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First published online May 1, 2009
Journal of Experimental Biology 212, 1576-1591 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025460

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Ontogeny of joint mechanics in squirrel monkeys (Saimiri boliviensis): functional implications for mammalian limb growth and locomotor development

Jesse W. Young

Department of Anthropology, University of Texas at Austin, Austin, TX 78712, USA

View larger version (21K): [in this window] [in a new window]   Fig. 1. Path diagrams specifying the hypothesized influence of limb length, joint posture, limb posture and substrate reaction force (SRF) orientation on joint load arm length. (A) Shoulder, (B) elbow, (C) hip and (D) knee joints. (E) A schematic representation of average forelimb and hind limb postures across the current dataset to help visualize the predicted effects of variation in posture and SRF orientation on load arm lengths. Red and blue lines indicate the average orientation of forelimb and hind limb SRF, respectively. Within the path diagrams, single-headed arrows indicate a directed causal link between predictor variables and moment arm lengths. Double-headed arrows indicate an undirected correlation between predictor variables. Red + and – symbols indicate the predicted direction of the relationship. For all joints, limb length was predicted to have a positive effect on load arm length. Because joint extension is a well-established means of shortening joint load arms (Gray, 1968; Biewener, 1989), larger, more extended, joint angles were predicted to decrease joint load arm lengths. The influence of limb angles was predicted to vary according to limb and joint (cf.E). Increasing forelimb protraction and hind limb retraction while maintaining SRF orientation should bring the limb axis more in line with the SRF vector, thus shortening shoulder/hip load arms but increasing the distance between the middle joint and the SRF vector and lengthening elbow/knee load arms. Similarly, cranial deviation of forelimb SRF angles should decrease shoulder load arm lengths and increase elbow load arm lengths, whereas caudal deviation of hind limb SRF angles should increase hip load arm lengths but increase knee load arm lengths.

View larger version (8K): [in this window] [in a new window]   Fig. 2. Body mass plotted against age for all infant Saimiri boliviensis. Body mass was strongly positively correlated with age in each infant. Red circles, animal 4428 (r=0.957); purple circles, animal 4433; yellow circles, animal 4445 (r=0.938); green circles, animal 4466 (r=0.855); blue circles, animal 4475 (r=0.977); orange circles, animal 4483 (r=0.947). A correlation coefficient was not computed for animal 4433 because of this animal's limited participation in the study.

View larger version (40K): [in this window] [in a new window]   Fig. 3. Allometry of limb growth in Saimiri boliviensis. Data are plotted on log–log axes. Black lines indicate the calculated reduced major axis (RMA) slopes for each segment computed across individuals. Dashed gray lines indicate isometry. Forelimbs and forelimb segments are represented by circles whereas hind limbs and hind limb segments are represented by diamonds. Color codes for individual monkeys follow Fig. 1. Graphs are plotted on the same scale to indicate absolute differences in segment length. Allometric regression equations and coefficients of determination (i.e. R2 values) are provided for each relationship at the bottom of the plot.

View larger version (46K): [in this window] [in a new window]   Fig. 4. Scatter plots of absolute joint moment magnitudes versus body mass in all substrate and gait conditions. The gray horizontal bar indicates the division between positive flexing moments and negative extending moments.

View larger version (30K): [in this window] [in a new window]   Fig. 5. Path analyses of the influences of limb length, posture and substrate reaction force (SRF) direction on (A) shoulder, (B) elbow, (C) hip and (D) knee joint load arm lengths during locomotion on the ground. Values in parentheses next to the path coefficients are the percentage of load arm length variance uniquely explained by each predictor variable, as determined by hierarchical partitioning. Gray shading indicates that the path or variance partition was not significant. 2 tests of model fit are also presented for each joint. The total coefficient of determination (R2) for each model is also shown in bold red type.

View larger version (30K): [in this window] [in a new window]   Fig. 6. Path analyses of the influences of limb length, posture, and substrate reaction force (SRF) direction on joint load arm lengths during locomotion on the pole. Data presented as in Fig. 5.

View larger version (7K): [in this window] [in a new window]   Fig. 7. Angular frequency histograms (Batschelet, 1981) of metacarpal and metatarsal elevation angles relative to the horizontal axis. Filled circles on the perimeter of the plot indicate mean elevation angles.

View larger version (55K): [in this window] [in a new window]   Fig. 8. Scaling of limb growth in primates and other mammalian taxa. In each set of bar graphs, the left hand panels represent complete limbs or stylopodia/zeugopodia (i.e. arms, forearms, thighs or legs) and right-hand panels represent autopodia (metacarpals/metatarsals or complete hands and feet). Forelimb segments are distinguished by lighter shading. Except where indicated by the asterisks next to the species name, allometric exponents were calculated from reduced major axis regressions of segment length on body mass. 95% confidence intervals on the exponents are shown where available. Dashed lines indicate isometry (i.e. slope equal to 0.333). Data sources: Propithecus tattersalli [golden-crowned sifaka (Ravosa et al., 1993)] Propithecus diadema [diademed sifaka (Ravosa et al., 1993)]; Propithecus verreauxi [Verreaux's sifaka (Lawler, 2006)]; Saimiri boliviensis [Bolivian squirrel monkey (this study)]; Cebus albifrons [white-fronted capuchin monkey (Jungers and Fleagle, 1980)]; Cebus apella [tufted capuchin monkey (Jungers and Fleagle, 1980)]; Papio cynocephalus [yellow baboon (Raichlen, 2005)]; Chlorocebus aethiops [vervet monkey (Turner et al., 1997)]; Hylobates lar [white-handed gibbon (Jungers and Cole, 1992)]; Pan troglodytes [common chimpanzee (Hartwig-Scherer and Martin, 1992)]; Gorilla gorilla [gorilla (Hartwig-Scherer and Martin, 1992)]; Pongo pygmaeus [orangutan (Hartwig-Scherer and Martin, 1992)]; Monodelphis domestica [gray short-tailed opossum (Lammers and German, 2002)]; Trichosurus vulpecula [brushtail possum (Lentle et al., 2006)]; Chinchilla lanigera [chinchilla (Lammers and German, 2002)]; Orytolagus cuniculus [domestic white rabbit (Lammers and German, 2002)]; Lepus californicus [black-tailed jackrabbit (Carrier, 1983)]; Rattus norvegicus [rat (Lammers and German, 2002)]; Galea musteloides [cui (Schilling and Petrovitch, 2006)]; Felis domesticus [domestic cat (Carrier, 1983)]; Tupaia glis [tree shrew (Schilling and Petrovitch, 2006)]; Sus scrofa [domestic pig (Liu et al., 1999)]; Ovibos moschatus [musk ox (Heinrich et al., 1999)].

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