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Common hippopotamuses (hippos) are among the largest extant land mammals. They thus offer potential further insight into how giant body size on land influences locomotor patterns and abilities. Furthermore, as they have semi-aquatic habits and unusual morphology, they prompt important questions about how locomotion evolved in Hippopotamidae. However, basic information about how hippos move is limited and sometimes contradictory. We aimed to test if hippos trot at all speeds and if they ever use an aerial (suspended) phase, and to quantify how their locomotor patterns (footfalls and stride parameters) change with approximate speed. We surveyed videos available online and collected new video data from two zoo hippos in order to calculate the data needed to achieve our aims; gathering a sample of 169 strides from 32 hippos. No hippos studied used other than trotting (or near-trotting) footfall patterns, but at the fastest relative speeds hippos used brief aerial phases, apparently a new discovery. Hippos exhibit relatively greater athletic capacity than elephants in several ways, but perhaps not greater than rhinoceroses. Our data help form a baseline for assessing if other hippos use normal locomotion; relevant to clinical veterinary assessments of lameness; and for reconstructing the evolutionary biomechanics of hippo lineages.

The force a muscle generates is dependent on muscle structure, in which fibre length, pennation angle and tendon slack length all influence force production. Muscles are not preserved in the fossil record and these parameters must be estimated when constructing a musculoskeletal model. Here, we test the capability of digitally reconstructed muscles of the Australopithecus afarensis model (specimen AL 288-1) to maintain an upright, single-support limb posture. Our aim was to ascertain the influence that different architectural estimation methods have on muscle specialisation and on the subsequent inferences that can be extrapolated about limb function. Parameters were estimated for 36 muscles in the pelvis and lower limb and seven different musculoskeletal models of AL 288-1 were produced. These parameters represented either a ‘static’ Hill-type muscle model (n = 4 variants) which only incorporated force, or instead a ‘dynamic’ Hill-type muscle model with an elastic tendon and fibres that could vary force-length-velocity properties (n = 3 variants). Each muscle’s fibre length, pennation angle, tendon slack length and maximal isometric force were calculated based upon different input variables. Static (inverse) simulations were computed in which the vertical and mediolateral ground reaction forces (GRF) were incrementally increased until limb collapse (simulation failure). All AL 288-1 variants produced somewhat similar simulated muscle activation patterns, but the maximum vertical GRF that could be exerted on a single limb was not consistent between models. Three of the four static-muscle models were unable to support >1.8 times body weight and produced models that under-performed. The dynamic-muscle models were stronger. Comparative results with a human model imply that similar muscle group activations between species are needed to sustain single-limb support at maximally applied GRFs in terms of the simplified static simulations (e.g., same walking pose) used here. This approach demonstrated the range of outputs that can be generated for a model of an extinct individual. Despite mostly comparable outputs, the models diverged mostly in terms of strength.

Here, the authors track the evolution of mass distribution through bird evolution challenging suggested coupling between body shape and centre-of-mass position, and instead showing that crouched bipedalism evolved after powered flight.

During the Mesozoic, non-avian theropods represented one of the most successful clades globally distributed, with a wide diversity of forms. An example is the clade Megalosauroidea, which included medium- to large-bodied forms. Here, we analyse the macroevolution of the locomotor system in early Theropoda, emphasizing the Megalosauroidea. We scored the Spinosaurus neotype in a published taxon-character matrix and described the associated modifications in character states, mapping them onto a phylogeny and using these to study disparity. In the evolution of Megalosauroidea, there was the mosaic emergence of a low swollen ridge; enlargement of the posterior brevis fossa and emergence of a posterodorsal process on the ilium in some megalosauroids; emergence of a femoral head oriented anteromedially and medially angled, and appearance of posterolaterally oriented medial femoral condyles in spinosaurids. The greatest morphological disparity is in the ilium of megalosaurids; the ischium seems to have a high degree of homoplasy; there is a clear distinction in the femoral morphospace regarding megalosauroids and other theropods; piatnitzkysaurids show considerable disparity of zeugopodial characters. These reconstructions of osteological evolution form a stronger basis on which other studies could build, such as mapping of pelvic/appendicular musculature and/or correlating skeletal traits with changes in locomotor function.

Abstract Biomechanical models and simulations of musculoskeletal function rely on accurate muscle parameters, such as muscle masses and lines of action, to estimate force production potential and moment arms. These parameters are often obtained through destructive techniques (i.e., dissection) in living taxa, frequently hindering the measurement of other relevant parameters from a single individual, thus making it necessary to combine multiple specimens and/or sources. Estimating these parameters in extinct taxa is even more challenging as soft tissues are rarely preserved in fossil taxa and the skeletal remains contain relatively little information about the size or exact path of a muscle. Here we describe a new protocol that facilitates the estimation of missing muscle parameters (i.e., muscle volume and path) for extant and extinct taxa. We created three-dimensional volumetric reconstructions for the hindlimb muscles of the extant Nile crocodile and extinct stem-archosaur Euparkeria, and the shoulder muscles of an extant gorilla to demonstrate the broad applicability of this methodology across living and extinct animal clades. Additionally, our method can be combined with surface geometry data digitally captured during dissection, thus facilitating downstream analyses. We evaluated the estimated muscle masses against physical measurements to test their accuracy in estimating missing parameters. Our estimated muscle masses generally compare favourably with segmented iodine-stained muscles and almost all fall within or close to the range of observed muscle masses, thus indicating that our estimates are reliable and the resulting lines of action calculated sufficiently accurately. This method has potential for diverse applications in evolutionary morphology and biomechanics.

Birds and crocodylians are the only remaining members of Archosauria (ruling reptiles) and they exhibit major differences in posture and gait, which are polar opposites in terms of locomotor strategies. Their broader lineages (Avemetatarsalia and Pseudosuchia) evolved a multitude of locomotor modes in the Triassic and Jurassic periods, including several occurrences of bipedalism. The exact timings and frequencies of bipedal origins within archosaurs, and thus their ancestral capabilities, are contentious. It is often suggested that archosaurs ancestrally exhibited some form of bipedalism. Euparkeria capensis is a central taxon for the investigation of locomotion in archosaurs due to its phylogenetic position and intermediate skeletal morphology, and is argued to be representative of facultative bipedalism in this group. However, no studies to date have biomechanically tested if bipedality was feasible in Eupakeria. Here, we use musculoskeletal models and static simulations in its hindlimb to test the influences of body posture and muscle parameter estimation methods on locomotor potential. Our analyses show that the resulting negative pitching moments around the centre of mass were prohibitive to sustainable bipedality. We conclude that it is unlikely that Euparkeria was facultatively bipedal, and was probably quadrupedal, rendering the inference of ancestral bipedal abilities in Archosauria unlikely.

Fossil trackways provide a glimpse into the behavior of extinct animals. However, while providing information of the trackmaker size, stride, and even speed, the actual gait of the organism can be ambiguous. This is especially true of quadrupedal animals, where disparate gaits can have similar trackway patterns. Here, predictive simulation using trajectory optimization can help distinguish gaits used by trackmakers. First, we demonstrated that a planar, five-link quadrupedal biomechanical model can generate the qualitative trackway patterns made by domestic dogs, although a systematic error emerges in the track phase (relative distance between ipsilateral pes and manus prints). Next, we used trackway dimensions as inputs to a model of Batrachotomus kupferzellensis, a long-limbed, crocodile-line archosaur (clade Pseudosuchia) from the Middle Triassic of Germany. We found energetically optimal gaits and compared their predicted track phases to those of fossil trackways of Isochirotherium and Brachychirotherium. The optimal results agree with trackways at slow speeds but differ at faster speeds. However, all simulations point to a gait transition around a non-dimensional speed of 0.4 and another at 1.0. The trackways likewise exhibit stark differences in the track phase at these speeds. In all cases, including when simulations are constrained to the fossil track phase, the optimal simulations after the first gait transition do not correspond to a trot, as often used by living crocodiles. Instead, they are a diagonal sequence gait similar to the slow tölt of Icelandic horses. This is the first evidence that extinct pseudosuchians may have exhibited different gaits than their modern relatives and of a gait transition in an extinct pseudosuchian. The results of this analysis highlight areas where the models can be improved to generate more reliable predictions for fossil data while also showcasing how simple models can generate insights about the behavior of extinct animals.

Land mammals support and move their body using their musculoskeletal system. Their musculature usually presents varying adaptations with body mass or mode of locomotion. Rhinocerotidae is an interesting clade in this regard, as they are heavy animals potentially reaching three tons but are still capable of adopting a galloping gait. However, their musculature has been poorly studied. Here we report the dissection of both forelimb and hindlimb of one neonate and one adult each for two species of rhinoceroses, the Indian rhinoceros (Rhinoceros unicornis) and the white rhinoceros (Ceratotherium simum). We show that their muscular organisation is similar to that of their relatives, equids and tapirs, and that few evolutionary convergences with other heavy mammals (e.g. elephants and hippopotamuses) are present. Nevertheless, they show clear adaptations to their large body mass, such as more distal insertions for the protractor and adductor muscles of the limbs, giving them longer lever arms. The quantitative architecture of rhino muscles is again reminiscent of that of horses and tapirs, although contrary to horses, the forelimb is much stronger than the hindlimb, which is likely due to its great role in body mass support. Muscles involved mainly in counteracting gravity (e.g. serratus ventralis thoracis, infraspinatus, gastrocnemius, flexores digitorum) are usually highly pennate with short fascicles facilitating strong joint extension. Muscles involved in propulsion (e.g. gluteal muscles, gluteobiceps, quadriceps femoris) seem to represent a compromise between a high maximal isometric force and long fascicles, allowing a reasonably fast and wide working range. Neonates present higher normalized maximal isometric force than the adults for almost every muscle, except sometimes for the extensor and propulsor muscles, which presumably acquire their great force-generating capacity during the growth of the animal. Our study clarifies the way the muscles of animals of cursorial ancestry can adapt to support a greater body mass and calls for further investigations in other clades of large body mass.

The musculoskeletal system of marsupial mammals has numerous unusual features beyond the pouch and epipubic bones. One example is the widespread absence or reduction (to a fibrous “patelloid”) of the patella (“kneecap”) sesamoid bone, but prior studies with coarse sampling indicated complex patterns of evolution of this absence or reduction. Here, we conducted an in-depth investigation into the form of the patella of extant marsupial species and used the assembled dataset to reconstruct the likely pattern of evolution of the marsupial patella. Critical assessment of the available literature was followed by examination and imaging of museum specimens, as well as CT scanning and histological examination of dissected wet specimens. Our results, from sampling about 19% of extant marsupial species-level diversity, include new images and descriptions of the fibrocartilaginous patelloid in Thylacinus cynocephalus (the thylacine or “marsupial wolf”) and other marsupials as well as the ossified patella in Notoryctes ‘marsupial moles’, Caenolestes shrew opossums, bandicoots and bilbies. We found novel evidence of an ossified patella in one specimen of Macropus rufogriseus (Bennett’s wallaby), with hints of similar variation in other species. It remains uncertain whether such ossifications are ontogenetic variation, unusual individual variation, pathological or otherwise, but future studies must continue to be conscious of variation in metatherian patellar sesamoid morphology. Our evolutionary reconstructions using our assembled data vary, too, depending on the reconstruction algorithm used. A maximum likelihood algorithm favours ancestral fibrocartilaginous “patelloid” for crown clade Marsupialia and independent origins of ossified patellae in extinct sparassodonts, peramelids, notoryctids and caenolestids. A maximum parsimony algorithm favours ancestral ossified patella for the clade [Marsupialia + sparassodonts] and subsequent reductions into fibrocartilage in didelphids, dasyuromorphs and diprotodonts; but this result changed to agree more with the maximum likelihood results if the character state reconstructions were ordered. Thus, there is substantial homoplasy in marsupial patellae regardless of the evolutionary algorithm adopted. We contend that the most plausible inference, however, is that metatherians independently ossified their patellae at least three times in their evolution. Furthermore, the variability of the patellar state we observed, even within single species (e.g. M. rufogriseus), is fascinating and warrants further investigation, especially as it hints at developmental plasticity that might have been harnessed in marsupial evolution to drive the complex patterns inferred here.

The locomotion strategies of fossil invertebrates are typically interpreted on the basis of morphological descriptions. However, it has been shown that homologous structures with disparate morphologies in extant invertebrates do not necessarily correlate with differences in their locomotory capability. Here, we present a new methodology for analysing locomotion in fossil invertebrates with a rigid skeleton through an investigation of a cornute stylophoran, an extinct fossil echinoderm with enigmatic morphology that has made its mode of locomotion difficult to reconstruct. We determined the range of motion of a stylophoran arm based on digitized three-dimensional morphology of an early Ordovician form, Phyllocystis crassimarginata. Our analysis showed that efficient arm-forward epifaunal locomotion based on dorsoventral movements, as previously hypothesized for cornute stylophorans, was not possible for this taxon; locomotion driven primarily by lateral movement of the proximal aulacophore was more likely. Three-dimensional digital modelling provides an objective and rigorous methodology for illuminating the movement capabilities and locomotion strategies of fossil invertebrates.

Abstract Background Morphological diversity of limb bone lengths, diameters, and proportions in mammals is known to vary strongly with locomotor habit. It remains less well known how different locomotor habits are correlated with cross-sectional traits of the limb skeleton, such as cross-sectional area (CSA), second moments of area (SMA), and section modulus (MOD) and whether these traits have evolved adaptively. CSA and SMA represent the bone’s resistance to axial compression and bending, respectively, whereas MOD represents bone structural strength related to shape. Sampling 28 species of mustelids, a carnivoran lineage with diverse locomotor habits, we tested for differences in humeral, radial, and ulnar cross-sectional traits among specialists for climbing, digging, and swimming, in addition to generalists. Given that the limbs of digging specialists function in the dense substance of soil, and that swimming specialists need to counteract buoyancy, we predicted that these mustelids with these specializations should have the greatest values of cross-sectional traits. Results We analyzed cross-sectional traits (calculated via μCT scanning and rendered dimensionless) in 5% increments along a bone’s length and found significant differences among locomotor habits, though differences in ulnar cross-sectional traits were fewer than those for the humerus and radius. Swimming specialists had the greatest values of cross-sectional traits, followed by digging specialists. Climbing specialists had the lowest values of cross-sectional traits. However, phylogenetic affinity underlies these results. Fitting models of trait evolution to CSA and SMA revealed that a multi-rate Brownian motion model and a multi-optima Ornstein-Uhlenbeck model are the best-fitting models of evolution for these traits. However, inspection of α-values uncovered that many of the OU models did not differ from a Brownian motion model. Conclusions Within Mustelidae, differences in limb function and locomotor habit influence cross-sectional traits in ways that produce patterns that may diverge from adaptive patterns exhibited by external traits (e.g., bone lengths) of the mammalian limb skeleton. These results suggest that not all the traits of a single organ evolve under a single evolutionary process and that models of trait evolution should be fit to a range of traits for a better understanding of the evolution of the mammalian locomotor system.

Abstract Background The mouse is one of the most widely used animal models to study neuromuscular diseases and test new therapeutic strategies. However, findings from successful pre-clinical studies using mouse models frequently fail to translate to humans due to various factors. Differences in muscle function between the two species could be crucial but often have been overlooked. The purpose of this study was to evaluate and compare muscle excursions in walking between mice and humans. Methods Recently published musculoskeletal models of the mouse hindlimb and human lower limb were used to simulate muscle-tendon dynamics during mouse and human walking, a key daily activity. Muscle fiber length changes (fiber excursions) of 25 muscle homologs in the two species were calculated from these simulations and then compared. To understand potential causes of differences in fiber excursions in walking, joint excursions and muscle moment arms were also compared across one gait cycle. Results Most muscles (19 out of 25 muscles) of the mouse hindlimb had much smaller fiber excursions as compared to human lower limb muscles during walking. For these muscles, fiber excursions in mice were only 48 ± 19% of those in humans. The differences in fiber excursion between the two species were primarily due to the reduced joint excursions and smaller muscle moment arms in mice as compared to humans. Conclusions Since progressive neuromuscular diseases, such as Duchenne muscular dystrophy, are known to be accelerated by damage accumulated from active muscle lengthening, these results suggest that biomechanical differences in muscle function during walking between mice and humans may impede the translations of knowledge gained from mouse models to humans. This knowledge would add a fresh perspective on how pre-clinical studies on mice might be better designed to improve translation to human clinical trials.

Birds have a more crouched posture compared to their theropod dinosaur ancestors. Here, Jiang and colleagues describe a lower hindlimb of the Early Cretaceous birdConfuciusorniswith soft tissues apparently preserved even as molecules, indicating a somewhat more modern posture in ancient birds.

White rhinoceroses (Ceratotherium simum) are odd-toed ungulates that belong to the group Perissodactyla. Being second only to elephants in terms of large body mass amongst extant tetrapods, rhinoceroses make fascinating subjects for the study of how large land animals support and move themselves. Rhinoceroses often are kept in captivity for protection from ivory poachers and for educational/touristic purposes, yet a detrimental side effect of captivity can be foot disease (i.e., enthesopathies and osteoarthritis around the phalanges). Foot diseases in large mammals are multifactorial, but locomotor biomechanics (e.g., pressures routinely experienced by the feet) surely can be a contributing factor. However, due to a lack of in vivo experimental data on rhinoceros foot pressures, our knowledge of locomotor performance and its links to foot disease is limited. The overall aim of this study was to characterize peak pressures and center of pressure trajectories in white rhinoceroses during walking. We asked two major questions. First, are peak locomotor pressures the lowest around the fat pad and its lobes (as in the case of elephants)? Second, are peak locomotor pressures concentrated around the areas with the highest reported incidence of pathologies? Our results show a reduction of pressures around the fat pad and its lobes, which is potentially due to the material properties of the fat pad or a tendency to avoid or limit “heel” contact at impact. We also found an even and gradual concentration of foot pressures across all digits, which may be a by-product of the more horizontal foot roll-off during the stance phase. While our exploratory, descriptive sample precluded hypothesis testing, our study provides important new data on rhinoceros locomotion for future studies to build on, and thus impetus for improved implementation in the care of captive/managed rhinoceroses.

The study of animal locomotion can be logistically challenging, especially in the case of large or unhandleable animals in uncontrolled environments. Here we demonstrate the utility of a low cost unmanned aerial vehicle (UAV) in measuring two-dimensional running kinematics from free-roaming giraffes (Giraffa camelopardalis giraffa) in the Free State Province, South Africa. We collected 120 Hz video of running giraffes, and calibrated each video frame using metatarsal length as a constant object of scale. We tested a number of methods to measure metatarsal length. The method with the least variation used close range photography and a trigonometric equation to spatially calibrate the still image, and derive metatarsal length. In the absence of this option, a spatially calibrated surface model of the study terrain was used to estimate topographical dimensions in video footage of interest. Data for the terrain models were collected using the same equipment, during the same study period. We subsequently validated the accuracy of the UAV method by comparing similar speed measurements of a human subject running on a treadmill, with treadmill speed. At 8 m focal distance we observed an error of 8% between the two measures of speed. This error was greater at a shorter focal distance, and when the subject was not in the central field of view. We recommend that future users maximise the camera focal distance, and keep the subject in the central field of view. The studied giraffes used a grounded rotary gallop with a speed range of 3.4–6.9 ms−1 (never cantering, trotting or pacing), and lower duty factors when compared with other cursorial quadrupeds. As this pattern might result in adverse increases in peak vertical limb forces with speed, it was notable to find that contralateral limbs became more in-phase with speed. Considering the latter pattern and the modest maximal speed of giraffes, we speculate that tissue safety factors are maintained within tolerable bounds this way. Furthermore, the angular kinematics of the neck were frequently isolated from the pitching of the body during running; this may be a result of the large mass of the head and neck. Further field experiments and biomechanical models are needed to robustly test these speculations.

Standing up from a prone position is a critical daily activity for animals: failing to do so effectively may cause an injurious fall or increase predation susceptibility. This sit-to-stand behaviour (StS) is biomechanically interesting because it necessitates transitioning through near-maximal joint motion ranges from a crouched (i.e., poor mechanical advantage) to a more upright posture. Such large joint excursions should require large length changes of muscle-tendon units. Here we integrate experimental and musculoskeletal simulation methods to quantify the joint motions, limb forces, and muscle fibre forces, activations and length changes during StS in an extreme athlete—the greyhound—which has large hindlimb muscles bearing short-fibred distal muscles and long tendons. Study results indicate that hindlimb anti-gravity muscle fibres operate near their ~50% limits of length change during StS; mostly by starting at highly lengthened positions. StS also requires high muscle activations (>50%), in part due to non-sagittal motions. Finally, StS movements require passive non-muscular support in the distal hindlimb where short-fibred muscles are incapable of sustaining StS themselves. Non-locomotor behaviours like StS likely impose important trade-offs between muscle fibre force capacity and length changes, as well as active and passive mechanisms of support, that have been neglected in locomotor biomechanics studies.

Flapping flight is the most power-demanding mode of locomotion, associated with a suite of anatomical specializations in extant adult birds. In contrast, many developing birds use their forelimbs to negotiate environments long before acquiring “flight adaptations,” recruiting their developing wings to continuously enhance leg performance and, in some cases, fly. How does anatomical development influence these locomotor behaviors? Isolating morphological contributions to wing performance is extremely challenging using purely empirical approaches. However, musculoskeletal modeling and simulation techniques can incorporate empirical data to explicitly examine the functional consequences of changing morphology by manipulating anatomical parameters individually and estimating their effects on locomotion. To assess how ontogenetic changes in anatomy affect locomotor capacity, we combined existing empirical data on muscle morphology, skeletal kinematics, and aerodynamic force production with advanced biomechanical modeling and simulation techniques to analyze the ontogeny of pectoral limb function in a precocial ground bird (Alectoris chukar). Simulations of wing-assisted incline running (WAIR) using these newly developed musculoskeletal models collectively suggest that immature birds have excess muscle capacity and are limited more by feather morphology, possibly because feathers grow more quickly and have a different style of growth than bones and muscles. These results provide critical information about the ontogeny and evolution of avian locomotion by (i) establishing how muscular and aerodynamic forces interface with the skeletal system to generate movement in morphing juvenile birds, and (ii) providing a benchmark to inform biomechanical modeling and simulation of other locomotor behaviors, both across extant species and among extinct theropod dinosaurs.

This paper is the last of a three-part series that investigates the architecture of cancellous bone in the main hindlimb bones of theropod dinosaurs, and uses cancellous bone architectural patterns to infer locomotor biomechanics in extinct non-avian species. Cancellous bone is highly sensitive to its prevailing mechanical environment, and may therefore help further understanding of locomotor biomechanics in extinct tetrapod vertebrates such as dinosaurs. Here in Part III, the biomechanical modelling approach derived previously was applied to two species of extinct, non-avian theropods, Daspletosaurus torosus and Troodon formosus. Observed cancellous bone architectural patterns were linked with quasi-static, three-dimensional musculoskeletal and finite element models of the hindlimb of both species, and used to derive characteristic postures that best aligned continuum-level principal stresses with cancellous bone fabric. The posture identified for Daspletosaurus was largely upright, with a subvertical femoral orientation, whilst that identified for Troodon was more crouched, but not to the degree observed in extant birds. In addition to providing new insight on posture and limb articulation, this study also tested previous hypotheses of limb bone loading mechanics and muscular control strategies in non-avian theropods, and how these aspects evolved on the line to birds. The results support the hypothesis that an upright femoral posture is correlated with bending-dominant bone loading and abduction-based muscular support of the hip, whereas a crouched femoral posture is correlated with torsion-dominant bone loading and long-axis rotation-based muscular support. Moreover, the results of this study also support the inference that hindlimb posture, bone loading mechanics and muscular support strategies evolved in a gradual fashion along the line to extant birds.

This paper is the second of a three-part series that investigates the architecture of cancellous bone in the main hindlimb bones of theropod dinosaurs, and uses cancellous bone architectural patterns to infer locomotor biomechanics in extinct non-avian species. Cancellous bone is widely known to be highly sensitive to its mechanical environment, and therefore has the potential to provide insight into locomotor biomechanics in extinct tetrapod vertebrates such as dinosaurs. Here in Part II, a new biomechanical modelling approach is outlined, one which mechanistically links cancellous bone architectural patterns with three-dimensional musculoskeletal and finite element modelling of the hindlimb. In particular, the architecture of cancellous bone is used to derive a single ‘characteristic posture’ for a given species—one in which bone continuum-level principal stresses best align with cancellous bone fabric—and thereby clarify hindlimb locomotor biomechanics. The quasi-static approach was validated for an extant theropod, the chicken, and is shown to provide a good estimate of limb posture at around mid-stance. It also provides reasonable predictions of bone loading mechanics, especially for the proximal hindlimb, and also provides a broadly accurate assessment of muscle recruitment insofar as limb stabilization is concerned. In addition to being useful for better understanding locomotor biomechanics in extant species, the approach hence provides a new avenue by which to analyse, test and refine palaeobiomechanical hypotheses, not just for extinct theropods, but potentially many other extinct tetrapod groups as well.

This paper is the first of a three-part series that investigates the architecture of cancellous (‘spongy’) bone in the main hindlimb bones of theropod dinosaurs, and uses cancellous bone architectural patterns to infer locomotor biomechanics in extinct non-avian species. Cancellous bone is widely known to be highly sensitive to its mechanical environment, and has previously been used to infer locomotor biomechanics in extinct tetrapod vertebrates, especially primates. Despite great promise, cancellous bone architecture has remained little utilized for investigating locomotion in many other extinct vertebrate groups, such as dinosaurs. Documentation and quantification of architectural patterns across a whole bone, and across multiple bones, can provide much information on cancellous bone architectural patterns and variation across species. Additionally, this also lends itself to analysis of the musculoskeletal biomechanical factors involved in a direct, mechanistic fashion. On this premise, computed tomographic and image analysis techniques were used to describe and analyse the three-dimensional architecture of cancellous bone in the main hindlimb bones of theropod dinosaurs for the first time. A comprehensive survey across many extant and extinct species is produced, identifying several patterns of similarity and contrast between groups. For instance, more stemward non-avian theropods (e.g. ceratosaurs and tyrannosaurids) exhibit cancellous bone architectures more comparable to that present in humans, whereas species more closely related to birds (e.g. paravians) exhibit architectural patterns bearing greater similarity to those of extant birds. Many of the observed patterns may be linked to particular aspects of locomotor biomechanics, such as the degree of hip or knee flexion during stance and gait. A further important observation is the abundance of markedly oblique trabeculae in the diaphyses of the femur and tibia of birds, which in large species produces spiralling patterns along the endosteal surface. Not only do these observations provide new insight into theropod anatomy and behaviour, they also provide the foundation for mechanistic testing of locomotor hypotheses via musculoskeletal biomechanical modelling.

Mice are often used as animal models of various human neuromuscular diseases, and analysis of these models often requires detailed gait analysis. However, little is known of the dynamics of the mouse musculoskeletal system during locomotion. In this study, we used computer optimization procedures to create a simulation of trotting in a mouse, using a previously developed mouse hindlimb musculoskeletal model in conjunction with new experimental data, allowing muscle forces, activation patterns, and levels of mechanical work to be estimated. Analyzing musculotendon unit (MTU) mechanical work throughout the stride allowed a deeper understanding of their respective functions, with the rectus femoris MTU dominating the generation of positive and negative mechanical work during the swing and stance phases. This analysis also tested previous functional inferences of the mouse hindlimb made from anatomical data alone, such as the existence of a proximo-distal gradient of muscle function, thought to reflect adaptations for energy-efficient locomotion. The results do not strongly support the presence of this gradient within the mouse musculoskeletal system, particularly given relatively high negative net work output from the ankle plantarflexor MTUs, although more detailed simulations could test this further. This modeling analysis lays a foundation for future studies of the control of vertebrate movement through the development of neuromechanical simulations.

An understanding of bone apparent and material densities and how they vary within bone at the organ level is of great interest in the understanding of degenerative bone conditions and for biomedical engineering applications. The densities of bone tissue have been shown to appreciably influence the mechanical competency of bone tissue. In order to assess the density of bone in the body, it is important to ensure that the parameters being measured in vivo are truly representative of the real values that have been measured in vitro. To assess the densities of bone across the entire spectrum of available porosities, 112 samples from an elephant femur were assessed using the Archimedes method (water displacement) and by micro-computed tomography (μ-CT). Comparisons were drawn between the two methods to determine if the densities calculated by μ-CT were representative of physically measured densities. The results showed that the apparent densities measured over the entire spectrum were very similar but varied in the intermediate regions of bone tissue, probably due to an increased presence of osteoid, increased remodeling, or experimental error as these type of bone is known for the presence of regions of closed cell geometry in the cancellous architecture. It could be argued that the measurements taken by μ-CT are more reliable of bone density values for the mineralized regions of bone as the threshold is defined with respect to the absorption of X-rays by the mineral. In contrast, the Archimedes method thresholds everything with a density value above that of the surrounding medium, 1 (g cm−3) for water, and hence it is more sensitive to the presence of osteoid, soft collagenous matrix, and epithelial cell layers. Further research is required to optimize the parameters of scanning methods for the structural properties of different bone tissue porosities, which hopefully in turn will be able to provide a basis for the development of predictive remodeling models.

Bone adaptation is modulated by the timing, direction, rate and magnitude of mechanical loads. To investigate whether frequent slow, or infrequent fast, gaits could dominate bone adaptation to load, we compared scaling of the limb bones from two mammalian herbivore clades that use radically different high-speed gaits, bipedal hopping (suborder Macropodiformes; kangaroos and kin) and quadrupedal galloping (order Artiodactyla; goats, deer and kin). Forelimb and hindlimb bones were collected from 20 artiodactyl and 15 macropod species (body mass M 1.05–1536 kg) and scanned in computed tomography or X-ray microtomography. Second moment of area (Imax) and bone length (l) were measured. Scaling relations (y = axb) were calculated for l versus M for each bone and for Imax versus M and Imax versus l for every 5% of length. Imax versus M scaling relationships were broadly similar between clades despite the macropod forelimb being nearly unloaded, and the hindlimb highly loaded, during bipedal hopping. Imax versus l and l versus M scaling were related to locomotor and behavioural specializations. Low-intensity loads may be sufficient to maintain bone mass across a wide range of species. Occasional high-intensity gaits might not break through the load sensitivity saturation engendered by frequent low-intensity gaits.

Many of the major locomotor transitions during the evolution of Archosauria, the lineage including crocodiles and birds as well as extinct Dinosauria, were shifts from quadrupedalism to bipedalism (and vice versa). Those occurred within a continuum between more sprawling and erect modes of locomotion and involved drastic changes of limb anatomy and function in several lineages, including sauropodomorph dinosaurs. We present biomechanical computer models of two locomotor extremes within Archosauria in an analysis of joint ranges of motion and the moment arms of the major forelimb muscles in order to quantify biomechanical differences between more sprawling, pseudosuchian (represented the crocodile Crocodylus johnstoni) and more erect, dinosaurian (represented by the sauropodomorph Mussaurus patagonicus) modes of forelimb function. We compare these two locomotor extremes in terms of the reconstructed musculoskeletal anatomy, ranges of motion of the forelimb joints and the moment arm patterns of muscles across those ranges of joint motion. We reconstructed the three-dimensional paths of 30 muscles acting around the shoulder, elbow and wrist joints. We explicitly evaluate how forelimb joint mobility and muscle actions may have changed with postural and anatomical alterations from basal archosaurs to early sauropodomorphs. We thus evaluate in which ways forelimb posture was correlated with muscle leverage, and how such differences fit into a broader evolutionary context (i.e. transition from sprawling quadrupedalism to erect bipedalism and then shifting to graviportal quadrupedalism). Our analysis reveals major differences of muscle actions between the more sprawling and erect models at the shoulder joint. These differences are related not only to the articular surfaces but also to the orientation of the scapula, in which extension/flexion movements in Crocodylus (e.g. protraction of the humerus) correspond to elevation/depression in Mussaurus. Muscle action is highly influenced by limb posture, more so than morphology. Habitual quadrupedalism in Mussaurus is not supported by our analysis of joint range of motion, which indicates that glenohumeral protraction was severely restricted. Additionally, some active pronation of the manus may have been possible in Mussaurus, allowing semi-pronation by a rearranging of the whole antebrachium (not the radius against the ulna, as previously thought) via long-axis rotation at the elbow joint. However, the muscles acting around this joint to actively pronate it may have been too weak to drive or maintain such orientations as opposed to a neutral position in between pronation and supination. Regardless, the origin of quadrupedalism in Sauropoda is not only linked to manus pronation but also to multiple shifts of forelimb morphology, allowing greater flexion movements of the glenohumeral joint and a more columnar forelimb posture.

The patella is a sesamoid bone located in the major extensor tendon of the knee joint, in the hindlimb of many tetrapods. Although numerous aspects of knee morphology are ancient and conserved among most tetrapods, the evolutionary occurrence of an ossified patella is highly variable. Among extant (crown clade) groups it is found in most birds, most lizards, the monotreme mammals and almost all placental mammals, but it is absent in most marsupial mammals as well as many reptiles. Here, we integrate data from the literature and first-hand studies of fossil and recent skeletal remains to reconstruct the evolution of the mammalian patella. We infer that bony patellae most likely evolved between four and six times in crown group Mammalia: in monotremes, in the extinct multituberculates, in one or more stem-mammal genera outside of therian or eutherian mammals and up to three times in therian mammals. Furthermore, an ossified patella was lost several times in mammals, not including those with absent hindlimbs: once or more in marsupials (with some re-acquisition) and at least once in bats. Our inferences about patellar evolution in mammals are reciprocally informed by the existence of several human genetic conditions in which the patella is either absent or severely reduced. Clearly, development of the patella is under close genomic control, although its responsiveness to its mechanical environment is also important (and perhaps variable among taxa). Where a bony patella is present it plays an important role in hindlimb function, especially in resisting gravity by providing an enhanced lever system for the knee joint. Yet the evolutionary origins, persistence and modifications of a patella in diverse groups with widely varying habits and habitats—from digging to running to aquatic, small or large body sizes, bipeds or quadrupeds—remain complex and perplexing, impeding a conclusive synthesis of form, function, development and genetics across mammalian evolution. This meta-analysis takes an initial step toward such a synthesis by collating available data and elucidating areas of promising future inquiry.

The appearance and shape of sesamoid bones within a tendon or ligament wrapping around a joint are understood to be influenced by both genetic and epigenetic factors. Ostriches (Struthio camelus) possess two sesamoid patellae (kneecaps), one of which (the distal patella) is unique to their lineage, making them a good model for investigating sesamoid tissue development and evolution. Here we used finite-element modelling to test the hypothesis that specific mechanical cues in the ostrich patellar tendon favour the formation of multiple patellae. Using three-dimensional models that allow application of loading conditions in which all muscles, or only distal or only proximal muscles to be activated, we found that there were multiple regions within the tendon where transformation from soft tissue to fibrocartilage was favourable and therefore a potential for multiple patellae based solely upon mechanical stimuli. While more studies are needed to better understand universal mechanobiological principles as well as full developmental processes, our findings suggest that a tissue differentiation algorithm using shear strain and compressive strain as inputs may be a roughly effective predictor of the tissue differentiation required for sesamoid development.

Foot problems are a major cause of morbidity and mortality in elephants, but are underreported due to difficulties in diagnosis, particularly of conditions affecting the bones and internal structures. Here we evaluate post-mortem computer tomographic (CT) scans of 52 feet from 21 elephants (seven African Loxodonta africana and 14 Asian Elephas maximus), describing both pathology and variant anatomy (including the appearance of phalangeal and sesamoid bones) that could be mistaken for disease. We found all the elephants in our study to have pathology of some type in at least one foot. The most common pathological changes observed were bone remodelling, enthesopathy, osseous cyst-like lesions, and osteoarthritis, with soft tissue mineralisation, osteitis, infectious osteoarthriti, subluxation, fracture and enostoses observed less frequently. Most feet had multiple categories of pathological change (81% with two or more diagnoses, versus 10% with a single diagnosis, and 9% without significant pathology). Much of the pathological change was focused over the middle/lateral digits, which bear most weight and experience high peak pressures during walking. We found remodelling and osteoarthritis to be correlated with increasing age, more enthesopathy in Asian elephants, and more cyst-like lesions in females. We also observed multipartite, missing and misshapen phalanges as common and apparently incidental findings. The proximal (paired) sesamoids can appear fused or absent, and the predigits (radial/tibial sesamoids) can be variably ossified, though are significantly more ossified in Asian elephants. Our study reinforces the need for regular examination and radiography of elephant feet to monitor for pathology and as a tool for improving welfare.

Horse racing is a multi-billion-dollar industry that has raised welfare concerns due to injured and euthanized animals. Whilst the cause of musculoskeletal injuries that lead to horse morbidity and mortality is multifactorial, pre-existing pathologies, increased speeds and substrate of the racecourse are likely contributors to foot disease. Horse hooves have the ability to naturally deform during locomotion and dissipate locomotor stresses, yet farriery approaches are utilised to increase performance and protect hooves from wear. Previous studies have assessed the effect of different shoe designs on locomotor performance; however, no biomechanical study has hitherto measured the effect of horseshoes on the stresses of the foot skeleton in vivo. This preliminary study introduces a novel methodology combining three-dimensional data from biplanar radiography with inverse dynamics methods and finite element analysis (FEA) to evaluate the effect of a stainless steel shoe on the function of a Thoroughbred horse’s forefoot during walking. Our preliminary results suggest that the stainless steel shoe shifts craniocaudal, mediolateral and vertical GRFs at mid-stance. We document a similar pattern of flexion-extension in the PIP (pastern) and DIP (coffin) joints between the unshod and shod conditions, with slight variation in rotation angles throughout the stance phase. For both conditions, the PIP and DIP joints begin in a flexed posture and extend over the entire stance phase. At mid-stance, small differences in joint angle are observed in the PIP joint, with the shod condition being more extended than the unshod horse, whereas the DIP joint is extended more in the unshod than the shod condition. We also document that the DIP joint extends more than the PIP after mid-stance and until the end of the stance in both conditions. Our FEA analysis, conducted solely on the bones, shows increased von Mises and Maximum principal stresses on the forefoot phalanges in the shod condition at mid-stance, consistent with the tentative conclusion that a steel shoe might increase mechanical loading. However, because of our limited sample size none of these apparent differences have been tested for statistical significance. Our preliminary study illustrates how the shoe may influence the dynamics and mechanics of a Thoroughbred horse’s forefoot during slow walking, but more research is needed to quantify the effect of the shoe on the equine forefoot during the whole stance phase, at faster speeds/gaits and with more individuals as well as with a similar focus on the hind feet. We anticipate that our preliminary analysis using advanced methodological approaches will pave the way for new directions in research on the form/function relationship of the equine foot, with the ultimate goal to minimise foot injuries and improve animal health and welfare.

Elephants, the largest living land mammals, have evolved a specialized foot morphology to help reduce locomotor pressures while supporting their large body mass. Peak pressures that could cause tissue damage are mitigated passively by the anatomy of elephants' feet, yet this mechanism does not seem to work well for some captive animals. This study tests how foot pressures vary among African and Asian elephants from habitats where natural substrates predominate but where foot care protocols differ. Variations in pressure patterns might be related to differences in husbandry, including but not limited to trimming and the substrates that elephants typically stand and move on. Both species' samples exhibited the highest concentration of peak pressures on the lateral digits of their feet (which tend to develop more disease in elephants) and lower pressures around the heel. The trajectories of the foot's centre of pressure were also similar, confirming that when walking at similar speeds, both species load their feet laterally at impact and then shift their weight medially throughout the step until toe-off. Overall, we found evidence of variations in foot pressure patterns that might be attributable to husbandry and other causes, deserving further examination using broader, more comparable samples.

The colossal size and body plan of sauropod dinosaurs are unparalleled in terrestrial vertebrates. However, to date, there have been only limited attempts to examine temporal and phylogenetic patterns in the sauropod bauplan. Here, we combine three-dimensional computational models with phylogenetic reconstructions to quantify the evolution of whole-body shape and body segment properties across the sauropod radiation. Limitations associated with the absence of soft tissue preservation in fossils result in large error bars about mean absolute body shape predictions. However, applying any consistent skeleton : body volume ratio to all taxa does yield changes in body shape that appear concurrent with major macroevolutionary events in sauropod history. A caudad shift in centre-of-mass (CoM) in Middle Triassic Saurischia, associated with the evolution of bipedalism in various dinosaur lineages, was reversed in Late Triassic sauropodomorphs. A craniad CoM shift coincided with the evolution of quadrupedalism in the Late Triassic, followed by a more striking craniad shift in Late Jurassic–Cretaceous titanosauriforms, which included the largest sauropods. These craniad CoM shifts are strongly correlated with neck enlargement, a key innovation in sauropod evolution and pivotal to their gigantism. By creating a much larger feeding envelope, neck elongation is thought to have increased feeding efficiency and opened up trophic niches that were inaccessible to other herbivores. However, we find that relative neck size and CoM position are not strongly correlated with inferred feeding habits. Instead the craniad CoM positions of titanosauriforms appear closely linked with locomotion and environmental distributions, potentially contributing to the continued success of this group until the end-Cretaceous, with all other sauropods having gone extinct by the early Late Cretaceous.

We developed a three-dimensional, biomechanical computer model of the 36 major pelvic limb muscle groups in an ostrich (Struthio camelus) to investigate muscle function in this, the largest of extant birds and model organism for many studies of locomotor mechanics, body size, anatomy and evolution. Combined with experimental data, we use this model to test two main hypotheses. We first query whether ostriches use limb orientations (joint angles) that optimize the moment-generating capacities of their muscles during walking or running. Next, we test whether ostriches use limb orientations at mid-stance that keep their extensor muscles near maximal, and flexor muscles near minimal, moment arms. Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support. We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles. We infer that dynamic properties of muscles or tendons might be better candidates for locomotor optimization. Regardless, general principles explaining why species choose particular joint orientations during locomotion are lacking, raising the question of whether such general principles exist or if clades evolve different patterns (e.g., weighting of muscle force–length or force–velocity properties in selecting postures). This leaves theoretical studies of muscle moment arms estimated for extinct animals at an impasse until studies of extant taxa answer these questions. Finally, we compare our model’s results against those of two prior studies of ostrich limb muscle moment arms, finding general agreement for many muscles. Some flexor and extensor muscles exhibit self-stabilization patterns (posture-dependent switches between flexor/extensor action) that ostriches may use to coordinate their locomotion. However, some conspicuous areas of disagreement in our results illustrate some cautionary principles. Importantly, tendon-travel empirical measurements of muscle moment arms must be carefully designed to preserve 3D muscle geometry lest their accuracy suffer relative to that of anatomically realistic models. The dearth of accurate experimental measurements of 3D moment arms of muscles in birds leaves uncertainty regarding the relative accuracy of different modelling or experimental datasets such as in ostriches. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in ostriches for the first time, emphasizing that avian limb mechanics are highly three-dimensional and complex, and how no muscles act purely in the sagittal plane. A comparative synthesis of experiments and models such as ours could provide powerful synthesis into how anatomy, mechanics and control interact during locomotion and how these interactions evolve. Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.

The lineage leading to modern Crocodylia has undergone dramatic evolutionary changes in morphology, ecology and locomotion over the past 200+ Myr. These functional innovations may be explained in part by morphological changes in the axial skeleton, which is an integral part of the vertebrate locomotor system. Our objective was to estimate changes in osteological range of motion (RoM) and intervertebral joint stiffness of thoracic and lumbar vertebrae with increasing aquatic adaptation in crocodylomorphs. Using three-dimensional virtual models and morphometrics, we compared the modern crocodile Crocodylus to five extinct crocodylomorphs: Terrestrisuchus, Protosuchus, Pelagosaurus, Steneosaurus and Metriorhynchus, which span the spectrum from terrestrial to fully aquatic. In Crocodylus, we also experimentally measured changes in trunk flexibility with sequential removal of osteoderms and soft tissues. Our results for the more aquatic species matched our predictions fairly well, but those for the more terrestrial early crocodylomorphs did not. A likely explanation for this lack of correspondence is the influence of other axial structures, particularly the rigid series of dorsal osteoderms in early crocodylomorphs. The most important structures for determining RoM and stiffness of the trunk in Crocodylus were different in dorsoventral versus mediolateral bending, suggesting that changes in osteoderm and rib morphology over crocodylomorph evolution would have affected movements in some directions more than others.

The patella (kneecap) exhibits multiple evolutionary origins in birds, mammals, and lizards, and is thought to increase the mechanical advantage of the knee extensor muscles. Despite appreciable interest in the specialized anatomy and locomotion of palaeognathous birds (ratites and relatives), the structure, ontogeny and evolution of the patella in these species remains poorly characterized. Within Palaeognathae, the patella has been reported to be either present, absent, or fused with other bones, but it is unclear how much of this variation is real, erroneous or ontogenetic. Clarification of the patella’s form in palaeognaths would provide insight into the early evolution of the patella in birds, in addition to the specialized locomotion of these species. Findings would also provide new character data of use in resolving the controversial evolutionary relationships of palaeognaths. In this study, we examined the gross and histological anatomy of the emu patellar tendon across several age groups from five weeks to 18 months. We combined these results with our observations and those of others regarding the patella in palaeognaths and their outgroups (both extant and extinct), to reconstruct the evolution of the patella in birds. We found no evidence of an ossified patella in emus, but noted its tendon to have a highly unusual morphology comprising large volumes of adipose tissue contained within a collagenous meshwork. The emu patellar tendon also included increasing amounts of a cartilage-like tissue throughout ontogeny. We speculate that the unusual morphology of the patellar tendon in emus results from assimilation of a peri-articular fat pad, and metaplastic formation of cartilage, both potentially as adaptations to increasing tendon load. We corroborate previous observations of a ‘double patella’ in ostriches, but in contrast to some assertions, we find independent (i.e., unfused) ossified patellae in kiwis and tinamous. Our reconstructions suggest a single evolutionary origin of the patella in birds and that the ancestral patella is likely to have been a composite structure comprising a small ossified portion, lost by some species (e.g., emus, moa) but expanded in others (e.g., ostriches).

Emus (Dromaius novaehollandiae) are exclusively terrestrial, bipedal and cursorial ratites with some similar biomechanical characteristics to humans. Their growth rates are impressive, as their body mass increases eighty-fold from hatching to adulthood whilst maintaining the same mode of locomotion throughout life. These ontogenetic characteristics stimulate biomechanical questions about the strategies that allow emus to cope with their rapid growth and locomotion, which can be partly addressed via scaling (allometric) analysis of morphology. In this study we have collected pelvic limb anatomical data (muscle architecture, tendon length, tendon mass and bone lengths) and calculated muscle physiological cross sectional area (PCSA) and average tendon cross sectional area from emus across three ontogenetic stages (n = 17, body masses from 3.6 to 42 kg). The data were analysed by reduced major axis regression to determine how these biomechanically relevant aspects of morphology scaled with body mass. Muscle mass and PCSA showed a marked trend towards positive allometry (26 and 27 out of 34 muscles respectively) and fascicle length showed a more mixed scaling pattern. The long tendons of the main digital flexors scaled with positive allometry for all characteristics whilst other tendons demonstrated a less clear scaling pattern. Finally, the two longer bones of the limb (tibiotarsus and tarsometatarsus) also exhibited positive allometry for length, and two others (femur and first phalanx of digit III) had trends towards isometry. These results indicate that emus experience a relative increase in their muscle force-generating capacities, as well as potentially increasing the force-sustaining capacities of their tendons, as they grow. Furthermore, we have clarified anatomical descriptions and provided illustrations of the pelvic limb muscle–tendon units in emus.

The three-dimensional anatomy of the ostrich (Struthio camelus) knee (femorotibial, femorofibular, and femoropatellar) joint has scarcely been studied, and could elucidate certain mechanobiological properties of sesamoid bones. The adult ostrich is unique in that it has double patellae, while another similar ratite bird, the emu, has none. Understanding why these patellae form and what purpose they may serve is dually important for future studies on ratites as well as for understanding the mechanobiological characteristics of sesamoid bone development. For this purpose, we present a three-dimensional anatomical study of the ostrich knee joint, detailing osteology, ligaments and menisci, and myology. We have identified seven muscles which connect to the two patellae and compare our findings to past descriptions. These descriptions can be used to further study the biomechanical loading and implications of the double patella in the ostrich.

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.

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.

The lungs of birds have long been known to move air in only one direction during both inspiration and expiration through most of the tubular gas-exchanging bronchi (parabronchi). Recently a similar pattern of airflow has been observed in American alligators, a sister taxon to birds. The pattern of flow appears to be due to the arrangement of the primary and secondary bronchi, which, via their branching angles, generate inspiratory and expiratory aerodynamic valves. Both the anatomical similarity of the avian and alligator lung and the similarity in the patterns of airflow raise the possibility that these features are plesiomorphic for Archosauria and therefore did not evolve in response to selection for flapping flight or an endothermic metabolism, as has been generally assumed. To further test the hypothesis that unidirectional airflow is ancestral for Archosauria, we measured airflow in the lungs of the Nile crocodile (Crocodylus niloticus). As in birds and alligators, air flows cranially to caudally in the cervical ventral bronchus, and caudally to cranially in the dorsobronchi in the lungs of Nile crocodiles. We also visualized the gross anatomy of the primary, secondary and tertiary pulmonary bronchi of C. niloticus using computed tomography (CT) and microCT. The cervical ventral bronchus, cranial dorsobronchi and cranial medial bronchi display similar characteristics to their proposed homologues in the alligator, while there is considerable variation in the tertiary and caudal group bronchi. Our data indicate that the aspects of the crocodilian bronchial tree that maintain the aerodynamic valves and thus generate unidirectional airflow, are ancestral for Archosauria.