Anatomical and biomechanical traits of broiler chickens across ontogeny. Part I. Anatomy of the musculoskeletal respiratory apparatus and changes in organ size.

Genetic selection for improved meat yields, digestive efficiency and growth rates have transformed the biology of broiler chickens. Modern birds undergo a 50-fold multiplication in body mass in just six weeks, from hatching to slaughter weight. However, this selection for rapid growth and improvements in broiler productivity is also widely thought to be associated with increased welfare problems as many birds suffer from leg, circulatory and respiratory diseases. To understand growth-related changes in musculoskeletal and organ morphology and respiratory skeletal development over the standard six-week rearing period, we present data from post-hatch cadaveric commercial broiler chickens aged 0, 2, 4 and 6 weeks. The heart, lungs and intestines decreased in size for hatch to slaughter weight when considered as a proportion of body mass. Proportional liver size increased in the two weeks after hatch but decreased between 2 and 6 weeks. Breast muscle mass on the other hand displayed strong positive allometry, increasing in mass faster than the increase in body mass. Contrastingly, less rapid isometric growth was found in the external oblique muscle, a major respiratory muscle that moves the sternum dorsally during expiration. Considered together with the relatively slow ossification of elements of the respiratory skeleton, it seems that rapid growth of the breast muscles might compromise the efficacy of the respiratory apparatus. Furthermore, the relative reduction in size of the major organs indicates that selective breeding in meat-producing birds has unintended consequences that may bias these birds toward compromised welfare and could limit further improvements in meat-production and feed efficiency.

Anatomical and biomechanical traits of broiler chickens across ontogeny. Part II. Body segment inertial properties and muscle architecture of the pelvic limb.

In broiler chickens, genetic success for desired production traits is often shadowed by welfare concerns related to musculoskeletal health. Whilst these concerns are clear, a viable solution is still elusive. Part of the solution lies in knowing how anatomical changes in afflicted body systems that occur across ontogeny influence standing and moving. Here, to demonstrate these changes we quantify the segment inertial properties of the whole body, trunk (legs removed) and the right pelvic limb segments of five broilers at three different age groups across development. We also consider how muscle architecture (mass, fascicle length and other properties related to mechanics) changes for selected muscles of the pelvic limb. All broilers used had no observed lameness, but we document the limb pathologies identified post mortem, since these two factors do not always correlate, as shown here. The most common leg disorders, including bacterial chondronecrosis with osteomyelitis and rotational and angular deformities of the lower limb, were observed in chickens at all developmental stages. Whole limb morphology is not uniform relative to body size, with broilers obtaining large thighs and feet between four and six weeks of age. This implies that the energetic cost of swinging the limbs is markedly increased across this growth period, perhaps contributing to reduced activity levels. Hindlimb bone length does not change during this period, which may be advantageous for increased stability despite the increased energetic costs. Increased pectoral muscle growth appears to move the centre of mass cranio-dorsally in the last two weeks of growth. This has direct consequences for locomotion (potentially greater limb muscle stresses during standing and moving). Our study is the first to measure these changes in the musculoskeletal system across growth in chickens, and reveals how artificially selected changes of the morphology of the pectoral apparatus may cause deficits in locomotion.

The gait dynamics of the modern broiler chicken: a cautionary tale of selective breeding.

One of the most extraordinary results of selective breeding is the modern broiler chicken, whose phenotypic attributes reflect its genetic success. Unfortunately, leg health issues and poor walking ability are prevalent in the broiler population, with the exact aetiopathogenesis unknown. Here we present a biomechanical analysis of the gait dynamics of the modern broiler and its two pureline commercial broiler breeder lines (A and B) in order to clarify how changes in basic morphology are associated with the way these chickens walk. We collected force plate and kinematic data from 25 chickens (market age), over a range of walking speeds, to quantify the three-dimensional dynamics of the centre of mass (CoM) and determine how these birds modulate the force and mechanical work of locomotion. Common features of their gait include extremely slow walking speeds, a wide base of support and large lateral motions of the CoM, which primarily reflect changes to cope with their apparent instability and large body mass. These features allowed the chickens to keep their peak vertical forces low, but resulted in high mediolateral forces, which exceeded fore-aft forces. Gait differences directly related to morphological characteristics also exist. This was particularly evident in Pureline B birds, which have a more crouched limb posture. Mechanical costs of transport were still similar across all lines and were not exceptional when compared with more wild-type ground-running birds. Broiler chickens seem to have an awkward gait, but some aspects of their dynamics show rather surprising similarities to other avian bipeds.

The effects of selective breeding on the architectural properties of the pelvic limb in broiler chickens: a comparative study across modern and ancestral populations.

Intensive artificial selection has led to the production of the modern broiler chicken, which over the last few decades has undergone a dramatic increase in growth rate and noticeable changes in body conformation. Unfortunately, this has been associated with musculoskeletal abnormalities which have altered the walking ability of these birds, raising obvious welfare concerns, as well as causing economic losses. Here we present a comparative study of ancestral and derived muscle anatomy in chickens to begin to tease apart how evolutionary alterations of muscle form in chickens have influenced their locomotor function and perhaps contributed to lameness. We measured the muscle architectural properties of the right pelvic limb in 50 birds, including the Giant Junglefowl, a commercial strain broiler and four pureline commercial broiler breeder lines (from which the broiler populations are derived) to identify which features of the broiler's architectural design have diverged the most from the ancestral condition. We report a decline in pelvic limb muscle mass in the commercial line birds that may compromise their locomotor abilities because they carry a larger body mass. This greater demand on the pelvic limb muscles has mostly led to changes in support at the hip joint, revealing significantly larger abductors and additionally much larger medial rotators in the broiler population. Differences were seen within the commercial line bird populations, which are likely attributed to different selection pressures and may reflect differences in the walking ability of these birds. In addition, Junglefowl seem to have both greater force-generating capabilities and longer, presumably faster contracting muscles, indicative of superior musculoskeletal/locomotor function. We have provided baseline data for generating hypotheses to investigate in greater depth the specific biomechanical constraints that compromise the modern broiler's walking ability and propose that these factors should be considered in the selection for musculoskeletal health in the chickens of the future. Our new anatomical data for a wide range of domestic and wild-type chickens is useful in a comparative context and for deeper functional analysis including computer modelling/simulation of limb mechanics.

Variation in center of mass estimates for extant sauropsids and its importance for reconstructing inertial properties of extinct archosaurs.

Inertial properties of animal bodies and segments are critical input parameters for biomechanical analysis of standing and moving, and thus are important for paleobiological inquiries into the broader behaviors, ecology and evolution of extinct taxa such as dinosaurs. But how accurately can these be estimated? Computational modeling was used to estimate the inertial properties including mass, density, and center of mass (COM) for extant crocodiles (adult and juvenile Crocodylus johnstoni) and birds (Gallus gallus; junglefowl and broiler chickens), to identify the chief sources of variation and methodological errors, and their significance. High-resolution computed tomography scans were segmented into 3D objects and imported into inertial property estimation software that allowed for the examination of variable body segment densities (e.g., air spaces such as lungs, and deformable body outlines). Considerable biological variation of inertial properties was found within groups due to ontogenetic changes as well as evolutionary changes between chicken groups. COM positions shift in variable directions during ontogeny in different groups. Our method was repeatable and the resolution was sufficient for accurate estimations of mass and density in particular. However, we also found considerable potential methodological errors for COM related to (1) assumed body segment orientation, (2) what frames of reference are used to normalize COM for size-independent comparisons among animals, and (3) assumptions about tail shape. Methods and assumptions are suggested to minimize these errors in the future and thereby improve estimation of inertial properties for extant and extinct animals. In the best cases, 10%-15% errors in these estimates are unavoidable, but particularly for extinct taxa errors closer to 50% should be expected, and therefore, cautiously investigated. Nonetheless in the best cases these methods allow rigorous estimation of inertial properties.

The movements of limb segments and joints during locomotion in African and Asian elephants.

As the largest extant terrestrial animals, elephants do not trot or gallop but can move smoothly to faster speeds without markedly changing their kinematics, yet with a shift from vaulting to bouncing kinetics. To understand this unusual mechanism, we quantified the forelimb and hindlimb motions of eight Asian elephants (Elephas maximus) and seven African elephants (Loxodonta africana). We used 240 Hz motion analysis (tracking 10 joint markers) to measure the flexion/extension angles and angular velocities of the limb segments and joints for 288 strides across an eightfold range of speeds (0.6-4.9 m s(-1)) and a sevenfold range of body mass (521-3684 kg). We show that the columnar limb orientation that elephants supposedly exemplify is an oversimplification--few segments or joints are extremely vertical during weight support (especially at faster speeds), and joint flexion during the swing phase is considerable. The 'inflexible' ankle is shown to have potentially spring-like motion, unlike the highly flexible wrist, which ironically is more static during support. Elephants use approximately 31-77% of their maximal joint ranges of motion during rapid locomotion, with this fraction increasing distally in the limbs, a trend observed in some other running animals. All angular velocities decrease with increasing size, whereas smaller elephant limbs are not markedly more flexed than adults. We find no major quantitative differences between African and Asian elephant locomotion but show that elephant limb motions are more similar to those of smaller animals, including humans and horses, than commonly recognized. Such similarities have been obscured by the reliance on the term ;columnar' to differentiate elephant limb posture from that of other animals. Our database will be helpful for identifying elephants with unusual limb movements, facilitating early recognition of musculoskeletal pathology.