Segmental morphometrics of the olive baboon (Papio anubis): a longitudinal study from birth to adulthood

Abstract

The linear dimensions and inertial characteristics of the body are important in locomotion and they change considerably during the ontogeny of animals, including humans. This longitudinal and ontogenetic study has produced the largest dataset to date of segmental morphometrics in a Catarrhini species, the olive baboon. The objectives of the study were to quantify the changes in body linear and inertial dimensions and to explore their (theoretical) mechanical significance for locomotion. We took full‐body measurements of captive individuals at regular intervals. Altogether, 14 females and 16 males were followed over a 7‐year period, i.e. from infancy to adulthood. Our results show that individual patterns of growth are very consistent and follow the general growth pattern previously described in olive baboons. Furthermore, we obtained similar growth curve structures for segment lengths and masses, although the respective time scales were slightly different. The most significant changes in body morphometrics occurred during the first 2 years of life and concerned the distal parts of the body. Females and males were similar in size and shape at birth. The rate and duration of growth produced substantial size‐related differences throughout ontogeny, while body shapes remained very similar between the sexes. We also observed significant age‐related variations in limb composition, with a proximal shift of the centre of mass within the limbs, mainly due to changes in mass distribution and in the length of distal segments. Finally, we observed what we hypothesize to be ‘early biomechanical optimization’ of the limbs for quadrupedal walking. This is due to a high degree of convergence between the limbs’ natural pendular periods in infants, which may facilitate the onset of quadrupedal walking. Furthermore, the mechanical significance of the morphological changes observed in growing baboons may be related to changing functional demands with the onset of autonomous (quadrupedal) locomotion. From a wider perspective, these data provide unique insights into questions surrounding both the processes of locomotor development in primates and how these processes might evolve.

Segmental morphometrics of bonobos (Pan paniscus): are they really different from chimpanzees (Pan troglodytes)?

“…; Druelle & Berthet, ; Druelle et al. ). Inertial properties of the body (segment mass and mass distribution) reflect the resistance to linear and angular acceleration about joints during locomotion, thereby influencing locomotor performance (Larson et al.…”

Ecomorphological specialization leads to loss of evolvability in primate limbs*

“…Conversely, stronger covariation in the appendicular skeleton among generalists may reflect selection for tighter functional integration between the limbs, for example, in arboreal quadrupeds, who must navigate complex three‐dimensional environments (Stevens ), and in terrestrial quadrupeds, where differences in fore‐ and hindlimb lengths may affect the coordinated pendular period of the limbs and hence decrease the efficiency of locomotion (Raichlen ; Druelle et al. ). Strong covariation in these species predicts their limbs may respond more slowly to selection for functional specialization, especially towards ecomorphologies involving disparate limb proportions.…”

Developments in development: What have we learned from primate locomotor ontogeny?

“…Because of their need to cling to their mother during initial locomotor efforts, infant primates have more well developed grasping muscles and more distally distributed limb mass compared to adults (Grand, ; Raichlen, ; Turnquist & Wells, ). Accordingly, in a longitudinal sample of baboons spanning the ages of 1–9 months, Raichlen () found a proximal shift in limb mass distribution with age (see also Druelle, Aerts, D'août, Moulin, & Berillon, ). Young infants with more distally distributed limb mass used relatively longer strides and lower stride frequencies than older infants with more proximally distributed limb mass (Raichlen, ).…”

“…Regardless, ontogeny has provided a means to test some of the more proximate biomechanical hypotheses for why some mammals, and primates in particular, prefer DSDC gaits. The utility of ontogeny for understanding primate gait stems from the fact that 1) although adult primates show variability in gait types, the gait profile of infant and juvenile primates is more variable than that of adults, and non‐DS gaits (e.g., lateral sequence, with either lateral or diagonal couplets; LSLC, LSDC) are used much more frequently (Dunbar & Badam, ; Hildebrand, ; Hurov, ; Nakano, ; Rollinson & Martin, ; Shapiro & Raichlen, ; Vilensky & Gankiewicz, ; Young, ), and 2) during growth, primates experience dramatic changes in body mass, body mass distribution, and limb proportions (Druelle et al, ; Druelle et al, in press; Grand, ; Jungers & Fleagle, ; Leigh, ; Lumer & Schultz, ; Raichlen, ; Shapiro & Raichlen, ; Turnquist & Wells, ; Young, ; Young & Heard‐Booth, ) permitting a direct real‐time test of how such morphological changes are correlated with gait selection.…”

“…Alternatively, if the body's center of mass lies behind the line connecting the supporting diagonal limb pair (as it theoretically would be in a primate with a caudally positioned center of mass), the hindlimb of the diagonal swinging limb pair should land first, encompassing the center of gravity vector within the supporting three limbs, preventing backward pitch, and resulting in a DS gait. This explanation, known as the “Support Polygon Model” (Cartmill et al, ; Gray, ; Hildebrand, ; Tomita, ; Young, ), is problematic for the following reasons: 1) the position of the whole body center of mass of primates is not particularly caudal—in the few primate species in which whole body COM has been measured, it appears to be located relatively close to the craniocaudal midline (Crompton, Li, Alexander, Wang, & Günther, ; Druelle et al, ; Grand, ; Raichlen, Pontzer, Shapiro, & Sockol, ; Reynolds, ; Turnquist & Wells, ; Vilensky, ; Wells & DeMenthon, ; Young, ); 2) experimental manipulations of body COM in primates, or comparisons of primates with COM shifts due to tail fattening, do not result in predicted changes of footfall sequences (Young, Patel, & Stevens, ); 3) regardless of the position of the body's center of mass, primates readily switch from DS to LS gaits under certain conditions (e.g., when moving from a narrow pole to the flat ground: Hesse, Nyakatura, Fischer, & Schmidt, ; Prost & Sussman, ; Shapiro, Young, & Souther, ; Stevens, ; Vilensky & Larson, ; Vilensky & Patrick, ; Vilensky et al, ; Wallace & Demes, ) 4) in DS gaits, the landing hindlimb of a diagonal pair is not necessarily in a position to prevent backward pitch, and at that moment the direction of pitch is likely forward anyway (Cartmill et al, ); 5) the Support Polygon Model is based on static stability, and primates most likely rely more often on dynamic stability when travelling at any appreciable speed (Chadwell & Young, ; Lammers & Zurcher, ; Larson & Stern, ; Vilensky & Larson, ; Young et al, ; Young, Russo, Fellmann, Thatikunta, & Chadwell, ); and 6) the idea that primates have a more caudal COM has been conflated with the hindlimb “dominance” of primates compared to other mammals (i.e., higher substrate reaction forces on hind compared to forelimbs). Yet limb force distribution does not necessarily equate to center of mass position; greater weight support on primate hindlimbs may stem from the location of the body COM relative to the limbs, the kinematic positioning of the hands and feet relative to the COM (regardless of the latter's fore‐aft position), or an active shift to ...…”