Geometry and evolutionary parallelism in the long bones of cavioid rodents and small artiodactyls

Morphological parallelism between South American cavioid rodents and small artiodactyls from the Old World has been postulated for a long time. Our study deals with this question from the point of view of biomechanical characteristics of the long bones. For this, cross-sectional area, second moment of the area, polar moment, athletic ability indicators and strength were calculated for the long bones (i.e. humerus, radius, femur and tibia) of five species of cavioids and two species of artiodactyls. Regressions of all these variables to body mass were established. Regarding the cross-sectional area, the confidence intervals show that the exponents calculated are not significantly different from the geometrical predicted value. The exponents obtained for the second moment of area and the polar moment are not significantly different from the geometrical prediction, except for the humerus. The two indicators of athletic ability scaled as expected, but the bending indicator of athletic ability of the femur was not correlated to body mass. The exponent calculated for femur strength is not different from zero, while the strength of the humerus decreases slightly with the body mass. Additional statistical tests (ANCOVAs) showed no difference between the values of these variables calculated for the samples studied of artiodactyls and rodents. The present results are consistent with the hypothesis that there is significant evolutionary parallelism between cavioid rodents and small artiodactyls.     

Structural and mechanical indicators of limb specialization in primates

The structural mechanics of femora and humeri from primates representing a wide spectrum of habitual locomotor activities were examined to determine how cross-sectional properties vary with functional specializations of the extremities. Average bending rigidities of the midshaft of humerus and femur were measured in 60 individuals of four nonhuman primate species (Macaca nemestrina, Macaca fascicularis, Presbytis cristata, Hylobates lar) using single-beam photon absorptiometry. Linear regression analyses of the loge transformed data were used to assess the relative usage of the forelimb and hindlimb in propulsion and weight bearing, and to evaluate deviations from generalized mammalian quadrupedalism. The results suggest that average bending rigidities of the humerus and femur in primates reflect the extent to which the forelimb and hindlimb are used differently in locomotion; deviations of average bending rigidity from geometric similarity indicate functional variations from generalized mammalian quadrupedalism and the ratio of humeral to femoral bending rigidity can be used to identify trends towards hindlimb or forelimb dominance in locomotion and can be employed in general to determine how the limb was used.     

Primate limb bones and locomotor types in arboreal or terrestrial environments

Postcranial limb bones were compared among primates of different locomotor types. Seventy-one primate species, in which all families of primates were included, were grouped into nine locomotor types. Osteometrical data on long bones and data on the cross-sectional geometry of the humerus and the femur were studied by means of allometric analysis and principal component analysis. Relatively robust forelimb bones were observed in the primate group which adopted the relatively terrestrial locomotor type compared with the group that adopted the arboreal locomotor type. The difference resembled the previously reported comparison between terrestrial and arboreal groups among all quadrupedal mammals. The degree of arboreality in daily life is connected with the degree of hindlimb dominance, or the ratio of force applied to the fore- and hindlimb in positional behaviour and also with the shape, size and robusticity of limb bones.     

Skeletal allometry and interlimb scaling patterns in mustelid carnivorans

To address the effects of an evolutionary increase in body size on long bone skeletal allometry, scaling patterns relating body mass, bone length, limb length, midshaft diameters, and cross-sectional properties of the humerus and femur were analyzed for four species of scansorial mustelids. Humeral and, to a lesser extent, femoral allometry is consistent with expectations of elastic similarity: bone and limb length scale with negative allometry on body mass while bone robusticity (cross-sectional parameters against bone length) scales with strong positive allometry. Differences between fore- and hindlimb scaling patterns, however, are observed, with size-dependent increases in forelimb length and humeral strength and robusticity exceeding those of the hindlimb and femur. It is hypothesized that this greater fore- than hindlimb lengthening results in postural modifications that serve to straighten the hindlimb of larger bodied scansorial mustelids relative to smaller mustelids. Straightening of hindlimb joints would more precisely align the long axis of the femur with peak (vertical) ground reaction forces, thereby accounting for the reduction in relative bending stresses acting on the femur compared to the humerus. J. Morphol. 235:121–134, 1998. © 1998 Wiley-Liss, Inc.     

Microstructure and Cross-Sectional Shape of Limb Bones in Great Horned Owls and Red-Tailed Hawks: How Do These Features Relate to Differences in Flight and Hunting Behavior?

The Red-tailed Hawk and Great Horned Owl are two species of raptor that are similar in body size, diet, and habitat. Both species use their hindlimbs during hunting, but differ in foot morphology, how they approach and immobilize prey, and the average size of prey captured. They also differ in primary flight style: the Red-tailed Hawk uses static soaring and the Great Horned Owl uses flap-gliding. The objectives of this study were to characterize the microstructure and cross-sectional shape of limb bones of these species and examine the relationship with flight and hunting behaviors. The mid-shaft of six limb bones from six individuals of each species was sampled. The degree of bone laminarity (proportion of circular primary vascular canals) and cross-sectional geometric parameters were calculated. In both species, the humerus and femur exhibited features that suggest high resistance to torsional loading, whereas the tibiotarsus and phalanges had a shape more likely to resist compression and bending in a specific plane. The femur of the Red-tailed Hawk exhibited higher laminarity and larger polar moment of area than that of the Great Horned Owl. The tibiotarsus was more elliptical than that of the Great Horned Owl. The hawk approaches prey from a more horizontal axis, takes prey of greater mass, and is more likely to pursue prey on the ground, which could potentially be causing more torsional loads on the femur and bending loads on the tibiotarsus. In addition, differences in polar moment of area of the phalanges between the species could relate to differences in foot morphology or digit length. The humerus and ulna of the flap-gliding Great Horned Owl are more elliptical than the static soaring Red-tailed Hawk, a shape that may better resist the bending loads associated with a larger amount of flapping.     

Differentiation between fore- and hindlimb bones and locomotor behaviour in primates

Primate appendicular limb bones were measured on the cross-sectional geometry at the mid-length of the humerus and femur and on the external dimensions of long bones of the same individuals. Cross sections were directly measured by means of computer tomography or direct sectioning. The morphometry of bones and locomotor behaviour is discussed from the viewpoint of the functional differentiation between the fore- and hindlimbs. The primate group which daily adopted a relatively terrestrial locomotor type demonstrates robust forelimb bones compared with the group which adopted a fully arboreal locomotor type. In contrast, the arboreal group showed relatively large and long hindlimb bones. The difference resembled the previously reported comparison between terrestrial and arboreal groups among wholly quadrupedal mammals. Humans were more similar to the arboreal group than to the terrestrial group. Parameters of the cross-sectional geometry showed a slightly positive allometry in total primate species. Slopes of the parameters were explained by the influence of muscle force.     

Scaling of the appendicular skeleton of the giraffe (Giraffa camelopardalis)

Giraffes have remarkably long and slender limb bones, but it is unknown how they grow with regard to body mass, sex, and neck length. In this study, we measured the length, mediolateral (ML) diameter, craniocaudal (CC) diameter and circumference of the humerus, radius, metacarpus, femur, tibia, and metatarsus in 10 fetuses, 21 females, and 23 males of known body masses. Allometric exponents were determined and compared. We found the average bone length increased from 340 ± 50 mm at birth to 700 ± 120 mm at maturity, while average diameters increased from 30 ± 3 to 70 ± 11 mm. Fetal bones increased with positive allometry in length (relative to body mass) and in diameter (relative to body mass and length). In postnatal giraffes bone lengths and diameters increased iso‐ or negatively allometric relative to increases in body mass, except for the humerus CC diameter which increased with positive allometry. Humerus circumference also increased with positive allometry, that of the radius and tibia isometrically and the femur and metapodials with negative allometry. Relative to increases in bone length, both the humerus and femur widened with positive allometry. In the distal limb bones, ML diameters increased isometrically (radius, metacarpus) or positively allometric (tibia, metatarsus) while the corresponding CC widths increased with negative allometry and isometrically, respectively. Except for the humerus and femur, exponents were not significantly different between corresponding front and hind limb segments. We concluded that the patterns of bone growth in males and females are identical. In fetuses, the growth of the appendicular skeleton is faster than it is after birth which is a pattern opposite to that reported for the neck. Allometric exponents seemed unremarkable compared to the few species described previously, and pointed to the importance of neck elongation rather than leg elongation during evolution. Nevertheless, the front limb bones and especially the humerus may show adaptation to behaviors such as drinking posture. J. Morphol. 276:503–516, 2015. © 2014 Wiley Periodicals, Inc.     

Allometry and curvature in the long bones of quadrupedal mammals

The allometric relationships between basic structural proportions in long bones are examined in the humerus, radius, femur and tibia for a diverse group of 42 terrestrial quadrupedal mammals that span a size range from 0.02–6000 kg. Non-linear scaling is found for length vs. diameter in the tibia and radius, suggesting that the mechanical constraints on the skeleton differ within large and small body-size mammals. Curvature normalized to mid-shaft radius scales differently in the different long bones. Curvature is poorly related to size in the proximal limb bones (humerus and femur) while it decreases systematically with size in the tibia (mass exponent −0.13). The scaling of normalized curvature in the radius is unique among long bones. Variability of curvature in the radius is reduced at any size in comparison to that found in the other long bones. Normalized curvature is constant within the small body size group (0.02 to approximately 100 kg) while it decreases sharply with size within animals over 100 kg body mass. The unusual scaling found in the radius is probably the result of this bone's close alignment with the extrinsic forces which act on it during locomotion. The change in scaling within the radius for animals of different size may be indicative of more general size-dependent mechanical trade-offs which are masked by the complex loading circumstances of the other long bones.     

The degree and pattern of phylogenetic signal in primate long-bone structure

Interspecific scaling is a fundamental tool for comparative studies of primate long-bone structure and adaptation. However, scaling analyses based on conventional statistical methods can lead to false positives regarding adaptive relationships when traits exhibit strong phylogenetic signal. This problem can be addressed through the use of phylogenetic comparative methods (PCMs). To date, PCMs have not been incorporated into comparative studies of primate long-bone structure because it has been assumed that long-bone structure is free of phylogenetic signal once appropriately scaled. To test this assumption, we evaluated the degree of phylogenetic signal in three types of long-bone structural traits (bone length, articular surface areas, and cross-sectional geometric properties) from 17 quadrupedal primate species. We compared the pattern of phylogenetic signal in raw trait values and residual trait values after regression against body mass, bone length, and the product of body mass x bone length. Our results show that significant phylogenetic signal is present in all traits before scaling, due in part to their strong covariance with body mass. After scaling, bone length still exhibits strong phylogenetic signal, but articular surface areas do not, and cross-sectional properties exhibit different levels of signal depending on the variable used to scale the data. These results suggest that PCMs should be incorporated into interspecific studies of bone length and perhaps cross-sectional geometric properties. Our results also demonstrate that tests for phylogenetic signal prior to implementing a PCM should focus on residual variance, not individual traits.     

Body size, locomotion, and long bone cross-sectional geometry in indriid primates.

The geometry of the midshaft cross-sections of the femur and humerus of five indriid species was analysed. Internal (marrow cavity) and external diameters were measured on X-rays in the anteroposterior (a-p) and mediolateral (m-l) planes; cross-sectional areas, second moments of area, and section moduli were calculated using formulae for a hollow ellipse. Cortical thickness, robusticity indices (relating external diameters to the length of the bones), and a-p/m-l shape variables were also calculated. Model II regression was supplemented by analyses of correlation between size and shape. Indriids are saltatory, i.e., their locomotion is dominated by the hind limbs. Accordingly, the femur is more rigid than the humerus, and it shows a consistent difference between the a-p and m-l planes in measures related to bending strength. Cortical thickness varies considerably both within and across species. The type specimen of the new species Propithecus tattersalli is virtually indistinguishable from P. verreauxi on the basis of its long bone cross-sectional geometry. Femoral robusticity is uncorrelated with size, but humeral robusticity decreases significantly with increasing size. Femoral shape variables (a-p/m-l) are all negatively correlated with body size, indicating that m-l dimensions of the femur increase at a faster rate than do a-p dimensions. The highly loaded plane of movement seems to be more reinforced in the smaller species. Contrary to static biomechanical scaling predictions of positive allometry, all cross-sectional parameters scale relatively close to isometry. It is concluded that either changes in locomotor performance must compensate for the weight-related increase in forces and moments or that the larger-bodied animals operate appreciably closer to the limits of their safety margins.     

Linking structural variability in long bone diaphyses to habitual behaviors: foragers from the southern African Later Stone Age and the Andaman Islands

The cross-sectional distribution of cortical bone in long bone diaphyses is highly responsive to mechanical loading during life, yet the relationship between systemic and localized influences on skeletal structure remains unclear. This study investigates postcranial robustness throughout the body among adults from two groups of foragers with different patterns and modes of mobility, to determine whether there is evidence for upper vs. lower body localization of skeletal robustness. The samples used for this comparison are from the southern African Later Stone Age (LSA; n = 65, male = 33, female = 28) dating from ca. 10,000 to 2,000 B.P., and 19th century indigenous Andaman Islanders (AI; n = 36, male = 17, female = 16). The LSA were highly mobile foragers who did not exploit offshore marine resources. In contrast, the AI had tightly constrained terrestrial, but significant marine, mobility. Geometric properties of cortical bone distribution in the diaphyses of the clavicle, humerus, femur, tibia, and first metatarsal are compared between the samples, providing a representation of skeletal robustness throughout the body. Multivariate ANOVA shows the AI to have significantly stronger clavicles and humeri, while the LSA femora, tibiae, and first metatarsals are stronger than those of the AI. These patterns, in which upper and lower limbs show biomechanical properties that are consistent with habitual behaviors, suggest localized osteogenic response. Although postcranial robustness appears to be correlated with overall limb function, the results suggest that more proximal elements within the limb may be more responsive to mechanical loading.     

Percentage of fat adjusted for build in postmenarchal Venezuelan adolescents

Adolescence is an important period of life characterised by morphological and physiological changes that have health-related significance. In recent decades, the improved standard of living conditions, as well as a change in the pattern of intake and quality of food plus reduced levels of physical activity, have increased the levels of overweight and obesity within this age group. The current cross-sectional study was conducted on 82 postmenarchal girls aged 13–17 years, from the city of Caracas, Venezuela. The aim of the investigation was to examine the relationship between frame size and percentage of body fat. Biceps, triceps, subscapular and medial calf skinfolds, and bicondylar widths of the humerus and femur were included in the anthropometric survey. The equations of Slaughter et al. (1988) and two linear regression analyses with humerus and femur widths as independent variables were used. Percentage body fat had a low to moderate (p<0.05) correlation with humerus (r=0.39) and femur (r=0.50) width. The results suggest that build, particularly as indicated by femur width may be a useful tool in the appraisal of adiposity in girls of these ages and may be of use in further research in other age groups.     

Body mass in large extant and extinct carnivores

Body mass in six species of Plio-Pleistocene carnivores was estimated based on the relationship between mass and cross-sectional geometric properties, distal articular surface area, lengths and circumferences of proximal limb bones (femur and humerus) in 28 species of extant carnivores. All measures, except lengths, were found to give congruent body mass estimates. Two of the extinct carnivores ( Smilodon fatalis and Panthera atrox ) are estimated to be as much as one and a half times heavier than previously thought. Based on these results inferences are made concerning possible prey species.     

Scaling of long bones in ruminants with respect to the scapula

The significance of the scapula for locomotion is becoming more and more established. Studies of locomotion in small and medium‐sized mammals show a considerable amplitude of the scapula and a large contribution to step length. Taking this into account, long bone studies of forelimb movement restricted to the ‘arm’ miss one important segment. A regression model (reduced major axis) was used for analysis of a sample of 77 species of ruminants. This sample was divided according to (1) phylogenetic relationships and (2) habitat. The proximal elements of the limbs, scapula and humerus in the anterior extremity, femur in the hindlimb, show a similar scaling in the different analyses. The changes to limb proportions in the different subsamples are caused by the variability of the distal segments. The anterior extremity scales with a higher coefficient than the hindlimb in all analyses. Concepts like elastic or geometric similarity are inadequate for long bone scaling when the full range of body size in the sample is used. Taking all analyses into account, the differences in limb proportions are due more to phylogenetic relationships than to habitat.     

Influence of early qualitative feed restriction and environmental temperature on long bone development of broiler chickens

This investigation was carried out to study the influence of early qualitative feed restriction and environmental rearing temperature on long bone development in broiler. Energy and protein restriction reduced femur width and humerus weight, but did not affect tibia parameters. Broilers kept at cold environmental temperature showed reduced femur, tibia and humerus length and tibia weight, but the calculated density was not affected by rearing temperature. These findings suggest that qualitative feed restriction and environmental temperature influenced the normal long bone growth; however, bone weight/bone length index (calculated density) was not affected by rearing temperature.     

Morphometry and allometry of the primate humerus

The primate distal humerus has been used both in phylogenetic reconstruction and in assessing locomotor and postural adaptations. This study uses an allometric approach to predict locomotor patterns of extant primates regardless of phylogenetic position. By showing the relationship between form and function in living primate taxa it will be possible to use this data set to predict locomotor behavior of extinct primates. Several linear measurements were taken from the distal humerus of 71 extant primate species (anthropoids and prosimians). Allometric regressions of each measurement were performed with mandibular M₂ area as a surrogate for body size. These measurements were used to determine if significant differences in distal humerus morphology exist among locomotor groups. The results were then used to test several hypotheses about the relationship between humeral form and function. For example, the hypothesis that suspensory primates have a large medial epicondyle is confirmed; the hypothesis that terrestrial quadrupeds have a deep olecranon fossa could not be confirmed with quantitative data. In addition to this hypothesis testing, the residuals from the allometric regressions of the humeral measurements were used in a discriminant functions analysis to estimate locomotor behavior from distal humerus morphology. The discriminant functions analysis correctly reclassified 64/71 (90%) species.     

The scaling of skeletal microanatomy in non-human primates

The study of scale-correlated changes in the external dimensions and cross-sectional geometry of primate long bones is fundamental to our understanding of primate limb bone structural adaptation. To date, however, there have been no studies of the effects of mechanical loading on patterns of skeletal scaling at the microstructural level. To remedy this, we analysed patterns of microanatomical scaling in the humeri and femora of 107 adult primates belonging to the families Galagonidae and Cercopithecidae. Seven species were included in our analysis. Proximal, midshaft, and distal sections of humeri and femora of each individual were examined and secondary osteonal and cortical area were measured. Secondary osteonal area scales positively allometrically with cortical cross-sectional area and with body mass. This pattern holds generally for humeri and femora—both within and across families. However, there are striking dissimilarities in the relative strengths of the allometric coefficients for humeri and femora measured for different families. These distinctions appear to be related to differences in the ways in which fore- and hindlimbs are loaded. Such differences highlight the promise of microstructural data and the importance of examining the confounding effects of locomotory behaviour in studies of skeletal scaling.     

Postnatal growth allometry of the extremities in Cebus albifrons and Cebus apella: A longitudinal and comparative study

Cebus albifrons and Cebus apella, partially sympatric capuchin monkeys from South America, are known to differ substantially in adult body mass and bodily proportions. C. apella possesses a robust, stocky build in contrast to the more gracile, relatively longer limbed body design of C. albifrons. Average birth weights and adult body lengths of these two congeners, however, are remarkably similar and do not serve to distinguish them. This study examines longitudinal growth rates and patterns of ontogenetic scaling in the extremities (humerus, radius, hand, femur, tibia, foot) in order to document the nature and magnitude of skeletal changes associated with increasing age and body mass. Our data indicate that the growth rates of the six skeletal components of the limbs differ only slightly and somewhat inconsistently between the two species. Body mass, however, increases at a consistently faster rate in C. apella. Relative to body mass, therefore, the extremities of C. albifrons scale much faster than those of C. apella. This implies that at any given postnatal body mass, C. albifrons is longer limbed than C. apella. Conversely, C. apella is heavier than C. albifrons at any given limb length or age. We suggest that such differences in body mass distribution are causally related to differences in locomotor behavior and foraging strategies. Specifically, the relatively long-limbed C. albifrons is probably more cursorial and tends to travel longer distances each day than C. apella. C. apella is a much more deliberate quadruped and is also characterized by especially vigorous and powerful foraging and feeding behaviors. We also compare our results to other (mostly cross-sectional) studies of skeletal growth allometry in nonhuman primates.     

The inverse relationship between species diversity and body mass: do primates play by the "rules"?

Evolutionary biologists have long commented on a seemingly universal "rule" of nature-that in large taxonomic assemblages from groups as diverse as bacteria, plants, insects, marine invertebrates, fish, reptiles, amphibians, birds, and mammals, there exists a frequency distribution of body sizes among species that is highly skewed to the right (positive skewness). This distribution reflects the strong inverse, or negative, relationship often noted between mean body size of taxa and the number of species they contain--i.e., the observation that small body size is often associated with high species diversity (speciosity). This is sometimes "explained" by recourse to the idea that smaller-bodied taxa are able to subdivide their environments more finely than larger-bodied taxa. With but few exceptions, the applicability of this "rule" to the Order Primates has not been studied in any detail. In this study I address the following questions of (paleo)anthropological interest: (1) How speciose is the Order Primates? (2) Does this biological "rule" characterize the Order Primates (at any taxonomic level) in any meaningful way? (3) Does the association between speciosity and body mass within the Order Primates provide any useful models for interpreting and/or predicting speciosity in the fossil primate record? Using phylogenetically independent contrasts methods, I conclude that the answers to those three questions are: (1) not very; (2) no; and (3) not particularly (with the possible exception of larger-bodied taxa).