Many terrestrial mammals are characterized by digitigrade distal limb postures. In digitigrade postures, the proximal ends of the metapodials are raised off the ground while the metapodial heads and the phalanges remain in contact with the substrate. The majority of mammals that adopt digitigrade distal limb postures do so in both their fore- and hind limbs (Howell, 1944). However, there are some exceptions to this generalization, such as bears that have plantigrade feet but adopt digitigrade forepaws (Brown and Yalden, 1973). Similarly, some of the terrestrial Old World monkeys, including baboons (Papio), geladas (Theropithecus), mandrills and drills (Mandrillus), patas monkeys (Erythrocebus), and some species of macaques (Macaca) and mangabeys (Cercocebus), digitigrade postures are only adopted in the hands while the feet assume semidigitigrade postures with only the proximal heel elevated (Napier and Napier, 1967; Tuttle, 1969; Brown and Yalden, 1973; Meldrum, 1991; Whitehead, 1993; Hayama et al., 1994; Schmitt and Larson, 1995; reviewed in Patel, 2008, 2009). For primates, this asymmetry in distal limb postures may be related to fundamental kinetic differences between the fore- and hind limbs during quadrupedal locomotion (Patel, 2010).
In general, quadrupedal primates support more weight on their hind limbs and thus experience relatively lower peak ground reaction forces (GRFs) on their forelimbs during locomotion (Demes et al., 1994; Schmitt and Lemelin, 2002; Schmitt and Hanna, 2004; Franz et al., 2005; Hanna et al., 2006). This fore- versus hind limb difference is generally considered to be one component of forelimb compliance among primate quadrupeds (Schmitt, 1999, but see Raichlen et al., 2009). The “compliance model” suggests that the relatively reduced loads on the forelimb during locomotion allow primates to retain relatively gracile forelimb bones (especially in the hand) and the capacity for increased forelimb mobility during arboreal locomotion (Schmitt, 1999). When traveling on the ground, primates generally experience higher forelimb GRFs compared to when utilizing arboreal (and simulated arboreal) supports (Schmitt, 1994, 1999; Schmitt and Hanna, 2004; Franz et al., 2005; Young, 2009). Because higher GRFs during ground locomotion could result in higher musculoskeletal stresses for an animal, adopting a digitigrade hand posture may help moderate these higher forces and potential stresses (Patel, 2010; see below). In fact, Schmitt (1994, 1995) reported that olive baboons (Papio anubis) change between a palmigrade hand posture on simulated branches to a digitigrade hand posture during terrestrial locomotion, and he related this change to the higher GRFs experienced by the baboon during terrestrial locomotion compared to arboreal locomotion. Zeininger et al. (2007) evaluated the ontogeny of digitigrade hand postures in yellow baboons (Papio cynocephalus) and found that they become increasingly more digitigrade with age. Because larger individuals will experience relatively higher GRFs on terrestrial substrates, these results further imply that adopting a digitigrade hand posture may help moderate higher GRFs.
Digitigrade distal limb postures are often suggested to be biomechanical adaptations for cursorial (i.e., high-speed) locomotion on terrestrial substrates for a variety of mammalian lineages (Howell, 1944; Gambaryan, 1974; Hildebrand and Goslow, 2001). Digitigrady likely serves as a component of an overall more extended limb posture adopted by terrestrial mammals which may help to moderate the negative effects of higher GRFs acting on the musculoskeletal system during fast locomotion (Biewener, 1983, 1989; Polk, 2002). Because fast locomotion is associated with higher peak GRFs (Rubin and Lanyon, 1982; Biewener, 1983, 1989; Demes et al., 1994; Polk, 2001, 2002; Patel, 2010), which in turn induces high levels of strain in long bones (Rubin and Lanyon, 1982; Biewener, 1983; Biewener and Taylor, 1986; Demes et al., 2001), adopting a digitigrade posture aligns the metapodials with the GRF vector and likely subjects the metapodials to a higher degree of axial compression, rather than the bending forces that predominate in many mammalian long bones (e.g., Biewener, 1991). Additionally, digitigrade postures help moderate wrist and ankle joint moments that antigravity muscles (e.g., wrist and digital flexor muscles; plantar flexor muscles) must resist by decreasing the moment arm between the GRF vector and the center of the wrist and ankle joints (e.g., Biewener, 1983, 1989; Polk, 2002; Patel, 2010). This will ultimately reduce the mass-specific amount of muscle force needed to prevent these joints from collapsing into dorsiflexion when subjected to higher forces at faster speeds. Consequently, animals that generate relatively higher GRFs at faster speeds are expected to adopt more digitigrade postures.
This hypothesis has been experimentally evaluated in three species of habitually terrestrial monkeys: Papio anubis, Macaca mulatta, Erythrocebus patas (Patel, 2010). As predicted, these monkeys exhibit lower wrist joint moments when they adopt digitigrade hand postures compared to when they adopt more palmigrade hand postures. Therefore, these primates may need less activity from wrist and digital flexor muscles when using a digitigrade hand posture during locomotion. These monkeys were also predicted to adopt more digitigrade hand postures at faster speeds. However, contrary to expectations, these monkeys become more palmigrade when they experience higher forces at faster speeds (Patel, 2010). Thus, these results suggest that primates do not alter their hand postures to reduce rising joint moments at faster speeds, and instead, they allow their hands to be forced into palmigrady. The most likely explanation for this is that these primates are simply unable to resist being forced into palmigrady as the weight of the body passes over the supported forelimb. This, in turn, is due to the highly mobile (i.e., compliant) wrist and hand joints these primates have evolved to effectively navigate arboreal substrates (e.g., Yalden, 1972). Because habitually terrestrial cercopithecine monkeys are digitigrade when moving slowly and are more palmigrade when moving at fast speeds, it is clear that a digitigrade hand posture in primates is not a cursorial adaptation (Patel, 2008, 2009, 2010, in press; Patel and Polk, 2010).
One possible benefit of changing from a digitigrade to a palmigrade-like hand posture at faster speeds may be to distribute the higher GRFs across the entire palmar surface of the hand. Increasing contact area would lower the stresses in individual hand bones and related soft tissues, which would be especially important when forces are high at faster speeds. Unlike most digitigrade mammals, primates have relatively large and thick thenar and hypothenar pads covering their metacarpals as they extend proximally from the base of their interdigital pads. These palmar pads may offer a larger area to distribute GRFs when adopting a palmigrade hand posture at fast speeds. This potential to dynamically moderate stresses in the hand is especially important for primates because they depend on their hands for not only locomotion, but also for manipulative behaviors (e.g., feeding, grooming).
In this study, we evaluate the relationship between speed, GRF, contact area, and pressure in the hands of two habitually digitigrade olive baboons (Papio anubis) during terrestrial locomotion. Peak GRF, contact area, peak pressure, and pressure-time integral are assessed in two regions of the hand: 1) the fingers and 2) the palm including metacarpal heads. Three predictions are made. First, as animals increase locomotor speed, their hands will be subjected to higher peak GRFs. Second, as animals increase locomotor speed, their hands will change from a digitigrade to a palmigrade hand posture, and contact area will increase in both the fingers and palm region of the hand. Third, as animals increase locomotor speed and experience higher GRFs, pressure in both the fingers and palm will not change substantially, and by extension, stresses and strains will be moderated.
MATERIALS AND METHODS
Olive baboons (Papio anubis Lessen 1827) were chosen for this study because they are highly terrestrial (Jolly, 1967) and have been observed to use digitigrade hand postures in both the wild and in captivity (e.g., Napier and Napier, 1967; Schmitt, 1994; Patel, 2009, 2010). One adult male (28 kg) and one adult female (23.1 kg) were housed separately in large rooms where they were permitted to move freely 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, NY).
Each animal was filmed using a video-based motion analysis system (Peak Performance Technologies, Inc., Englewood, CO) as it moved over a plywood platform (10.5 m long × 0.7 m wide) within a tunnel enclosed by clear Lexan (Fig. 1; Polk, 2001). One HSC -180NS video camera fitted with a Cosmicar/Pentax TV Zoom [8–48 mm] lens, shuttered at 1/2000 sec to avoid motion blur, and operating at 60 Hz, was positioned adjacent to the tunnel in lateral view. Video signals were time stamped using a GL-250 time-code generator (J.C. Labs, La Honda, CA). The video served two functions. First, it allowed for the proper identification of steps in which the hand made full contact with the pressure mat (see below). Second, the video was used to calculate the animal's speed as it traversed the pressure mat. Speed was calculated as the time interval required for a fixed anatomical marker (either the tip of the nose or the base of the tail) to pass between two markers spaced 1 m apart and located on either side of the pressure mat. Froude numbers, v2/gh, where v is velocity, g is the gravitational constant, and h is the cube-root of body mass (Hof, 1996; Biewener, 2003), were calculated to standardize and combine data from the two animals of different body size. The cube-root of body mass was used rather than hip height because the animals never stood still in front of the camera.
Dynamic palmar pressure distribution was collected using an EMED-SF platform (Novel, Inc., St. Paul, MN). The platform consists of a matrix of 0.5 × 0.5 cm capacitive sensors that quantify load normal to their surface; the platform does not quantify horizontal forces (e.g., fore-aft and mediolateral). A minimum load of 1 N/cm2 or 10 kPa was considered contact. Four variables were measured in the fingers and palm (which included the metacarpal heads): 1) peak GRF (%bw), 2) contact area (cm2), 3) peak palmar pressure (N/cm2), and 4) pressure-time integral ([N*s/cm2]). Peak GRF and pressure are obtained from the sensor that reports the highest force or pressure value across an entire step in each anatomical region (fingers and palm). Contact area for an anatomical region is not involved in the calculation of peak pressure for that area because each sensor's peak pressure is calculated, and the peak of these is used to determine the peak for an anatomical region. Pressure-time integral is a quantity similar to impulse that accounts for both pressure and time over which the pressure is applied and thus provides a valuable means to compare how much total pressure is supported by each anatomical region. Relative contact area for each region of the hand was calculated by taking the square-root of contact area and dividing this by hand length (cm) for each animal subject. Hand length was measured in each animal as the distance from the proximal end of the palmar pad (i.e., the wrist joint) to the distal end of the third digit (female baboon: 14.0 cm; male baboon: 15.4 cm). Finally, dynamic center of pressure (CoP) location was evaluated when possible to observe the pattern of total hand pressure throughout the step.
Twenty steps for each subject (total N = 40) at a range of speeds (0.68–4.0 m/s) were analyzed. Steps from both symmetrical and asymmetrical gaits were analyzed together and these included “kinematic” walks, runs, ambles, and gallops (e.g., Hildebrand, 1985; Biknevicius and Reilly, 2006; Schmitt et al., 2006). Combining data from symmetrical and asymmetrical steps was justified because Patel and Polk (2010) found no significant differences in hand postures when olive baboons use different gaits at the same speed (i.e., symmetrical-asymmetrical transition speeds). These authors also showed only little change in hand posture across galloping speeds. Because of the small number of gallops (female baboon: two steps; male baboon: five steps; all left hands), we did not differentiate between leading and trailing forelimbs, despite the potential for differences in peak vertical forces that can exist between these limb pairs when mammals gallop (Demes et al., 1994; Walter and Carrier, 2007). For similar reasons (i.e., small sample size), we did not distinguish different types of symmetrical gaits such as walks and ambles (e.g., Schmitt et al., 2006).
Two sets of analyses were performed. First, we qualitatively and quantitatively described (with descriptive statistics) the pressure distribution patterns in the fingers and palm during a typical step and across steps of different speeds. Second, we quantitatively examined (using Pearson product-moment correlation and ordinary least squares regression statistics) the bivariate relationships between Froude number, peak GRF, relative contact area, peak pressure, and pressure-time integral. All statistics were calculated using SPSS 16.0 for Mac OS X (SPSS Inc., Chicago, IL).
Irrespective of speed, both baboons make initial contact with the ground using their distal phalanges. Thus, the center of pressure (CoP) is consistently located on or near the finger-tips at the beginning of forelimb support (Fig. 2). From the pressure distribution patterns, it is also apparent that the other phalanges (middle and proximal) only occasionally make full contact with the ground (Fig. 2). This is not surprising because baboons (and cercopithecine monkeys in general) often flex their proximal interphalangeal joints and extend their metacarpophalangeal joint during locomotion, effectively shortening the functional length of the fingers (Nieschalk and Demes, 1993; Richmond, 1998). After this initial contact (i.e., touchdown), the metacarpal heads of Digits II–V make contact with the ground, typically within 1–2 frames. As a result, CoP migrates proximally from the distal phalanges towards the metacarpal heads. CoP remains under the metacarpal heads until the hand lifts off the ground.
Summary statistics of Froude number, peak GRF, relative contact area, peak pressure, and pressure-time integral are presented in Table 1. All correlation coefficients of the bivariate relationships are summarized in Table 2. Across all speeds, peak GRF and peak pressure is larger in the palm region of the hand compared to the finger region of the hand (Table 1). Thus, a larger proportion of weight is supported by the palm than by the fingers with any given step. Within the palm region of the hand, both GRF and peak pressure are greatest in the metacarpal heads across all speeds, and these peak pressures are consistently located in Digits III and IV, although the metacarpal head of Digit II can also experience high pressures (Fig. 2).
Froude number is significantly positively correlated with peak GRF in both the fingers (r = 0.624, P < 0.001) and the palms (r = 0.757, P < 0.001) making these results consistent with those reported for other studies on cercopithecine primates (Demes et al., 1994; Polk, 2002; Patel, 2010). Therefore, at higher Froude numbers, these primates have higher forelimb forces than at low Froude numbers (Fig. 3).
Froude number is significantly positively correlated with contact area for the palm region of the hand (r = 0.810, P < 0.001; Fig. 4). As a result, peak GRF in the palm is also significantly positively correlated with palmar contact area (r = 0.580, P < 0.001; Fig. 5a). At slower speeds, with lower peak forces, the baboons use stereotypical digitigrade hand postures and only the metacarpal heads make contact with the pressure mat (Fig. 2a). As speed and peak forces increase, the hand becomes less digitigrade (i.e., more palmigrade) and a greater portion of the palm (proximal to the metacarpal heads) makes contact with the pressure mat (Fig. 2b). More specifically, the thenar and hypothenar regions make contact with the ground. Even with this larger contact area, however, CoP does not appear to extend proximally beyond the area of the metacarpal heads (Fig. 2b).
In contrast, contact area of the fingers is not significantly correlated with Froude number (r = −0.238, P = 0.139; Fig. 4) despite the hand transitioning between a digitigrade and palmigrade posture. This finding, along with the resulting pressure maps (Fig. 2b), suggests that the digits are not becoming significantly more extended at faster speeds and that the skin underlying the middle and proximal phalanges are only making minimal contact with the ground. Thus, even at faster speeds, the digits retain their short functional lengths (see above). Peak GRF in the fingers is not significantly correlated with finger contact area (r = 0.066, P = 0.686; Fig. 5b).
Froude number is not correlated with peak pressure in the palm region of the hand (r = 0.090, P = 0.581; Fig. 6). This is not surprising since both peak force and palmar contact area increase at faster speeds (see above). Also, peak vertical force is not correlated with peak pressure in the palm (r = −0.052, P = 0.748; Fig. 7a). Therefore, pressures in the palm region of the hand are moderated across a large range of speeds and forces. In contrast, Froude number is significantly correlated with peak pressure in the fingers (r = 0.583, P < 0.001; Fig. 6), as is peak force (r = 0.719, P < 0.001; Fig. 7b). Accordingly, pressure is not moderated in the fingers as they are in the palms as these animals transition between digitigrade and palmigrade hand postures at faster speeds.
Further evidence of differences between the finger and palm regions in peak pressure is provided by the pressure-time integral results; pressure-time integrals are analogous to impulse (force-time integral) and represent the total pressure throughout a step in each anatomical region. At all but the fastest observed speeds, pressure-time integrals are typically larger in the palms compared to the fingers, indicating that the palms experience higher total pressure throughout the step (Table 1, Fig. 8a). As speed increases, peak pressure in the palm is moderated, but peak pressure in the fingers increases and approaches the levels seen in the palm region of the hand (Fig. 8a). For both the palm and finger regions of the hand, the relationship between Froude number and pressure-time integral is negative (Table 2), but the slope of the ordinary least-squares regression line for the palm is significantly greater than that for the fingers (P < 0.05; Fig. 8b).
This study provides a quantitative analysis of pressure distribution in two different functional regions of the hands of a nonhominoid primate. Previous studies have examined manual digital pressures in primates (Richmond, 1998; Wunderlich and Jungers, 2009), but these studies did not specifically evaluate speed effects on pressure patterns. Previous kinematic studies of terrestrial locomotion have shown that baboons (and other habitually terrestrial cercopithecoid primates including patas monkeys and rhesus macaques) can transit between a digitigrade hand posture typical of most terrestrial mammals to a more palmigrade hand posture across speeds (Patel, 2008, 2009, in press; Patel and Polk, 2010). In these studies, the angle between the metacarpals and the ground significantly decreased as these animals walked, ran, or galloped with faster speeds and experience higher GRFs. The larger palmar contact area at faster speeds and with higher peak forces reported in the present study further supports the conclusion that digitigrady in the primate forelimb is not a cursorial adaptation.
Pressure is equal to force per unit area. Thus, moderation of pressure can be achieved if both force and area increase with faster speeds. This is the pattern that is observed in the palm region of the hand. As baboons move at faster speeds on the ground, their forelimbs experience higher GRFs, and palmar contact area increases. Peak pressure in the palm region of the hand does not change significantly as these animals transit to a palmigrade hand posture from a digitigrade hand posture. Although in vivo bone strain in the hand was not measured in this study, the attenuation of peak pressure in the palm region of the hand likely attenuates strains in hand bones, specifically in the metacarpals.
The possibility of moderating strains in the metacarpals across different hand postures has implications for metacarpal morphology in cercopithecoid primates. Hands are in direct contact with the substrate and therefore their morphology is likely to reflect different loading regimes associated with different locomotor and postural behaviors (e.g., Etter, 1973; Lemelin, 1999; Wunderlich, 1999; Jungers et al., 2005; Patel et al., 2009). Patel (2008), unpublished observations, found that the metacarpals (II, III, and IV) of habitually digitigrade cercopithecoid monkeys (e.g., Papio, Mandrillus, Theropithecus, Erythrocebus) could only weakly be distinguished from those that only adopt palmigrade postures (i.e., habitually arboreal cercopithecine and colobine monkeys). Although digitigrade taxa were found to have relatively shorter metacarpals, they did not have relatively more robust metacarpal heads or midshaft cross-sectional areas. Furthermore, multivariate discriminant analyses resulted in several digitigrade taxa being classified as palmigrade and some palmigrade taxa being classified as digitigrade, suggesting some degree of morphological similarity in the palm bones of these primates (Patel, 2008, in press, unpublished observations). This similarity between hand posture groups could be attributed to the fact that even habitually digitigrade cercopithecoid monkeys adopt palmigrade hand postures in different situations such as terrestrial running (Patel, 2008, 2009, in press; Patel and Polk, 2010). Specifically, when forces are higher during running, the potentially higher pressures that could result in increased strain on the metacarpals are moderated by adopting a palmigrade hand posture with greater contact area in this region of the hand (Figs. 5a, 7a, 8a). Although obtaining strain data from these hand bones is unlikely due to the invasive nature of such experiments (e.g., Richmond, 1998; Demes et al., 2001), additional palmar pressure data from more baboons and other digitigrade taxa are necessary to see if these patterns are consistent.
Terrestrial cercopithecoids have a significantly smaller phalangeal index (middle phalanx III length + proximal phalanx III length/metacarpal III length) compared to their arboreal and semiterrestrial counterparts (Fig. 9; Midlo, 1934; Etter, 1973; Patel, in press), a pattern that is seen in other primates and nonprimate mammals (e.g., Lemelin, 1999; Kirk et al., 2008). Thus, terrestrial digitigrade primates have relatively short fingers. Relative elongation of phalanges serves as an arboreal adaptation because longer fingers facilitate the ability to grasp branches during arboreal locomotion (Napier, 1993; Lemelin, 1999). Because peak GRFs are higher during terrestrial compared to arboreal locomotion (Schmitt, 1994, 1999; Schmitt and Hanna, 2004; Franz et al., 2005; Young, 2009), shorter phalanges of terrestrial digitigrade monkeys may help to lower bending moments by effectively shortening the load arm on which the higher GRF vector acts (Nieschalk and Demes, 1993). This is also important since peak pressures are not moderated in the fingers at faster speeds and with hand postural changes as they are in the palm (Figs. 6, 8a). Although these patterns are robust, dynamic pressure data during terrestrial locomotion from primates with long fingers are necessary to further evaluate this issue. Our preliminary (unpublished) pressure data from two arboreal New World monkeys with relatively long fingers (Cebus and Ateles) do suggest that the finger region of the hand is not loaded as highly in these taxa as they are in the digitigrade baboon.
It is necessary to recognize that knowing the location of CoP is necessary for accurately measuring joint moments (e.g., Fowler et al., 1993; Carrier et al., 1998; Witte et al., 2002). For any given hand posture, a CoP located further away from a joint center will effectively result in large joint moments (due to longer GRF moment arms). Because contact area increased at faster speeds, resulting in a more palmigrade hand posture, it would be expected that CoP would also migrate proximally towards the carpus and will help lower wrist joint moments (Patel, 2010). Effectively, this proximal migration will shorten the GRF moment arm and will help moderate wrist joint moments when the hand is subjected to higher forces at faster speeds. Although the present study did not focus on hand CoP, our preliminary observations presented above do not suggest a proximal migration of CoP. While CoP does move from the fingertips of the hand at touchdown to a region underlying the metacarpal heads for all speeds, there is little proximal movement past the metacarpal heads even with increased palmar contact area (Fig. 2b). The lack of CoP movement despite increased palmar contact area may be a result of simultaneous increase in finger pressure. This supports the idea that transitioning from a digitigrade hand posture to a palmigrade hand posture may occur in these habitually terrestrial monkeys at the expense of rising wrist joint moments and increased wrist and digital flexor muscle activity (Patel, 2010). It is important to note, however, that these CoP patterns may not be representative of all primate hands during terrestrial locomotion. Additional dynamic pressure data, including CoP patterns, from other habitually digitigrade primates, as well as strictly palmigrade primates are necessary to evaluate this issue further.
Primates are well known to exhibit a number of morphological and behavioral features associated with arboreal lifestyles. Among these are their gracile limbs with long digits, high levels of forelimb protraction, compliant gaits, and higher hind limb than forelimb peak GRFs. However, catarrhine primates specialized for life on the ground are faced with higher peak GRFs acting on the forelimb, a substrate that is not compliant, and the need to move fast for long distances and/or to avoid predators. With faster locomotor speeds, peak vertical GRFs increase, and skeletal and soft tissue integrity can be compromised. To reduce peak loads on the hand, a structure that is integral for not only locomotion but also feeding and social behaviors, baboons distribute these higher forces over a larger palmar surface area, thereby attenuating palmar pressure. Such dynamic changes in palmar pressure likely moderate strain on their gracile hand bones. As far as we know, this is a unique adaptation to speed-related increases in GRFs and musculoskeletal load.
The authors thank Jason Organ and Qian Wang for inviting us to contribute to this volume. The baboons used in this study were kindly loaned to us by Daniel Schmitt and Robert Davis (Duke University). Kristin Fuehrer assisted with the experiments and training of the animals.