless speed(Figs S1 and S2) showed varying relationships across species. Forall species except Aotus, both dimensionless stride frequency andlength had a significant relationship on dimensionless speed.
During horizontal walking in Aotus, dimensionless stride frequencyhad a significant relationship with dimensionless speed, butdimensionless stride length did not. However, during verticalclimbing for this species, the opposite pattern was observed. Amongthe other species, four different solutions to modulation of speedduring vertical movement were detected (see Tables S3 and S4 forcorrelation coefficients and P-values). Cheirogaleus, Nycticebus,Saimiri and Daubentonia exhibited a strong correlation betweenspeed and stride frequency during climbing, whereas each of theother species exhibited differing relationships between speed, stridefrequency and stride length.
Overall, the phylogenetic signals in the variables analyzed (i.e.diagonality, forelimb and hindlimb duty factor, dimensionless stridelength, speed, and stride frequency, and correlation coefficients fordimensionless speed as a function of dimensionless stride lengthand stride frequency) were low in the sample species during bothhorizontal walking and vertical climbing, and were not significantlydifferent (Blomberg’s K≤1.04, P≥0.094; Pagel’s λ≤0.838,P≥0.079). Phylogenetically independent contrasts revealed nosignificant relationships between body mass or relative supportsize and any of the variables analyzed, with the exception ofdiagonality, which had a significant (P=0.01) positive relationship(y=0.0752x+0.0008) with body mass during horizontal walking(see Table S5 for correlation coefficients and P-values).
DISCUSSIONThe data presented here show that vertical climbing in primates doesnot demonstrate the same patterns observed during horizontalarboreal walking. Vertical climbing in primates is characterized bydecreased diagonality and an increase in trots and lateral-sequencegaits, compared with horizontal walking. Furthermore, on verticalsupports, the animals usually moved more slowly, with longerintervals of grasping the support. In the majority of the species,speed was regulated primarily by stride frequency, while stridelength had a secondary, but often significant, effect. Beyond thesevariables, patterns were inconsistent across species, andphylogenetic and size-related patterns were not observed.
In almost all of the species analyzed, diagonality decreasedduring vertical climbing and, as a consequence, the proportion ofwalking trots and LSDC gaits increased. So what drives footfallsequence during vertical climbing?We believe that there are notablebiomechanical advantages to switching from primarily DSDC gaitsduring horizontal walking to trots and LSDC gaits during verticalclimbing. As originally modeled by Preuschoft (2002), on verticalsubstrates the animal must grasp the support either superior orinferior to the COM in at least one of its limbs, otherwise the animalis faced with a situation where it must use large muscularcontractions to counteract the rotational torques acting on theCOM due to gravity (Cartmill, 1985; Preuschoft, 2002). DuringDSDC gaits, positioning of the limbs means that there is a portion ofthe stride where the animal is supporting body mass on two feetplaced close together near the COM (Cartmill et al., 2002, 2007;Shapiro and Raichlen, 2007). There are a number of strategies thatanimals can use to prevent this situation, including increasing dutyfactor so that more limbs are in contact with the support at any onetime (i.e. three- and four-limb support), or by adopting LSDC gaits,which effectively eliminates moments where body support is solelydependent on two feet placed close together near the COM (Cartmillet al., 2007; Shapiro and Raichlen, 2007). Our data suggest thatprimates employ both strategies during vertical climbing.
The continued presence of DSDC gaits (albeit with lowerdiagonality and thus closer to walking trots) may be explained by a
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Fig. 3. Mean diagonality collected during horizontal walking and verticalclimbing for eight species of primate. Values for horizontal walking (‘H’) areshown in white and vertical climbing (‘V’) in gray. Species are displayed in orderof increasing body mass: Loris tardigradus (NH=33 strides; NV=39 strides);Cheirogaleus medius (NH=32 strides; NV=60 strides); Nycticebus pygmaeus(NH=22 strides; NV=76 strides); Saimiri sciureus (NH=98 strides; NV=25strides); Aotus sp. (NH=45 strides; NV=30 strides); Eulemur mongoz (NH=29strides; NV=104 strides); Daubentonia madagascariensis (NH=50 strides;NV=34 strides); and Macaca fascicularis (NH=60 strides; NV=43 strides).Vertical bar represents one s.d. Based on intraspecific Mann–WhitneyU-tests,diagonality was significantly lower during vertical climbing compared withhorizontal walking for almost all species (P≤0.033). Only S. sciureusdemonstrated similar diagonality between the two locomotor modes (P=0.254).
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simple retention of neuromuscular gait parameters on both horizontaland vertical substrates (Schoonaert et al., 2016; Vilensky et al., 1994).However, the ability of primates to switch easily between gait typesdepending on different conditions (Granatosky et al., 2016a; Isler,2004; Nyakatura and Heymann, 2010; Stevens, 2008) suggests thatthis is not a complete answer. Understanding the continued use ofDSDC gaits during vertical climbing remains a wide-open questionthat deserves further exploration.As mentioned above, almost all species in this study
demonstrated lower speeds during vertical climbing comparedwith horizontal walking. This follows predictions by Schmidt andFischer (2010) and Karantanis and colleagues (2015, 2016, 2017a,b,c) that, in arboreal conditions, animals may adopt slower speeds asa way to increase static stability. More interesting, however, are thestrategies used by vertically climbing primates to regulate speed. Forprimates, increasing speed by increasing stride length is possiblysafer in an arboreal setting, allowing for a longer reach of theforelimbs and reducing involuntary branch sway (Cartmill, 1985;Demes et al., 1994; Larson et al., 2000, 2001). Additionally, longerstride lengths also have energetic benefits that may be especiallyimportant during vertical climbing for large-bodied primates(Hanna et al., 2008; Karantanis et al., 2016). In our study, onlySaimiri had significantly longer stride lengths during verticalclimbing compared with horizontal walking. For the rest of thespecies, stride length during vertical climbing was either lower than,or the same as, during horizontal walking. Accordingly, almost allof the species in our study primarily regulate speed by increasing
stride frequency rather than stride length (although both factors areimportant contributors in almost all species). Similar findings havebeen reported in geckos (Zaaf et al., 2001), cotton-top tamarins(Nyakatura et al., 2008), bonobos (Schoonaert et al., 2016), acaciarats (Karantanis et al., 2017c) and feathertail gliders (Karantaniset al., 2015). The regulation of speed by stride frequency versusstride length is thought to reduce body oscillations. Duringhorizontal locomotion, dorsoventral body oscillations are directedperpendicular to the branch and in the vertical plane (Cartmill,1985; Preuschoft, 2002). There are of course horizontal (anterior–posterior) and mediolateral oscillations of the COM as well, but theyare both smaller. During vertical climbing, much of the oscillationsare parallel to the substrate (Cartmill, 1985; Preuschoft, 2002). Onthin, arboreal substrates, body oscillations may cause substrateoscillations. Therefore, reducing body oscillations during arboreallocomotion (horizontally or vertically oriented) may increasearboreal stability (Delciellos and Vieira, 2007; Karantanis et al.,2015, 2017c; Strang and Steudel, 1990). With this in mind, it ispossible that the need to maximize stride length during verticalclimbing may be less important than previously thought.
Evolutionary implicationsOne of the major goals of this study was to test the hypothesis that theunusual spatiotemporal gait characteristics observed duringhorizontal walking in primates are present because of the effect ofusing these characteristics during vertical climbing. This argument isbased on previous studies showing an increase in diagonal-sequence
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Fig. 4. Mean forelimb and hindlimb duty factor collected during horizontal walking (white) and vertical climbing (gray) for eight species of primate.Meanforelimb (A) and hindlimb (B) duty factor values for horizontal walking (‘H’) are shown in white and vertical climbing (‘V’) in gray. Species are displayed in order ofincreasing body mass: Loris tardigradus (NH=33 strides; NV=39 strides); Cheirogaleus medius (NH=32 strides; NV=60 strides); Nycticebus pygmaeus (NH=22strides;NV=76 strides);Saimiri sciureus (NH=98 strides;NV=25 strides);Aotus sp. (NH=45 strides;NV=30 strides);Eulemurmongoz (NH=29 strides;NV=104 strides);Daubentonia madagascariensis (NH=50 strides; NV=34 strides); and Macaca fascicularis (NH=60 strides; NV=43 strides). Vertical bar represents one s.d.Based on intraspecific Mann–Whitney U-tests, forelimb duty factor was significantly (P≤0.041) lower during horizontal walking compared with vertical climbing foralmost all species except Loris, Nycticebus andMacaca. For these taxa, no significant differences (P≥0.289) were observed. Hindlimb duty factor was significantly(P<0.001) lower for Eulemur during vertical climbing, and there was no significant difference (P=0.452) in hindlimb duty factor observed in Saimiri between verticalclimbing and horizontal walking. All other species demonstrated significantly lower hindlimb duty factors during horizontal walking (P≤0.044).
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gaits on inclined supports (Prost and Sussman, 1969; Vilensky et al.,1994), and on recent suggestions by Hanna et al. (2017) that limb-loading patterns that characterize primates may have arisen inassociation with vertical climbing rather than horizontal locomotion.However, in regards to spatiotemporal patterns, the data presentedhere show that many of the gait characteristics observed duringvertical climbing in primates are quite similar to the patterns observedduring quadrupedal locomotion in non-primate mammals (Demeset al., 1994; Hildebrand, 1967; Muybridge, 1887; Rollinson andMartin, 1981; Schmitt and Lemelin, 2002). During vertical climbing,primates appear to select gaits that maximize security and stability.LSDC gaits, increased duty factor, decreased speed, and theregulation of speed through stride frequency are all ways that ananimal can increase stability on a vertical support (Cartmill, 1985;Karantanis et al., 2015, 2017c; Shapiro and Raichlen, 2007; Strangand Steudel, 1990). Vilensky and Larson (1989) emphasizedbehavioral flexibility – the ability to alter gait characteristicsdepending on environmental challenges – as an important featureassociated with primate origins. This flexibility may have beenessential to invasion and occupation of an arboreal, fine-branch nicheby the earliest primates as it allowed successful movement on bothvertical and horizontal substrates (Cartmill, 1992; Jenkins, 1974).Recent evidence, however, suggests that movement on arborealsubstrates requires all mammals, regardless of taxonomic affiliation,to demonstrate high behavioral flexibility (Granatosky, 2018b).
ConclusionsThese data reject the idea that the suite of spatiotemporal gait featuresobserved in primates during horizontal walking are in some waylinked to selective pressures associated with mechanical requirementsof vertical climbing. Instead, the use of different gait characteristicsduring climbing and horizontal movement emphasizes the innateflexibility of arboreal mammals to adjust spatiotemporal variables tomeet different substrate needs. Although these data do not definitivelyaddress the selective pressures leading to the evolution of DSDCgaits, functional differentiation of the limbs, or large limb excursions,they certainly provide for a broader discussion of the implications ofthese gaits in different environments. In short, primates do not simplyuse the same motor program for all surfaces. They differ inspatiotemporal gait characteristics on the ground, on horizontalsupports and on vertical supports. The data presented here, inconjunction with previous studies on primates (Granatosky, 2018b;Granatosky et al., 2016a; Isler, 2004; Nyakatura and Heymann, 2010;Stevens, 2008) and non-primate mammals (Granatosky, 2018b;Karantanis et al., 2015, 2017a,b,c; Shapiro and Young, 2010),highlight the importance of behavioral flexibility for mammals toeffectively traverse a complex, 3D arboreal environment.
AcknowledgementsWe thank Erin Ehmke, David Brewer and Meg Dye at the Duke Lemur Center forall their help with animal training and data collection. Without their help, we wouldnot have been able to complete this study. We thank Andrew A. Biewener and the
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Fig. 5. Mean dimensionless speed and dimensionless stride length collected during horizontal walking and vertical climbing for eight species ofprimate. Mean dimensionless speed (A) and dimensionless stride length (B) values for horizontal walking (‘H’) are shown in white and vertical climbing (‘V’) ingray. Species are displayed in order of increasing body mass: Loris tardigradus (NH=33 strides; NV=39 strides); Cheirogaleus medius (NH=32 strides; NV=60strides); Nycticebus pygmaeus (NH=22 strides; NV=76 strides); Saimiri sciureus (NH=98 strides; NV=25 strides); Aotus sp. (NH=45 strides; NV=30 strides);Eulemur mongoz (NH=29 strides; NV=104 strides); Daubentonia madagascariensis (NH=50 strides; NV=34 strides); and Macaca fascicularis (NH=60 strides;NV=43 strides). Vertical bar represents one s.d. Based on intraspecific Mann–Whitney U-tests, dimensionless speed tended to be significantly lower duringvertical climbing compared with horizontal walking for most species (P≤0.034). There was no significant difference in dimensionless speed observed in Eulemurbetween the two locomotor modes (P=0.163). Dimensionless stride length tended to be significantly lower during vertical climbing compared with horizontalwalking for most species (P≤0.001). The opposite pattern was observed in Saimiri (P<0.001). There was no significant difference (P≥0.133) in dimensionlessstride length observed in Loris, Cheirogaleus or Daubentonia between the two locomotor modes.
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two anonymous reviewers for their comments and inspiration that improved theoverall quality of this work.
Competing interestsThe authors declare no competing or financial interests.
FundingThis research was funded in part by the Leakey Foundation, Force and MotionFoundation and the National Science Foundation’s Graduate Research FellowshipProgram.
Supplementary informationSupplementary information available online athttp://jeb.biologists.org/lookup/doi/10.1242/jeb.185702.supplemental
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RESEARCH ARTICLE Journal of Experimental Biology (2019) 222, jeb185702. doi:10.1242/jeb.185702
