Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs

Allosaurus is one of the most common Mesozoic theropod dinosaurs. We present a histological analysis to assess its growth strategy and ontogenetic limb bone scaling. Based on an ontogenetic series of humeral, ulnar, femoral, and tibial sections of fibrolamellar bone, we estimate the ages of the largest individuals in the sample to be between 13-19 years. Growth curve reconstruction suggests that maximum growth occurred at 15 years, when body mass increased 148 kg/year. Based on larger bones of Allosaurus, we estimate an upper age limit of between 22-28 years of age, which is similar to preliminary data for other large theropods. Both Model I and Model II regression analyses suggest that relative to the length of the femur, the lengths of the humerus, ulna, and tibia increase in length more slowly than isometry predicts. That pattern of limb scaling in Allosaurus is similar to those in other large theropods such as the tyrannosaurids. Phylogenetic optimization suggests that large theropods independently evolved reduced humeral, ulnar, and tibial lengths by a phyletic reduction in longitudinal growth relative to the femur.     

Postcranial adaptations for climbing in Loridae (Primates)

The Loridae are an arboreal family of small primates that are specialized for slow and quiet climbing. This paper examines the relationship between lorid locomotory behaviour and postcranial skeletal morphology. Lorid humeral and femoral diaphyseal geometric cross-sectional properties, articular surface areas, and lengths are compared to those properties in other small primates with less specialized locomotory behaviour. The comparative sample includes both closely related prosimians and more distantly related platyrrhines.
Results indicate that lorids have greater humeral and femoral diaphyseal rigidity than other quadrupedal primates of similar body size, suggesting that lorid limbs are subjected to greater forces. Lorids also have relatively larger humeral and femoral articulations, corresponding to field and laboratory observations which indicate that lorid joints are highly mobilc. In addition, lorids have long humeri relative to femoral length, and compared to humeral length in less specialized prosimians of similar body mass. Long humeral length relative to femoral length is interpreted as a climbing adaptation because similar limb proportions are also seen in many non-primate climbers. Altogether, humeral and femoral diaphyseal cross-sectional properties, articular surface areas, and lengths comprise a suite of characters which have potential for identifying climbing specialists in the fossil record.     

Ontogenetic changes in limb bone structural proportions in mountain gorillas (Gorilla beringei beringei)

Behavioral studies indicate that adult mountain gorillas (Gorilla beringei) are the most terrestrial of all nonhuman hominoids, but that infant mountain gorillas are much more arboreal. Here we examine ontogenetic changes in diaphyseal strength and length of the femur, tibia, humerus, radius, and ulna in 30 Virunga mountain gorillas, including 18 immature specimens and 12 adults. Comparisons are also made with 14 adult western lowland gorillas (Gorilla gorilla gorilla), which are known to be more arboreal than adult mountain gorillas. Infant mountain gorillas have significantly stronger forelimbs relative to hind limbs than older juveniles and adults, but are nonsignificantly different from western lowland gorilla adults. The change in inter-limb strength proportions is abrupt at about two years of age, corresponding to the documented transition to committed terrestrial quadrupedalism in mountain gorillas. The one exception is the ulna, which shows a gradual increase in strength relative to the radius and other long bones during development, possibly corresponding to the gradual adoption of stereotypical fully pronated knuckle-walking in older juvenile gorillas. Inter-limb bone length proportions show a contrasting developmental pattern, with hind limb/forelimb length declining rapidly from birth to five months of age, and then showing no consistent change through adulthood. The very early change in length proportions, prior to significant independent locomotion, may be related to the need for relatively long forelimbs for climbing in a large-bodied hominoid. Virunga mountain gorilla older juveniles and adults have equal or longer forelimb relative to hind limb bones than western lowland adults. These findings indicate that both ontogenetically and among closely related species of Gorilla, long bone strength proportions better reflect actual locomotor behavior than bone length proportions.     

Limb growth in captive Galago senegalensis: getting in shape to be an adult

Since primate infants are not simply miniature adults, adult shape results from differential growth patterns of individual body segments. Initially an infant relies on its mother for transportation, and later begins independent locomotion. Skeletal growth patterns must meet the functional demands of independent locomotion. In this study we sought to determine whether Galago senegalensis braccatus follow the general primate pattern of decreasing intermembral index (IMI) throughout ontogeny. We also asked whether ontogenetic attainment of adult limb proportions coincides with attainment of independent locomotion, i.e., do infants reach adult limb proportions near the time they begin independent locomotion (approximately 7 weeks of age)? Mixed‐longitudinal data were taken from a sample of 10 captive‐born Galago senegalensis. Linear lengths of the trunk, arm, forearm, thigh, and leg were measured in the animals from birth until they were approximately 500 days old. The IMI and the ratio of each limb segment to both trunk length and the cube root of body mass were calculated. The results of a Mann‐Whitney Wilcoxon rank‐sum test for unmatched samples indicate that G. senegalensis do exhibit the primate pattern of decreasing IMI throughout ontogeny, and that the IMIs of infants at the time of initial locomotor independence are significantly higher than those of adult IMIs. Some (but not all) measures of relative limb lengths differed between neonates or 7‐week‐old infants and adults. Therefore, the hypothesis that infants acquire adult limb proportions by the time they begin independent locomotion is not supported by this study. The current results indicate that ontogenetic shape changes in galagos are a complex process and apparently cannot be explained by simple initial locomotor competency. Am. J. Primatol. 69:103–111, 2007. © 2006 Wiley‐Liss, Inc.     

Developmental basis of limb length in rodents: evidence for multiple divisions of labor in mechanisms of endochondral bone growth

SUMMARY Mammals are remarkably diverse in limb lengths and proportions, but the number and kind of developmental mechanisms that contribute to length differences between limb bones remain largely unknown. Intra- and interspecific differences in bone length could result from variations in the cellular processes of endochondral bone growth, creating differences in rates of chondrocyte proliferation or hypertrophy, variation in the shape and size of chondrocytes, differences in the number of chondrocytes in precursor populations and throughout growth, or a combination of these mechanisms. To address these questions, this study compared cellular mechanisms of endochondral bone growth in cross-sectional ontogenetic series of the appendicular skeleton of two rodent species: the mouse ( Mus musculus ) and Mongolian gerbil ( Meriones unguiculatus ). Results indicate that multiple cellular processes of endochondral bone growth contribute to phenotypic differences in limb bone length. The data also suggest that separate developmental processes contribute to intraspecific length differences in proximal versus distal limb bones, and that these proximo-distal mechanisms are distinct from mechanisms that contribute to interspecific differences in limb bone length related to body size. These developmental "divisions of labor" are hypothesized to be important features of vertebrate limb development that allow (1) morphology in the autopods to evolve independently of the proximal limb skeleton, and (2) adaptive changes in limb proportions related to locomotion to evolve independently of evolutionary changes in body size.     

Skeletal growth in early and late Neolithic foragers from the Cis‐Baikal region of Eastern Siberia

Skeletal growth is explored between Early Neolithic (EN) (8000 to 6800 BP) and Late Neolithic (LN) (6000 to 5200 BP) foragers from the Cis‐Baikal region of Eastern Siberia. Previous studies suggest that increased systemic stress and smaller adult body size characterize the EN compared to LN. On this basis, greater evidence for stunting and wasting is expected in the EN compared to LN. Skeletal growth parameters assessed here include femoral and tibial lengths, estimated stature and body mass, femoral midshaft cortical thickness, total bone thickness, and medullary width. Forward selection was used to fit polynomial lines to each skeletal growth parameter relative to dental age in the pooled samples, and standardized residuals were compared between groups using t tests. Standardized residuals of body mass and femoral length were significantly lower in the EN compared to LN sample, particularly from late infancy through early adolescence. However, no significant differences in the standardized residuals for cortical thickness, medullary width, total bone thickness, tibial length, or stature were found between the groups. Age ranges for stunting in femoral length and wasting in body mass are consistent with environmental perturbations experienced at the cessation of breast feeding and general resource insecurity in the EN compared to LN sample. Differences in relative femoral but not tibial length may be associated with age‐specific variation in growth‐acceleration for the distal and proximal limb segments. Similarity in cortical bone growth between the two samples may reflect the combined influences of systemic and mechanical factors on this parameter. Am J Phys Anthropol 153:377–386, 2014. © 2013 Wiley Periodicals, Inc.     

Effects of experimental hyperadrenocorticism on the growth of the femur and tibia in normal and bipedal rats

Daily subcutaneous injections of glucocorticoid preparations have been shown to produce clinical signs of hyperadrenocorticism which resulted in interference with the growth of rats, shown by measurements both of body weight and of the length of long bones. The purpose of this study was to see if increased, intermittent, compressive forces, produced by experimental bipedalism, would mitigate the negative effects of cortisone injections on long bone growth and if there would be a difference in reaction between male and female rats. Male and female Sprague-Dawley rats were used for control, cortisone-injected, and cortisone-injected plus bipedal groups. Experimental bipedalism was produced at 10 days of age; cortisone injections began at 30 days of age; all animals were sacrificed at 65 days of age. Tibial and femoral lengths were measured. The results do not support the hypothesis that bipedalism can be instrumental in mitigating the effects of hyperadrenocorticism on hindlimb long bone growth.     

Functional and ecological significance of relative growth in Alligator

Allometric coefficients are calculated for 27 cranial and 39 postcranial measurements of a growth series of Alligator mississipiensis that spans a size range of an order of magnitude. Developmental patterns are quite-well canalized, as expressed in coefficients of variation of 8 to 10 for isometric variables. A multivariate expression of allometry is discovered using principal components analysis. A number of allometric coefficients have expression in known aspects of the life history of Alligator. Negative allometry of limb lengths and limb proportions shows an ontogenetic decrease in importance of the limbs throughout life, and observations show large animals to be more dependent on water than small ones. Isometry of skull length with respect to body length represents an adaptation to ever-increasing size of prey items as body size increases. Positive allometry of snout length and size of the upper temporal fenestrae finds parallel in the structure of the highly aquatic gavial.     

THE EVOLUTION OF BIPEDALISM IN JERBOAS (RODENTIA: DIPODOIDEA): ORIGIN IN HUMID AND FORESTED ENVIRONMENTS

Mammalian bipedalism has long been thought to have arisen in response to arid and open environments. Here, we tested whether bipedalism coevolved with environmental changes using molecular and paleontological data from the rodent superfamily Dipodoidea and statistical methods for reconstructing ancestral characteristics and past climates. Our results show that the post‐Late Miocene aridification exerted selective pressures on tooth shape, but not on leg length of bipedal jerboas. Cheek tooth crown height has increased since the Late Miocene, but the hind limb/head‐body length ratios remained stable and high despite the environmental change from humid and forested to arid and open conditions, rather than increasing from low to high as predicted by the arid‐bipedalism hypothesis. The decoupling of locomotor and dental character evolution indicates that bipedalism evolved under selective pressure different from that of dental hypsodonty in jerboas. We reconstructed the habitats of early jerboas using floral and faunal data, and the results show that the environments in which bipedalism evolved were forested. Our results suggest that bipedalism evolved as an adaptation to humid woodlands or forests for vertical jumping. Running at high speeds is likely a by‐product of selection for jumping, which became advantageous in open environments later on.     

Sexual dimorphism in growth in the relative length of the forearm and relative knee height during adolescence

There are numerous studies concerning sexual dimorphism in body proportions, but only a few have investigated growth in the relative length of particular segments of the upper and lower limbs during adolescence. The aim of the study is an assessment of sex differences of longitudinal growth in the relative length of the forearm and knee height among adolescents. Sample involved 121 boys and 111 girls, participants of the Wroclaw Growth Study, examined annually between 8 and 18 years of age. Sexual dimorphism in six ratios: forearm length and knee height relatively to: trunk, height, and limb length were analyzed using a two‐way analysis of variance with repeated measurements. The sex and age relative to an estimate of maturity timing (3 years before, and after age class at peak height velocity [PHV]) were independent variables. All of the ratios showed significant sex differences in interaction with age relative to age at PHV. The relative length of the forearm, in boys, did not change significantly with the years relative to age at PHV, whereas in girls, was the lowest in the two first age classes and afterward significantly increased just 1 year before and during the adolescent growth spurt, remaining unchanged in further age classes. For relative knee height no clear pattern for sex differences was noticed. It is proposed that relatively longer forearms, particularly in relation to the trunk in girls, could have evolved as an adaptation to more efficient infant carrying and protection during breastfeeding.     

The Regourdou 1 Neandertal body size

In order to maximize sample sizes for the assessment of body size and proportions among Late Pleistocene humans, the femoral head diameter of the Regourdou 1 Neandertal was estimated from its ischial acetabular lunate surface, so as to provide a reliable measure for body mass assessment. This estimate was accomplished by fitting a sphere to the 3D surface of the acetabulum and then estimating femoral head diameter using a regression of acetabular sphere diameter to femoral head diameter based on associated recent human femora and ossa coxarum. The resultant mean and range of values for the Regourdou 1 femoral head dimension place it among the smaller of the European and southwest Asian Neandertals, although its humeral length is above average for that sample. Regourdou 1 therefore joins Kebara 2 in having moderately long arms for body core size, and it thereby emphasizes the variation in Neandertal body proportions.     

Adult proportionality in small-bodied foragers: a test of ecogeographic expectations

If predictable, ecogeographic patterning in body size and proportions of human populations can provide valuable information regarding human biology, adaptation to local environments, migration histories, and health, now and in the past. This paper evaluates the assumption that small-bodied Later Stone Age (LSA) foragers of Southern Africa show the adult proportions that would be expected of warm-adapted populations. Comparisons are also made with small-bodied foragers from the Andaman Islands (AI). Indices including brachial, crural, limb element length to skeletal trunk height, and femoral head and bi-iliac breadth to femoral length were calculated from samples of LSA (n = 124) and AI (n = 31) adult skeletons. Samples derived from the literature include those from high (Europe), middle (North Africa), and low (Sub-Saharan Africa) latitude regions. The LSA and AI samples match some but not all expected ecogeographic patterns for their particular regions of long term habitation. For most limb length to skeletal trunk height indices the LSA and AI are most similar to the other mid-latitude sample (North Africans). However, both groups are similar to low latitude groups in their narrow bi-iliac breadths, and the AI display relatively long radii. Proportions of LSA and AI samples also differ from those of African pygmies. In regions like southern-most Africa, that do not experience climatic extremes of temperature or humidity, or where small body size exists through drift or selection, body size, and proportions may also be influenced by nonclimatic variables, such as energetic efficiency.     

Femoral/humeral strength in early African Homo erectus

Lower-to-upper limb-bone proportions give valuable clues to locomotor behavior in fossil taxa. However, to date only external linear dimensions have been included in such analyses of early hominins. In this study, cross-sectional measures of femoral and humeral diaphyseal strength are determined for the two most complete early Homo erectus (or ergaster) associated skeletons--the juvenile KNM-WT 15000 and the adult KNM-ER 1808. Modern comparative samples include an adult human skeletal sample representative of diverse body shapes, a human longitudinal growth series, and an adult chimpanzee sample. When compared to appropriately age-matched samples, both H. erectus specimens fall very close to modern human mean proportions and far from chimpanzee proportions (which do not overlap with those of humans). This implies very similar mechanical load-sharing between the lower and upper limbs, and by implication, similar locomotor behavior in early H. erectus and modern humans. Thus, by the earliest Pleistocene (1.7 Ma), completely modern patterns of bipedal behavior were fully established in at least one early hominin taxon.     

Physical anthropology: Human evolution. By Ivan G. Pawson. Wiley,New York. 1977. x + 246 pp., figures,tables, index. $4.95 (paper)

Growth is marked by changes in body shape as well as increase in body size. It is suggested that changes in body shape in childhood and adolescence be analyzed by least squares fit lines for one dimension on a second at successive ages. These are preferred during childhood to the traditional indices of anthropologists because body proportions change with growth, and one can identify the direction of the change and observe which body dimension is changing, or if both are. Furthermore, populations may be compared by analysis of covariance for different patterns of growth related to sex and ethnic groups. Analysis of a number of populations have demonstrated clear differences between the sexes and between populations for the following body proportions: sitting height to leg length, arm length to leg length, biacromial width to biiliac width.     

The influence of body proportions on femoral and tibial midshaft shape in hunter‐gatherers

Variation in femoral and tibial diaphyseal shape is used as an indicator of adaptation to patterns of terrestrial mobility. Recent experimentation has implied that lower limb diaphyseal shape may be primarily influenced by lower limb length, and less so by mobility patterns. If valid, this would, at most, render previous interpretations of mobility patterns based on analyses of diaphyseal shape questionable, and, at least, require additional standardization that considers the influence of limb length. Although the consequences could be profound, this implication has yet to be directly tested. Additionally, the influence of body breadth on tibial shape (and to a lesser extent femoral shape) remains uncertain. Tibial and femoral cross‐sectional midshaft shape measurements, taken from nine Pleistocene and Holocene skeletal populations, were compared against lower limb length, limb segment length, and bi‐iliac breadth. Generally, limb length and limb segment length do not significantly influence femoral or tibial midshaft shape. After controlling for body mass greater bi‐iliac breadth is associated with a relative mediolateral strengthening of the femoral midshaft, while the influence of a wider body shape (BIB/length) is associated with a relative M‐L strengthening of the tibia and femur of males, and the tibia of females. We conclude that; (1) mechanical interpretations of lower limb diaphyseal shape are most parsimonious due to the lack of evidence for a consistent relationship between segment length and shape; however, (2) further work is required to investigate the influence of bi‐iliac breadth on both femoral and tibial midshaft shape. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

Bipedal locomotion: effects of speed, size and limb posture in birds and humans

Seven species of ground-dwelling birds (body mass range: 0.045-90 kg) were filmed while walking and running on a treadmill. High-speed light films were also taken of humans to compare kinematic patterns of avian with human bipedalism. Consistent patterns of stride frequency, stride length, step length, duty factor and limb excursion were observed in all species, with most of the variation among species being due to differences in body size. In general, smaller bipeds have higher stride frequencies (α M ^−0.18), shorter stride lengths (α M ^0.38) and more limited ranges of speed within each gait than large bipeds. After normalizing for size (based on Froude number, after Alexander, 1977), remaining kinematic variation is largely due to interspecific differences in posture and relative limb segment lengths. For their size, smaller bipeds have greater step lengths, limb excursion angles and duty factors than large bipeds because of their more crouched posture and greater effective limb length. The most notable differences in limb kinematics between birds and humans occur at the walk-run transition and are maintained as running speed increases. Change of gait is smooth and difficult to discern in birds, but distinct in humans, involving abrupt decreases in step length and duty factor (time of contact) and a corresponding increase in limb swing time. These differences appear to reflect a spring-like run that is stiff in humans (favouring elastic energy recovery) but more compliant in birds (increasing time of ground contact). Differences between birds and humans in balance of the body's centre of mass not only affect femoral orientation and motion, but also affect pattern of limb excursion with speed.     

Body Mass Estimates in Extinct Mammals from Limb Bone Dimensions: the Case of North American Hyaenodontids

The body mass estimation of several limb bone dimensions (shaft cross-sectional properties, articular sizes, and bone lengths) were examined using bivariate linear regression analyses. The sample included taxonomically and behaviourally diverse small to medium-sized Recent carnivorans and carnivorous marsupials. All examined limb bone dimensions indicated low errors (percentage standard error of estimate, 8–13) for the body mass estimations. Among them, humeral and femoral shaft properties correlated best with body weight, while limb bone lengths gave larger errors. Both humeral and femoral head dimensions have relatively large individual variations, and distal humeral articular dimensions seem to be influenced more by phylogenetic differences. The regressions based on each locomotor group gave slightly lower errors than those based on the total pooled sample. The results were then applied to hyaenodontid creodonts from the Eocene–Oligocene of North America. The estimated body masses (kg) are: Arfia , 5.4–9.5; Prototomus , <6.0; Pyrocyon , 2.6; Sinopa , 1.3–1.4; Tritemnodon , 7.6–13; Prolimnocyon , 1.6; Thinocyon , 0.7–2.5; Machaeroides , 12; Limnocyon , 7.8– 16; Hyaenodon , 9.1–43. The various limb bone dimensions give different body mass values, but the variation in estimates is smaller compared to those derived from dental or cranial measurements.     

Ontogeny and limb bone scaling in two new world marsupials,Monodelphis domestica and Didelphis virginiana

This study examines the growth of two species of marsupials who share common ancestry and are born at the same neonatal size of a little less than 1 g. Despite this similarity at birth, adult size of these two species differs by about 50 times, with the smaller species believed to be the more ancestral. We quantified the growth in the limb bones (humerus, femur, ulna, tibia, metacarpal, and metatarsal) beginning around 40 days of age until adult size was reached. Results indicate that the larger species grows at a higher rate of growth as well as for a longer period of time to reach its larger adult size. Despite these differences in growth, there were few differences observed in the scaling over time of length to width in the various limb bones that were measured. The two species, although different in their adult size and the patterns of growth, maintain the same length to width proportions in each limb bone. The biggest difference between species in scaling was observed in the bones of the hands and feet, which may suggest adaptation to size and/or locomotor performance as body size increases. Despite variation in size, these heterochronic patterns do not affect the shape among adults or over evolutionary time. J Morphol 231:117–130, 1997. © 1997 Wiley-Liss, Inc.     

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum

Allometric relationships describe the proportional covariation between morphological, physiological, or life‐history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size‐related changes in the selection pressures acting on horn length and body mass.