AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 141:222–234 (2010)
The Interplay Between Speed, Kinetics, and Hand Postures During Primate Terrestrial Locomotion Biren A. Patel* Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-8081 KEY WORDS
cercopithecoid; hand; digitigrade; palmigrade; terrestrial
ABSTRACT Nonprimate terrestrial mammals may use digitigrade postures to help moderate distal limb joint moments and metapodial stresses that may arise during high-speed locomotion with high-ground reaction forces (GRF). This study evaluates the relationships between speed, GRFs, and distal forelimb kinematics in order to evaluate if primates also adopt digitigrade hand postures during terrestrial locomotion for these same reasons. Three cercopithecine monkey species (Papio anubis, Macaca mulatta, Erythrocebus patas) were videotaped moving unrestrained along a horizontal runway instrumented with a force platform. Three-dimensional forelimb kinematics and GRFs were measured when the vertical force component reached its peak. Hand posture was measured as the angle between the metacarpal segment and the ground (MGA). As predicted, digitigrade hand postures (larger MGA) are associated with shorter
GRF moment arms and lower wrist joint moments. Contrary to expectations, individuals used more palmigradelike (i.e. less digitigrade) hand postures (smaller MGA) when the forelimb was subjected to higher forces (at faster speeds) resulting in potentially larger wrist joint moments. Accordingly, these primates may not use their ability to alter their hand postures to reduce rising joint moments at faster speeds. Digitigrady at slow speeds may improve the mechanical advantage of antigravity muscles crossing the wrist joint. At faster speeds, greater palmigrady is likely caused by joint collapse, but this posture may be suited to distribute higher GRFs over a larger surface area to lower stresses throughout the hand. Thus, a digitigrade hand posture is not a cursorial (i.e. high speed) adaptation in primates and differs from that of other mammals. Am J Phys Anthropol 141:222–234, 2010. V 2009 Wiley-Liss, Inc.
Animals that use digitigrade hand postures walk and run with their metacarpals elevated off the ground and have wrist joints that are more flexed (i.e. less dorsiflexed) than those animals that use palmigrade hand postures. Digitigrade postures are characteristic of many terrestrial animals and are most often associated with those that have the ability to move at high speeds (Howell, 1944; Gambaryan, 1974; Coombs, 1978; Hildebrand and Goslow, 2001). The reasons for adopting digitigrade posture, however, are not necessarily equivalent for all animals, and it is not yet clear why such postures evolved numerous times in different vertebrate groups. A reason for this confusion is the large amount of inter- and intraspecific variation, as well as differences within individuals, in distal limb posture use (Gregory, 1912; Howell, 1944; Gambaryan, 1974; Coombs, 1978; Hildebrand, 1985; Carrano, 1997; Fieler and Jayne, 1998). This is particularly evident among digitigrade quadrupedal primates (Rawlins, 1993; Patel, 2008, 2009). Several large-bodied cercopithecine primates habitually adopt digitigrade hand postures during terrestrial locomotion. These include baboons (Papio), geladas (Theropithecus), mandrills (Mandrillus), some macaques (Macaca) and mangabeys (Cercocebus), patas (Erythrocebus), and possibly vervets (Chlorocebus) (Bishop, 1964; Jolly, 1967; Napier and Napier, 1967; Tuttle, 1969; Rose, 1973; Rollinson and Martin, 1981; Nengo, 1993; Rawlins, 1993; Whitehead, 1993; Hayama et al., 1994; Schmitt, 1994, 1995; Richmond, 1998; Zeininger et al., 2007; Patel, 2008, 2009). One important distinction between nonprimate digitigrade animals and these habitually digitigrade monkeys is that monkeys are also capable of using palmigrade hand postures on the ground in different situations (Rawlins, 1993; Hayama et al., 1994;
Patel, 2008, 2009). Therefore, the context in which these primates use digitigrade hand postures during terrestrial locomotion differs from that of other habitually digitigrade animals and is likely due to different biomechanical factors. It is often accepted that the biomechanics of digitigrade postures in terrestrial monkeys is functionally convergent with digitigrady seen in typical cursorial animals.1 As a component of cursorial locomotion, several functional proposals have been offered to explain the biomechanical advantages of adopting digitigrade distal limb postures during quadrupedal locomotion. One proposal for adopting digitigrade postures, following work by Gray (1968) and Biewener (e.g., 1983, 1989), suggests
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WILEY-LISS, INC.
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1 There are several definitions of cursoriality in the literature (Howell, 1944; Jenkins, 1971; Coombs, 1978; Stein and Casinos, 1997; Carrano, 1999), but for the purposes of this paper, a cursorial animal is one that travels fast on the ground (Hildebrand, 1985).
Additional Supporting Information may be found in the online version of this article. Grant sponsor: National Science Foundation; Grant numbers: BCS 0524988, BCS 0509190, BCS 0548892. *Correspondence to: Biren A. Patel, Department of Anatomical Sciences, Health Sciences Center, Tower A, 8th Floor, Stony Brook University, Stony Brook, NY 11794-8081, USA. E-mail:
[email protected] Received 20 January 2009; accepted 10 June 2009 DOI 10.1002/ajpa.21138 Published online 28 July 2009 in Wiley InterScience (www.interscience.wiley.com).
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PRIMATE DIGITIGRADY that digitigrady may be a component of an extended limb posture, which may help attenuate the negative effects of higher ground reaction forces (GRF) imposed on the musculoskeletal system during high-speed locomotion. High-speed locomotion is associated with greater peak reaction forces (Rubin and Lanyon, 1982; Biewener, 1983, 1989; Miller, 1990; Demes et al., 1994; Polk, 2001, 2002), which, in turn, induces higher levels of strain in long bones, especially in larger bodied animals (Rubin and Lanyon, 1982; Biewener, 1983; Biewener and Taylor, 1986; Demes et al., 2001). Although peak stress and therefore strains can be lowered with an increase in duty factor (Alexander et al., 1977) or by limiting peak locomotor speeds and accelerations, high-speed locomotion is a necessity, either as a predator or to prevent being preyed upon, and these strategies may not be the option for many animals (Howell, 1944; Janis and Wilhelm, 1993; Harris and Steudel, 1997). At faster speeds, adopting a digitigrade posture would align the metacarpals with the GRF vector and would subject the metacarpals to predominately axial compression rather than bending. This has been documented in horse metapodia that are nearly vertical in orientation and experience primarily axial compression rather than bending moments (Biewener, 1991). Additionally, digitigrade postures would help moderate wrist joint moments that antigravity muscles (e.g., wrist and digital flexor muscles) must resist by shortening the moment arm between the GRF vector and the center of the wrist joint (Fig. 1; e.g., Biewener, 1983, 1989; Polk, 2002). This will ultimately reduce the mass-specific amount of muscle force needed to prevent the wrist joint from collapsing into dorsiflexion/hyper-extension (with the forearm in a pronated position) when subjected to higher forces. Consequently, individuals that generate relatively higher GRFs at higher speeds should adopt more digitigrade postures. Animals, such as cercopithecine monkeys, that are capable of using both palmigrade and digitigrade hand postures, should therefore actively change from a palmigrade to digitigrade stance as their forelimbs experience higher GRF. However, based on current available evidence, habitually digitigrade terrestrial monkeys use more palmigrade-like hand postures at higher speeds, that is, their hands become less digitigrade (Patel, 2008, 2009). Do primates become palmigrade at the expense of increasing wrist joint moments and higher metacarpal bending strains? Because the relationship between GRFs and hand kinematics has not been explored in quadrupedal primates, this study investigates the interactions between speed, kinetics, hand posture kinematics, and wrist joint moments in three cercopithecine monkey species that facultatively change between digitigrade and palmigrade hand postures during terrestrial locomotion.
MATERIALS AND METHODS Animal subjects Three closely related cercopithecine monkey species were examined in this study: the olive baboon (Papio anubis Lessen 1827), the rhesus macaque (Macaca mulatta Zimmermann 1780), and the patas monkey (Erythrocebus patas Schreber 1827). These animals were chosen, because they are among the most highly terrestrial of all Old World monkeys (Jolly, 1967; Rose, 1973; Isbell et al., 1998; Fleagle, 1999) and have been observed to facultatively use digitigrade hand postures during
Fig. 1. Illustrations of forelimbs with varying degrees of digitigrady. At equivalent magnitudes of ground reaction force (GRF), the more digitigrade hand posture with its shorter moment arm (R1) will experience lower wrist joint moments compared to the less digitigrade (i.e. more palmigrade) hand posture with its longer moment arm (R2). Filled circles represent the center of the wrist joint.
locomotion in both the wild and captivity (Napier and Napier, 1967; Tuttle, 1969; Rawlins, 1993; Schmitt, 1994, 1995; Richmond, 1998; Patel, 2008, 2009). A total of six animal subjects, two adult individuals of each species, were studied to investigate intraindividual variation in the relationships between speed, kinematic, and kinetic variables (Table 1). The animals were housed in large rooms where they were permitted to freely move on the ground and on ‘‘arboreal’’ supports between experiments. All experiments were conducted at the Stony Brook University Primate Locomotion Laboratory (Stony Brook, NY), and all protocols were approved by the Institutional Animal Care and Use Committee of Stony Brook University (Stony Brook) and Duke University (Durham, NC).
Kinematic methods Three-dimensional kinematics were collected from each animal’s forelimb using a video-based motion analysis system (Peak Performance Technologies, Englewood, American Journal of Physical Anthropology
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B.A. PATEL TABLE 1. Names of the species, sex, body mass, and number of steps analyzed for each animal subject Animal
Common name
Animal code
Sex
Body mass (kg)
Steps
Papio anubis Papio anubis Macaca mulatta Macaca mulatta Erythrocebus patas Erythrocebus patas
Olive Baboon Olive Baboon Rhesus Macaque Rhesus Macaque Patas Monkey Patas Monkey
BM BF M1 M2 PM PF
Male Female Female Female Male Female
28.0 23.1 5.8 5.25 12.9 7.3
89 114 55 50 70 59
Fig. 2. Still images showing four different camera views and marker placements in Subject M1 (from Table 1) used to obtain three-dimensional coordinates of forelimb joints.
CO) as the animal moved unrestrained through a plywood tunnel (10.5 m long 3 0.7 m wide) enclosed by clear Lexan (Polk, 2001; Patel, 2008, 2009). Four HSC180NS video cameras fitted with Cosmicar/Pentax TV Zoom (8–48 mm) lenses, shuttered at 1/2,000 s to avoid motion blur, and operating at 60 Hz, were positioned adjacent to the tunnel in lateral or oblique views (see Fig. 2). Following Polk et al. (2005), sampling at 60 Hz was deemed adequate for the animal subjects in the body size and speed ranges of this study. All video cameras and video signals were synchronized with a GL-250 time-code generator (J.C. Labs, La Honda, CA), which superimposes a time stamp onto the videos. One video camera was operated with its lens in a wide field-of-view (zoomed-out position) to measure stride length and stride duration from which speed was calculated. Stride length was measured as the horizontal displacement of the shoulder marker between two consecutive forelimb touchdown (TD) events, and stride duration was measured as the time elapsed between the same consecutive forelimb TDs. Froude numbers, v2/gh, where v is velocity, g is the gravitational constant, and h is the American Journal of Physical Anthropology
cube-root of body mass (Hof, 1996; Biewener, 2003), were calculated to standardize and compare animals of different size moving at different speeds. The cube-root of body mass was used rather than hip height, because some of the animals never stood still in front of the cameras. Both raw speeds and Froude numbers are reported. The three other video cameras were centered on the force platform (see below) and recorded a zoomed-in lateral view and two zoomed-in oblique views. These cameras were used to determine the three-dimensional (3D) coordinates of reflective joint markers attached to the shaved skin overlying bony landmarks (see Fig. 2). Reflective markers were applied to each animal while it was anesthetized with isoflurane gas. The bony landmarks include the shoulder joint (lateral-most aspect of the scapular spine), elbow joint (lateral epicondyle of the humerus), wrist joint (ulnar styloid process), and fifth metacarpophalangeal (MP) joint (distal end of the fifth metacarpal). Forearm segment length was defined as the absolute distance between the elbow and wrist joints. Metacarpal segment length was defined as the absolute
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PRIMATE DIGITIGRADY distance between the wrist and fifth MP joint. During playback of videos, the position of each marker was digitized with Peak Motus software version 2000 (Peak Performance Technologies, Englewood, CO), which derived the 3D coordinates of the markers using a direct linear transformation algorithm (Abdel-Aziz and Karara, 1971). From these coordinates, 3D joint angles were calculated at the time when the vertical component of the GRF was at its peak (PK) (see below). Wrist angle was measured on the extensor side between the forearm and metacarpal segments. Following Patel (2008, 2009), a metacarpal-ground angle (MGA) was measured as the angle between the metacarpal segment on the palmar (ventral) side and the ground. A more digitigrade posture will have a larger MGA and corresponds to more dorsiflexion (i.e. extension) at the MP joint. A less digitigrade posture (e.g., a semi-palmigrade or palmigrade posture) will have a smaller MGA.
Kinetic methods Three-dimensional GRF were obtained from force plates incorporated into the center of the plywood tunnel (see Fig. 2). Force plates with plywood cover plates were secured to the ground, and the testing surface was set flush with the runway surface. Small gaps of no more than 1.5 cm surrounded the force plate to minimize the effects of runway vibration noise. For the patas monkey and rhesus macaque experiments, a single Kistler 9281B force plate (Kistler Instruments, Amherst, NY) was used, and the analog force data were amplified with Kistler 5217 summing amplifiers. For the baboon experiments, two AMTI BP400600-1000 force plates (Advanced Mechanical Technology, Watertown, MA) were used, and the analog force data were amplified with AMTI MSA-6 amplifiers. The amplified analog signals were converted into digital signals using a SCXI-1000 A-D converter (National Instruments, Austin, TX) and recorded with LabView version 5.01 software (National Instruments) at a sampling rate of 2700 Hz. A custom-written virtual instrument (Franz et al., 2005) displayed the traces of the GRF components (vertical, fore/aft, and mediolateral) onto a computer monitor simulating a storage oscilloscope with 4 s sweeps. Each sweep was then saved as separate binary data files, each of which was composed of 10,800 data points per channel per file. The oscilloscope display and associated file information was D-A converted to a standard video signal and superimposed onto the zoomed-out camera’s video image (see above) using a WJ 45P special effects generator (Panasonic, Secaucus, NJ). This allowed the proper identification of steps and associated binary force files when the forelimb was in complete contact with the force plate (see Fig. 2). The binary files were then imported into Igor Pro 5.0 software (WaveMetrics, Lake Oswego, OR) where the forces were smoothed and graphed. Force traces were smoothed using a binomial curve fit algorithm with a window of 400; this corresponds to a lowpass filter where a binomial average mean is taken over a 0.15 s interval and replaces each data point (Franz et al., 2005; Young et al., 2007). Raw voltages were transformed into force units (Newton) using calibration factors derived from amplifier settings, and the forces were then transformed into body weight (bw) units to obtain standardized GRF values. Both raw and standardized values of GRF are reported.
Custom macros were written to export the values of the vertical, fore/aft, and mediolateral components of GRF at the time when the vertical component was at its peak (PK). Although these cercopithecine monkeys use diagonal sequence footfall patterns, which results in overlap between fore- and hind limb contacts on the force plate, accurate readings of forelimb forces at PK can still be obtained because forelimb peak vertical forces occur well before hind limb contact occurs [see also Demes et al. (2006)]. The three force components were then resolved to obtain the magnitude and direction (i.e. vector) of the three-dimensional GRF. Following convention in the primate biomechanics literature (e.g., Schmitt, 1995, 1999; Polk, 2001, 2002), the three-dimensional GRF vector was projected at the MP joint [i.e., assuming a uniform center of pressure (CoP) and location]. It should be noted, however, that it is possible for CoP to change between different hand postures or at different times during forelimb support (cf. Carrier et al., 1994). However, this method of GRF vector projection was justified for the following reasons. First, Richmond (1998) has shown that the majority of the vertical component of GRF acts on the metacarpal heads in the terrestrial digitigrade patas monkey. Second, methodological constraints with raw force acquisition prevented accurate measurement of CoP location at PK in the small hands of the animal subjects. Third, sensitivity analyses by Witte et al. (2002) demonstrated that calculations of joint moments are not significantly influenced by changes in CoP in smaller mammals (like most primate species) that adopt more crouched limb configurations. External wrist joint moments were calculated as the product between the magnitude of GRF at PK and the GRF moment arm (i.e., the perpendicular distance between the GRF vector and the wrist joint). Wrist joint moments were calculated at PK, because they are typically the highest at this point of the step (cf. Schmitt, 1999). To facilitate comparisons between individuals of different size, standardized GRF moment arm was derived by dividing the GRF moment arm length by metacarpal segment length. Also, standardized wrist joint moments were calculated as the product of the standardized GRF moment arm length and standardized GRF magnitude (bw units; see above). Both raw and standardized moments are reported.
Data analysis At least 50 steps for each animal subject at a range of speeds were analyzed for a total of 437 steps (Tables 1 and 2). Only symmetrical gaits (i.e. no gallops) were included in this study. Descriptive statistics of kinematic and kinetic variables are reported in Table 2. Pearson product-moment correlation coefficients (and significance values) were calculated between Froude number, standardized GRF, standardized wrist joint moments, and MGA. Reduced major axis (RMA) regression analysis was used to determine the RMA slopes, confidence intervals of slopes, and intercepts for each bivariate relationship. Although ordinary least squares (Model I) regressions are often used in kinematic studies, it was considered more appropriate to use RMA regressions (Model II) in this study, because all variables were subject to measurement errors, and because RMA techniques provide a superior estimate of the line summarizing the relationship between two variables (Ricker, 1984; Rayner, 1985; Sokal and Rohlf, 1995). RMA routines were performed using the American Journal of Physical Anthropology
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B.A. PATEL TABLE 2. Descriptive statistics of kinematic and kinetic variables by experimental subjecta
Variableb
BM
Speed (m/s) Median 0.72 Range 0.41–1.72 Mean 0.77 Std. Dev. 0.24 Froude number Median 0.017 Range 0.006–0.099 Mean 0.022 Std. Dev. 0.016 GRF (N) Median 126.55 Range 103.07–262.59 Mean 132.76 Std. Dev. 26.67 Std. GRF (bw) Median 0.461 Range 0.375–0.956 Mean 0.483 Std. Dev. 0.097 Wrist angle (8) Median 154.03 Range 116.26–168.05 Mean 152.09 Std. Dev. 10.33 MGA (8) Median 50.35 Range 27.18–75.21 Mean 51.60 Std. Dev. 9.60 GRF moment arm (m) Median 0.028 Range 0.014–0.051 Mean 0.028 Std. Dev. 0.008 Std. GRF moment arm Median 0.469 Range 0.219–0.830 Mean 0.475 Std. Dev. 0.140 Wrist moment (Nm) Median 3.443 Range 1.665–9.999 Mean 3.766 Std. Dev. 1.697 Std. wrist moment Median 0.216 Range 0.095–0.770 Mean 0.238 Std. Dev. 0.122 a b
BF
M1
M2
PM
PF
0.72 0.41–1.94 0.85 0.32
0.94 0.53–2.33 1.04 0.40
1.16 0.43–2.90 1.21 0.51
2.22 1.00–2.86 2.19 0.33
2.47 0.60–3.20 2.21 0.77
0.019 0.006–0.135 0.029 0.024
0.051 0.016–0.309 0.071 0.061
0.079 0.011–0.494 0.101 0.095
0.215 0.043–0.356 0.213 0.059
0.320 0.019–0.540 0.287 0.155
164.51 89.64–200.97 163.23 20.11
95.01 37.22–129.56 89.11 26.89
116.65 95.93–220.89 125.88 26.24
34.40 26.20–69.67 37.18 9.76
37.28 20.98–76.72 39.38 11.31
0.515 0.423–0.975 0.556 0.116
0.605 0.460–1.224 0.654 0.172
0.724 0.407–1.490 0.765 0.220
1.305 0.711–1.594 1.295 0.160
1.327 0.520–1.809 1.244 0.375
150.28 124.93–164.26 148.18 8.17
148.98 110.90–162.12 146.38 13.22
127.07 108.31–142.77 126.20 8.37
107.34 82.32–123.23 106.65 6.26
111.38 86.92–141.89 111.14 11.78
48.09 26.91–64.08 47.07 7.92
40.21 9.42–73.02 39.34 13.95
15.01 8.23–59.08 18.85 10.84
10.36 0.91–20.52 10.62 4.43
19.35 0.39–54.79 22.98 12.65
0.024 0.013–0.039 0.025 0.005
0.033 0.012–0.046 0.033 0.008
0.033 0.012–0.041 0.033 0.005
0.045 0.034–0.049 0.043 0.004
0.031 0.018–0.039 0.030 0.004
0.501 0.309–0.779 0.513 0.111
0.847 0.239–1.000 0.807 0.168
0.993 0.344–1.000 0.948 0.123
0.990 0.912–1.000 0.982 0.020
0.953 0.461–1.000 0.901 0.122
2.780 1.398–7.164 3.170 1.203
1.151 0.460–2.851 1.256 0.502
1.212 0.389–2.436 1.287 0.415
7.272 4.114–8.797 7.081 0.989
2.762 1.109–4.937 2.700 0.948
0.258 0.141–.0626 0.291 0.112
0.493 0.156–1.217 0.537 0.222
0.718 0.222–1.478 0.728 0.238
1.280 0.707–1.575 1.272 0.162
1.157 0.407–1.767 1.130 0.405
BM: baboon male; BF: baboon female; M1: macaque 1; M2: macaque 2; PM: patas male; PF; patas female. Std: standardized values (see text).
program (S)MATR Version 2.0 (Falster et al., 2006; Warton et al., 2006). A Bonferroni correction was used to make alpha levels more conservative (Sokal and Rohlf, 1995). Analysis of variance (ANOVA) and post hoc comparisons within and between experimental subjects of Froude number, standardized GRF, standardized wrist joint moments, and MGA were performed using SPSS 13.0 (SPSS, Chicago, IL). MGA was also compared between subjects using analysis of covariance (ANCOVA) where standardized GRF was used as the covariate.
RESULTS Collectively, for all animal subjects, there is a strong negative relationship between MGA and GRF moment American Journal of Physical Anthropology
arm (r 5 20.798, P \ 0.001), MGA and standardized GRF moment arm (r 5 20.942, P \ 0.001), MGA and wrist joint moment (r 5 20.424, P \ 0.001), and MGA and standardized wrist joint moment (r 5 20.865, P \ 0.001). The relationship between MGA and standardized GRF moment arm and standardized wrist joint moment is also significantly negative within each animal subject (Table 3). A forelimb that adopts a more digitigrade hand posture (i.e. larger MGA) will shorten the perpendicular distance between the GRF vector and the center of the wrist joint. Consequently, at any given speed and associated GRF, a forelimb with a digitigrade hand posture experiences lower wrist joint moments (see Fig. 3). Froude number is significantly correlated with standardized GRF at PK for each animal subject (Table 3) and
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TABLE 3. Bivariate relationships between kinematic and kinetic variables Variable
Subject
r
P
RMA Slope
Lower CI
Upper CI
Intercept
Std. GRF moment arm versus MGA
BM BF M1 M2 PM PF BM BF M1 M2 PM PF BM BF M1 M2 PM PF BM BF M1 M2 PM PF BM BF M1 M2 PM PF BM BF M1 M2 PM PF
20.967 20.929 20.914 20.934 20.747 20.892 20.864 20.745 20.885 20.483 20.148 20.637 0.898 0.853 0.930 0.893 0.680 0.895 20.822 20.624 20.847 20.591 20.187 20.756 20.625 20.414 20.619 20.190 20.032 20.373 0.910 0.891 0.890 0.943 0.987 0.941
\0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 0.217 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 0.120 \0.001 \0.001 \0.001 \0.001 0.188 0.816 0.004 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001
20.015 20.014 20.012 20.011 20.005 20.010 20.013 20.014 20.016 20.022 20.037 20.032 6.060 4.760 2.830 2.320 2.700 2.420 2106.300 270.500 277.100 238.100 239.200 231.400 298.900 268.400 281.300 249.400 227.800 233.700 1.256 0.967 1.294 1.085 1.014 1.080
20.015 20.015 20.014 20.013 20.005 20.011 20.014 20.016 20.018 20.028 20.046 20.039 5.520 4.320 2.560 2.040 2.260 2.150 2120.000 281.600 289.200 248.000 249.700 237.300 2116.700 281.000 2100.800 265.400 235.300 243.000 1.150 0.888 1.141 0.986 0.976 0.987
20.014 20.013 20.011 20.010 20.004 20.009 20.011 20.013 20.014 20.017 20.029 20.026 6.660 5.250 3.130 2.650 3.220 2.720 294.200 261.000 266.600 230.200 231.000 226.400 283.800 257.700 265.600 237.300 221.900 226.400 1.371 1.052 1.466 1.195 1.054 1.181
1.227 1.171 1.282 1.162 1.030 1.121 0.893 0.956 1.163 1.143 1.659 1.866 0.351 0.415 0.453 0.530 0.720 0.549 203.476 187.349 196.739 155.326 157.452 150.193 99.373 85.059 92.474 56.599 46.621 64.914 20.369 20.246 20.308 20.102 20.041 20.214
Std. wrist moment versus MGA
Std. GRF versus Froude number
Wrist angle versus Std. GRF
MGA versus Std. GRF
Std. wrist moment versus Std. GRF
a
r values based on Pearson product-moment correlations; Std, standardized values (see text).
Fig. 3. Scatter plot showing a significant negative relationship between metacarpal-ground angle (MGA) at the time of peak vertical force and standardized wrist joint moment in all animal subjects. Abbreviations are defined in Table 1. See text and Table 3 for relevant statistics.
when examined collectively (r 5 0.956, P \ 0.001) making these results consistent with those reported for other animals (e.g., Rubin and Lanyon, 1982) including cercopithecine primates (Demes et al., 1994; Polk, 2002).
Fig. 4. Scatter plot showing a significant positive relationship between Froude number and standardized GRF in all animal subjects. Abbreviations are defined in Table 1. See text and Table 3 for relevant statistics.
Therefore, at higher Froude numbers, these primates have higher forelimb forces (see Fig. 4). For most of the cercopithecine monkeys at PK, wrist joint angle and MGA showed negative relationships with GRF (Table 3). For all animals, the wrist joint becomes significantly more dorsiflexed and MGA decreases resultAmerican Journal of Physical Anthropology
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B.A. PATEL
Fig. 5. Scatter plots of metacarpal-ground angle (MGA) versus standardized ground reaction force (GRF) at the time of peak vertical force (PK) for each animal subject. Abbreviations for each animal are defined in Table 1. Correlation coefficients and RMA slopes are reported in Table 3. Lines in this figure represent RMA slopes. Note the negative relationship between MGA and GRF for all animals.
ing in a less digitigrade (i.e. more palmigrade-like) hand posture as the animals experience higher GRFs (Figs. 5 and 6; Supporting Information Movies 1 and 2). This latter relationship, however, is only significant for the two baboons, one macaque (M1), and the female patas monkey (PF). As forelimb forces increase at PK (i.e. higher GRF), wrist joint moments increase significantly (Table 3). This pattern is not surprising, because higher speeds are associated with higher GRF, and these animals adopt more palmigrade-like hand postures that have larger American Journal of Physical Anthropology
GRF moment arms between the GRF vector and the center of the wrist joint (see Fig. 3). ANOVAs revealed significant differences in Froude number, standardized GRF, standardized wrist joint moment, and MGA between experimental subjects (P \ 0.001 for all comparisons). Probability values of the post hoc comparisons between individuals are provided in Table 4. In general, the baboons (BM, BF) moved with relatively slower speeds had relatively lower forelimbs forces, had relatively lower wrist joint moments, and had more extended forelimb postures including being
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TABLE 4. ANOVA post hoc comparisons of Froude number, standardized GRF, standardized wrist joint moment, and MGA between all animal subjects Probability levels Variablea
Fig. 6. Stick figures representing a lateral view of a forelimb at the time of peak vertical force (PK) at three different speeds in the male baboon (BM). At the slow speed of 0.41 m/s, relative GRF has a magnitude of 0.41 bw. At the median speed 0.73 m/s, relative GRF has a magnitude of 0.43 bw. At the fast speed of 1.72 m/s, relative GRF has a magnitude of 0.96 bw. Note the more vertical orientation of the metacarpal segment (black) at the two lower values of GRF and the near horizontal orientation of the metacarpal segment at the highest GRF resulting in a more palmigrade-like posture.
more digitigrade compared to the other species (Table 2). The patas monkeys (PM, PF) displayed the opposite patterns by generally moving at relatively higher speeds, having relatively higher forelimb forces, having relatively higher wrist joint moments, and adopting more flexed forelimb postures including being less digitigrade (i.e. more palmigrade-like). One macaque (M1) was behaviorally more similar to the baboons, and the other macaque (M2) was more similar to the patas monkeys. The post hoc comparisons of least square mean values obtained from the ANCOVAs are presented in Table 5. At equivalent mean magnitudes of standardized GRF, the baboons used significantly more digitigrade postures (large MGA) than all other animals. The male patas monkey (PM) and one macaque (M2) were significantly less digitigrade (small MGA) than the other subjects.
DISCUSSION Terrestrial animals can moderate the negative effects of high GRF imposed on the musculoskeletal system by adopting extended limb postures (Biewener, 1989). Extended limb postures help lower the amount of antigravity muscle force needed to resist external joint moments by reducing the moment arm between the GRF vector and the center of the joint. Two benefits of lowering muscle activity include lowering metabolic costs (through reduced ATP breakdown) and decreasing peak stresses imposed upon long bones as muscles contract (Biewener, 1989, 1990, 1991). As a component of an extended forelimb, a digitigrade hand posture may specifically help reduce the muscular effort needed to resist higher wrist joint moments. As predicted, the cercopithecine monkeys in this study experience lower wrist joint moments when they adopt digitigrade hand postures compared to when they adopt more palmigrade-like hand postures. These results are also consistent with previous studies of cercopithecine monkeys that have documented that animals with more extended limb postures tend to experience lower joint moments (Polk, 2002). Therefore, adopting a more digitigrade hand pos-
BF
Froude number BM BF M1 M2 PM Std. GRF BM BF M1 M2 PM Std. Moment BM BF M1 M2 PM MGA BM BF M1 M2 PM a
M1
M2
PM
0.465 \0.001 \0.001 \0.001 0.001 \0.001 \0.001 0.039 \0.001 \0.001 0.009 \0.001 \0.001 \0.001 0.002 \0.001 \0.001 0.004 \0.001 \0.001 0.077 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001
PF \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 0.141 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001 0.030 \0.001
Std: standardized values (see text).
ture may require less wrist and digital flexor muscle activity than when adopting a palmigrade posture during locomotion. Despite experiencing lower wrist joint moments, muscles acting on the wrist joint are never completely inactive during ground locomotion. Electromyography data from wrist and digital flexor muscles in several habitually terrestrial cercopithecine monkeys indicate low to moderate levels of activity during terrestrial quadrupedal locomotion with digitigrade hand postures (Macaca mulatta: Courtine et al., 2005; Papio anubis and Erythrocebus patas: unpublished data). Some activity in these muscles through isometric contractions may be needed to maintain postures (and resist gravitational forces), because these primates lack the bony and soft tissue anatomy to keep the wrist joint in a close-packed position during support (Tuttle, 1970; Susman and Stern, 1979). In addition to helping resist collapse at the wrist joint, the digital flexor muscles contract to counteract the torques created by the GRF acting on the distal phalanges. Whether these muscles are active when palmigrade hand postures are adopted has yet to be evaluated. Because extended limb postures also help align limb elements more closely with the GRF vector, bones will be subjected to more axial compressive loads and reduced bending moments. Therefore, the metacarpals should experience more axial compression and less bending when adopting digitigrade hand postures. In fact, Biewener (1991) has documented that horse metapodia, which are nearly vertical in orientation due to their unguligrade posture, experience primarily axial compression rather than bending moments (bending-axial strain ratio of 0.3–0.4). Although metacarpal strains were not directly measured in this study due to the inherent difficulty and invasive nature of obtaining this type of data from primate hands (Richmond, 1998), it is unlikely that primate metacarpals experience pure axial compression, because these bones are never completely vertical, especially at the time of peak vertical force (Table 2; Fig. 6). Indeed, American Journal of Physical Anthropology
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TABLE 5. Least squares (LS) means (and standard errors) of MGA (degrees) at PK for all animal subjects obtained from ANCOVA with standardized GRF as the covariate Direction of mean difference and probability levels BM BF M1 M2 PM PF
LS mean
Std. Err. LS mean
45.95 42.75 36.85 18.41 19.99 31.42
1.20 1.02 1.28 1.31 1.60 1.59
BM BF M2 M2 PM PF
BM
BF
M1
M2
PM
PF
– 0.015 \0.000 \0.000 \0.000 \0.000
[ – \0.000 \0.000 \0.000 \0.000
[ [ – \0.000 \0.000 0.014
[ [ [ – 0.451 \0.000
[ [ [ ns – \0.000
[ [ [ \ \ –
Preuschoft’s (1973) hypothetical model of a digitigrade primate hand posture suggests that bending moments cannot be avoided in the metacarpals. Nevertheless, a more palmigrade-like hand posture will still expose the metacarpals to a greater amount of bending throughout a step, because the GRF vector will be more perpendicular to the metacarpal shaft for a longer duration. Because the monkeys in this study have higher forelimb forces at higher speeds [which is consistent with previous studies exploring this interaction (Demes et al., 1994; Polk, 2001, 2002)], it would be expected then that they should adopt more digitigrade hand postures as speed increases. Although this may be true in other animals, these primates become less digitigrade and more palmigrade-like when they experience higher forces. Furthermore, the individuals with relatively higher forelimb forces at higher speeds (e.g. patas monkeys) are less digitigrade (smaller MGA) than those animals that have relatively lower forelimb forces (i.e. baboons). Therefore, cercopithecine primates do not use their ability to alter their hand postures to reduce rising joint moments at higher speeds. Instead, they allow their hands to be forced into palmigrady. It may be that they are unable to resist being forced into palmigrady as the weight of the body passes over the supported forelimb (i.e. joint collapse; Goslow et al., 1973) due to morphological adaptations in the wrist and hand joints that promote mobility (i.e. compliant joints). Compared to most other mammals, all primates, including habitually terrestrial monkeys, have compliant joints in their hands and wrist that permit a greater range of motion, which can facilitate feeding and social behaviors (e.g. grooming) as well as help use arboreal substrates (e.g., Yalden, 1972). Even patas monkeys, considered to be the most terrestrial and ‘‘cursorial’’ of all primates (Gebo and Sargis, 1994), have distal forelimb joints that are relatively mobile (Tuttle, 1969). It is interesting to note that there is evidence from horses that indicates some degree of yield in the MP joints (i.e., increased plantarflexion at the fetlock joint) when experiencing higher forces (McGuigan and Wilson, 2003). However, unguligrade horses never become close to adopting a palmigrade posture as primates do (i.e., their metacarpals do not come to lie near horizontal in orientation), because their distal limb joints are not as mobile as those of primates (Yalden, 1971). Therefore, large-bodied cercopithecine primates may become more palmigrade at the expense of higher wrist joint moments. Because animals with longer effective limb lengths have a lower metabolic cost of locomotion than those animals with shorter effective limb lengths (Pontzer, 2007), it has been suggested that digitigrade postures increase effective limb length in order for animals to achieve higher locomotor speeds more efficiently (Brown and Yalden, 1973). As observed in other animals (e.g., Fieler American Journal of Physical Anthropology
and Jayne, 1998), effective forelimb length is longer when terrestrial cercopithecine monkeys (e.g., baboons, rhesus macaques, and patas monkeys) adopt digitigrade hand postures (Patel, 2008, 2009). Furthermore, changes in the angle between the metacarpals and the ground (a measure of digitigrady in the hand) significantly affect changes in total forelimb length, more so than similar changes in the more proximal elbow joint angle. However, change to a palmigrade-like posture at faster speeds significantly shortens effective forelimb length (Patel, 2008, 2009). Accordingly, despite the potential for digitigrade postures to (1) attenuate large wrist joint moments and (2) lower cost of locomotion by increasing effective forelimb length at higher speeds, it is most likely that forelimb digitigrady in primates is not associated with cursorial locomotion, because they only use digitigrade hand postures at slow speeds. This agrees well with the fact that primates in general lack most kinematic adaptations of cursoriality. Primates typically have relatively lower stride frequencies (Alexander and Maloiy, 1984), larger natural pendular periods (Preuschoft and Gu¨nther, 1994; Raichlen, 2004), larger limb excursions (Larson, 1998; Larson et al., 2000, 2001), generally have more limb yield in proximal joints (Larney and Larson, 2004), and have lower maximal running speeds on the ground compared to typical cursors. Alternatively, it is possible that becoming more palmigrade may in fact be beneficial for primates traveling at high speeds with higher forces. One possible benefit could be a gain in elastic strain energy in the tendons of the digital flexor muscles that cross the wrist and MP joints ventrally. Several studies have shown that cost of transport can be reduced by taking advantage of elastic recoil in long tendons of distal element (e.g., Alexander and Bennett-Clark, 1977; Alexander, 1984). Although this principle has generally been applied to larger animals and muscles that have short pinnate fibers and long tendons, they may also be applicable to smaller animals [(Bullimore and Burn, 2005), but see comments by Reilly et al. (2007)] and those with relatively shorter tendons (Tuttle, 1969). Because primates have relatively longer muscle fascicle lengths and shorter tendons, these tendons would have to be stretched more, possibly by adopting palmigrade hand postures, in order to accomplish the same storage of energy as the longer tendons of cursorial mammals. Another possible energy-saving mechanism could be taking advantage of the elastic properties in the ligaments of the hand (e.g., Ker et al., 1987; Bennett et al., 1989). When the hand becomes more palmigrade, the ligaments will stretch and may store elastic energy, which can be used as the hand enters the propulsive phase of stance and becomes more digitigrade. Further studies of the elastic properties of monkey forearm tendons and hand soft tissues are necessary to verify these possibilities.
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Fig. 7. A left lion paw (left), left baboon hand (center), and left dog paw (right) shown in ventral (palmar) view. Open circles show the locations of the interdigital pads covering the MP joints. Open stars show the locations of the metacarpal pads covering the wrist joint in the lion and dog and the palm in the baboon. Metacarpal pads in the baboon are further separated into the lateral thenar pad and the medial hypothenar pad. Although all three animals are habitually digitigrade, only the baboon has additional thenar and hypothenar pads that extend proximally from the interdigital pads. Pad nomenclature is from Brown and Yalden (1973). Lion and dog illustrations modified from Ellenberger et al. (1949). Images not to scale.
An additional benefit to change from a digitigrade to a palmigrade hand posture at higher speeds may be to distribute the higher GRF across the entire surface of the hand. Increasing the area of contact should lower the stresses in individual hand bones and related soft tissues, which would be beneficial when forces are high at faster speeds. Preliminary investigations of pressure data in baboon hands during quadrupedal locomotion indicate that overall relative pressure is lower in more palmigrade postures, even at faster speeds with higher forces (Patel and Wunderlich, 2008). The ability to spread forces across more of the hand would be especially important for primates that have five, long, thin fingers and depend on their hands for not only locomotion, but also for manipulation during feeding and social behaviors. Unlike most digitigrade mammals, primates have relatively large and thick thenar and hypothenar pads covering muscles and the metacarpals that extend proximally from the base of their interdigital pads (see Fig. 7). Furthermore, the palmar pads of ground-dwelling monkeys (e.g., Papio, Mandrillus, Theropithecus, and Erythrocebus) appear to be much more developed, at least externally, than those that are habitually arboreal and palmigrade (Pocock, 1925; Midlo, 1934; Napier and Napier, 1967). Although qualitative and quantitative comparisons of these soft tissues structures across primates with different hand postures have not been made, if indeed their pads are larger and elongated, this would offer a larger cushion to distribute reaction forces in a palmigrade hand posture (Brown and Yalden, 1973;
Alexander et al., 1986; Rawlins, 1993; Veron, 1999; Weissengruber et al., 2006). Distributing the GRF more broadly, rather than isolating it in the metacarpal heads by becoming more palmigrade at higher speeds should also cause the CoP in the primate hand to migrate proximally toward the carpus and wrist joint. Effectively, this proximal migration will reduce the GRF moment arm and will help moderate wrist joint moments when the hand is subjected to higher forces at higher speeds (Fowler et al., 1993). At the culmination of the step when the hand adopts a digitigrade posture, CoP should revert back toward the metacarpal heads. However, because GRF is lower near lift-off, a longer moment arm at this time will not drastically increase wrist joint moment, and there may be no negative consequence of dynamic changes in GRF moment arm length during support. Dynamically changing the length of the GRF moment arm by actively transitioning from a digitigrade to a more palmigrade hand posture may also help muscles to function at their optimal shortening velocities for efficiency or power (i.e. variable gear ratio) (Carrier et al., 1994). For example, being palmigrade in the first half of support should decrease the wrist joint gear ratio and prestretch muscle fibers that cross the wrist. After peak vertical force, the hand will become digitigrade and the wrist joint gear ratio should increase incrementally until the hand lifts off the ground (Carrier et al., 1994). These predictions are the opposite of what Carrier et al. (1998) observed at the wrist joint in trotting and galloping American Journal of Physical Anthropology
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dogs, most likely because they do not appear to display the same magnitude of yield at distal forelimb joints as seen in primate forelimbs and because they never adopt a true palmigrade hand posture during stance (Patel, 2008, 2009). Although Richmond (1998) has documented that the metacarpal heads in the patas monkey experience greater pressure than other parts of the hand, he did not examine intraindividual variation across speeds and therefore it is still unclear how much, if any, the CoP can move during stance. It would be worthwhile to examine changes in CoP throughout a step and across speeds in the future in order to evaluate some of these possible benefits for adopting palmigrade hand postures at higher speeds with higher GRFs. Additionally, if the location of the CoP changes during a step and/or when a hand changes from a digitigrade to a palmigrade posture in terrestrial primates, the convention of projecting the GRF vector upward through the metacarpal head (e.g., Schmitt, 1999; Polk, 2001, 2002; this study) may not be the most appropriate method to calculate external wrist joint moments in primates. More pressure data are needed to evaluate how the distribution of force across the hand varies during gait and across speed and to determine the most appropriate location of the GRF vector.
CONCLUSION At slow speeds with lower GRF, cercopithecine monkeys adopt digitigrade hand postures that should help lower the amount of muscle force needed to resist wrist joint moments and also possibly lower bending moments in the metacarpals. At faster speeds with higher GRF, these monkeys do not resist becoming more palmigrade. Their highly mobile wrist and hand joints may make it impossible for them to resist adopting palmigrade hand postures when subjected to high forces. Nonetheless, palmigrade hand postures may offer other benefits, such as distributing higher forces more broadly across the surface of the hand and/or moving the CoP proximally toward the wrist joint. The latter could actually reduce the moment arm of the GRF as well as help optimize muscle function at higher speeds.
ACKNOWLEDGMENTS This study benefited from numerous discussions with my dissertation committee: Susan Larson, Brigitte Demes, John Fleagle, Bill Jungers, and Brian Richmond. I also thank Kris Carlson, John Polk, Daniel Schmitt, Jack Stern, Anne Su, Roshna Wunderlich, and Jesse Young for valuable comments at different stages of this study. Kristin Fuehrer provided excellent training of the monkeys used in this study. The rhesus macaques were kindly loaned to me by James Gnadt (Howard University). The baboons were kindly loaned to me by Daniel Schmitt and Robert Davis (Duke University). This research was funded by the National Science Foundation.
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