Mechanics of heel-strike plantigrady in African apes

https://doi.org/10.1016/j.jhevol.2020.102840Get rights and content

Highlights

  • The evolution of heel strike in great apes and humans is poorly understood.

  • We test the function of heel strike and foot rollover in chimpanzees and gorillas.

  • Heel strike increases effective limb length in relatively short-legged African apes with long grasping toes.

  • Foot rollover and hip protraction increase stride length and may reduce energy costs.

  • These results add to our understanding of the evolution of the human foot.

Abstract

The initiation of a walking step with a heel strike is a defining characteristic of humans and great apes but is rarely found in other mammals. Despite the considerable importance of heel strike to an understanding of human locomotor evolution, no one has explicitly tested the fundamental mechanical question of why great apes use a heel strike. In this report, we test two hypotheses (1) that heel strike is a function of hip protraction and/or knee extension and (2) that short-legged apes with a midfoot that dorsiflexes at heel lift and long digits for whom digitigrady is not an option use heel-strike plantigrady. This strategy increases hip translation while potentially moderating the cost of redirecting the center of mass (‘collisional costs’) during stance via rollover along the full foot from the heel to toes. We quantified hind limb kinematics and relative hip translation in ten species of primates, including lemurs, terrestrial and arboreal monkeys, chimpanzees, and gorillas. Chimpanzees and gorillas walked with relatively extended knees but only with moderately protracted hips or hind limbs, partially rejecting the first hypothesis. Nonetheless, chimpanzees attained relative hip translations comparable with those of digitigrade primates. Heel-strike plantigrady may be a natural result of a need for increased hip translations when forelimbs are relatively long and digitigrady is morphologically restricted. In addition, foot rollover from the heel to toe in large, short-legged apes may reduce energetic costs of redirecting the center of mass at the step-to-step transition as it appears to do in humans. Heel strike appears to have been an important mechanism for increasing hip translation, and possibly reducing energetic costs, in early hominins and was fundamental to the evolution of the modern human foot and human bipedalism.

Introduction

One of the defining traits of humans and possibly all great apes, compared with all other primates and nonprimate mammals, is the use of heel-strike plantigrady in which the heel contacts the ground first at the end of the swing phase during walking (Weidenreich, 1923; Elftman and Manter, 1935; Gebo, 1992, 1993; Meldrum, 1993; Schmitt and Larson, 1995). Only humans, chimpanzees, and gorillas are definitively known to heel strike (Gebo, 1992, 1993; Schmitt and Larson, 1995). Orangutans are thought to have a modified lateral heel landing that is debatably also a form of heel strike (Gebo, 1992, 1993; Schmitt and Larson, 1995). In contrast, gibbons and all nonhominoid primates touch down with a flat foot (plantigrady), the forefoot (digitigrady), or the midfoot (semiplantigrady; Gebo, 1992; Gebo, 1993; Meldrum, 1993; Schmitt and Larson, 1995; Vereecke et al., 2006). No clear consensus exists regarding the functional or evolutionary significance of heel strike among large apes. There are currently two primary hypotheses concerning the evolution of heel-strike plantigrady, both of which relate to hind limb position and hip translation (the distance traveled by the hip from touchdown to toe-off).

Schmitt and Larson (1995) identified patterns of heel contact (in spider monkeys and gibbons) and heel strike (in great apes) that they thought related to limb position and the need to shift weight posteriorly (Reynolds, 1985). Specifically, they argued that “plantigrady, when present in arboreally adapted primates, is related to the protracted position of the hindlimb” at touchdown (Schmitt and Larson, 1995: 46). This protracted position of the whole hind limb was, in their view, a combination of high values of hip protraction (a small angle between the line of the thigh to the horizontal at touchdown) and highly extended knees. Later, Larson et al. (2001) made similar arguments, asserting that large excursion angles facilitated, in part, by large touchdown and toe-off angles of the hind limb would facilitate long hip translations in relatively short-legged great apes. The original suggestion by Schmitt and Larson (1995) that heel-strike plantigrady is a function of protracted hind limbs remains untested. In addition, the question of how heel-strike plantigrady and digitigrady compare in terms of hip translation during the stance phase remains unexplored.

In digitigrady, and to a lesser extent semiplantigrady, effective limb length (ELL, the distance from the hip to the pivot point) is increased because the length of the rearfoot and midfoot is added to that of the leg and thigh, thereby further increasing the potential excursion of the hind limb and hip translation (Fig. 1A; Smith and Savage, 1956). In addition, touching down with a raised heel and more plantarflexed ankle aligns the ground reaction force resultant with the ankle joint, reducing ankle moments and plantar flexor muscular effort to maintain ankle posture (Biewener, 1989). Apes, in contrast to other primates, may be unable to use digitigrade foot postures because of their long phalanges and their metatarsophalangeal joints that are less stable in dorsiflexion than in plantar flexion (Fernandez et al., 2016; Wunderlich and Ischinger, 2017). Touching down with the forefoot could incur high bending moments on these long digits in large-bodied apes.

Compared with other primates, apes may have additional reasons to increase hip translation because of their relatively short hind limbs. Most quadrupedal monkeys have larger forelimb angular excursions than hind limb angular excursions because of their relatively longer hind limbs (low intermembral index [IMI]; Larson et al., 2001). Apes, in contrast, have relatively longer hind limb angular excursions than forelimb angular excursions because of their relatively longer forelimbs (Reynolds, 1987; Larson et al., 2001). By using larger excursions (relative to the forelimb) of the shorter hind limb, apes should be able to maintain similar forelimb and hind limb hip and shoulder linear translations. Therefore, following the argument of Larson et al. (2001), the IMI predicts patterns of hind limb angular excursion, which, in turn, could affect foot placement (Schmitt and Larson, 1995).

Hind limb excursions can be increased without digitigrady by using (a) large amounts of hip protraction (flexion) before touchdown and hip retraction (extension) before toe-off, (b) extension of the knee throughout the stance phase, and/or (c) large amounts of ankle dorsiflexion at touchdown and plantar flexion at toe-off. These kinematic features may enhance hip translation and could be associated with heel strike in apes.

Increased hip translation is an important goal because it increases step length. This is turn increases stride length and reduces stride frequency, potentially decreasing energetic costs (Taylor, 1985; Kram and Taylor, 1990). Increased hip translation is made possible by both digitigrady and heel strike by increasing ELL in different ways (Fig. 1A, B). Here, we test the hypothesis that apes will increase ELL by using a highly dorsiflexed ankle at touchdown, touching down at the heel, then rolling over the foot, thereby maximizing hip translation (Fig. 1B). In humans, heel strike seems to be favored because it increases the ELL by extending the pivot point of the inverted pendulum that describes our center of mass movement below the ground (Pontzer, 2007; Webber and Raichlen, 2016), as it would with apes as well (Fig. 1B). Furthermore, a heel-striking foot can be described as a curved foot (Fig. 2) that promotes an effective rollover, translation of the center of pressure (the anchor point of the ground reaction force resultant) from the heel to toe (McGeer, 1990; Donelan et al., 2002; Adamczyk et al., 2006; Adamcyzk and Kuo, 2013; Fig. 2). Heel-to-toe rollover facilitates a reduction in cost of transport by allowing less protracted hind limbs to produce the same hip translation distance and reduce redirections of the center of mass (i.e., collisions) by allowing the hip to follow a flatter vertical path (McGeer, 1990; Donelan et al., 2002; Adamczyk et al., 2006; Cunningham et al., 2010; Usherwood et al., 2012; Adamcyzk and Kuo, 2013). Both these advantages of human heel strike have been posited by Holowka and Lieberman (2018) to be important to apes and to have played a role in the evolution of human locomotion. It is worth noting that semiplantigrady would also provide rollover (translation of the center of pressure along the portions of the foot in contact with the ground), but the touchdown point in semiplantigrady limits the rollover distance. Heel-strike plantigrady would provide the greatest potential translation of the center of pressure.

In this study, we examine a phylogenetically and morphologically diverse sample of primates and provide data that test models of hind limb position, foot rollover, and hip translation to explain the presence of heel strike in great apes.

  • 1)

    Hypothesis 1: Heel-strike plantigrady will be associated with high degrees of hind limb protraction compared with semiplantigrady and digitigrady. This hypothesis predicts one or more of the following: (a) hip angles at touchdown are smaller (more protraction) in heel-striking great apes than in other primates; (b) knee angles at touchdown are larger (more extension) in heel-striking great apes than in other primates; (c) ankle angles at touchdown are smaller (more dorsiflexion) in heel-striking great apes than in other primates; (d) hind limb protraction angles at touchdown are smaller (more protracted) in great apes than in other primates.

  • 2)

    Hypothesis 2: Heel-strike plantigrady with a foot rollover is used as part of a mechanism to increase ELL and hip translation in relatively short-legged, long-toed apes with forefoot adaptations for stability in plantar flexion. Thus, we predict that (a) heel-striking great apes exhibit ELL-to-anatomical limb length (ALL) ratios equal to or longer than those of other primates; (b) heel-striking great apes exhibit hip translation-to-ALL ratios that are equal to or longer than those of both digitigrade and semiplantigrade primates; and (c) compared with a theoretical footless model (hip translation/ALL), both digitigrady and heel-strike plantigrady offer an increased hip translation despite dissimilar mechanisms of achieving it.

Section snippets

Materials and methods

We examined hind limb kinematics in ten species of primates ranging from highly arboreal to highly terrestrial and exhibiting a range of foot contact patterns and hip and knee kinematics (see Schmitt and Larson, 1995), IMI (from Fleagle et al., 1981), and substrate preferences (reviewed in Rose, 1973, 1974; Fleagle, 2013). Two lemurs were included in the study, the ring-tailed lemur (Lemur catta, 3 adult males; IMI = 70) and the brown lemur (Eulemur fulvus, 2 adult males; IMI = 72). The monkeys

Hip, knee, and ankle angles

The mean and one standard deviation for hip, knee, and ankle angles at touchdown on terrestrial and arboreal substrates for the subjects in this study are displayed in Table 1. Hip angle at touchdown is displayed in Figure 4A. Contrary to expectations, Gorilla had the largest hip angles (least protracted hip) on the ground compared with all other genera (all comparisons at p < 0.01). Ateles and Eulemur had the smallest hip angles (most protracted hip) compared with all other genera (all

Discussion and conclusions

Heel-strike plantigrady is a foot contact pattern that is shared by humans, African apes, and possibly, orangutans and not reported in other mammals (Gebo, 1992, 1993; Meldrum, 1993; Schmitt and Larson, 1995). The selective pressures that may have driven the evolution of heel strike remain an area of debate. To explore this issue, we examined the kinematics of foot contact patterns in a phylogenetically diverse sample of primates, including chimpanzees and gorillas, and tested specific

Conflict of interest

The authors have no conflict of interest.

Acknowledgments

We would like to thank the faculty and staff at the Primate Locomotion Laboratory at Stony Brook University for access to animals, assistance, and advice. In particular, we would like to thank Marianne Crisci, Alex Belniak, and Kristin Fuehrer for their invaluable assistance with animal training. We thank Corinne Kendall, Jennifer Ireland, and Chris Goldston at the North Carolina Zoo for access to the gorillas and for support throughout the data collection process. We would also like to thank

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