How to walk carrying a huge egg? Trade‐offs between locomotion and reproduction explain the special pelvis and leg anatomy in kiwi (Aves; Apteryx spp.)

International audienceKiwi (Aves; genus Apteryx) are famous for laying an enormous egg in comparison with their relatively small body size. Considering the peculiar gait of this flightless bird, we suspected the existence of morpho-functional trade-offs between reproduction and locomotion. To understand how structural constraints, imposed by a large egg size, might influence the terrestrial locomotion of Apteryx, we analysed the anatomy of the limb osteomuscular system in two species of kiwi (Apteryx mantelli and Apteryx owenii). We performed detailed dissections and brought to light specific anatomical features of kiwi, in comparison with other ratites and neognathous birds. Our osteological study revealed a strongly curved pelvis, a rigid tail, and enlarged ribs. Our myology study showed an unusual location of the caudofemoralis muscle origin and insertion. The insertion of the pars pelvica along the entire caudal face of the femur, contrasts with the proximal insertion usually seen in other birds. Additionally, the pars caudalis originates along the entire tail, whereas it only inserts on the uropygium in the other birds. To interpret these specificities from a functional point of view, we built three-dimensional osteomuscular models based on computed tomography scans, radiographies and our dissections. We chose three postures associated with reproductive constraints: the standing position of a gravid compared with a non-gravid bird, as well as the brooding position. The 3D model of the brooding position suggested that the enlarged ribs could support the bodyweight when leaning on the huge egg in both males and females. Moreover, we found that in gravid females, the unusual shape of the pelvis and tail allowed the huge egg to sit ventrally below the pelvis, whereas it is held closer to the rachis in other birds. The specific conformation of the limb and the insertions of the two parses of the caudofemoralis help to maintain the tail flexed, and to keep the legs adducted when carrying the egg. The caudal location of the hip and its flexed position explains the long stance phase during the strange gait of kiwi, revealing the functional trade-off between reproduction and locomotion in this emblematic New Zealand bird

Functional implications of the intertarsal joint shape in a terrestrial ( Coturnix coturnix ) versus a semi-aquatic bird ( Callonetta leucophrys )

International audienceAs birds have a diversity of locomotor behaviors, their skeleton is subjected to a variety of mechanical constraints (gravitational, aerodynamic and sometimes hydrodynamic forces). Yet, only minor modifications in post-cranial skeleton shape are observed across the diversity of avian species in comparison with other vertebrates. The goal of this study was to explore potential morphological adjustments that allow locomotion in different habitats in Anatidae. Specifically, we compared a strictly terrestrial bird, the common quail Coturnix coturnix, and a semi-aquatic bird, the ringed teal Callonetta leucophrys, to explore whether their anatomy reflects the constraints of locomotion in different habitats (water vs. land). We compared the tibiotarsus and the tarsometatarsus shape between the two species using a geometric morphometric approach. Our data illustrate distinct differences between species with a more medially oriented intertarsal joint in the ringed teal than in the common quail, which may be linked to the kinematics of walking and paddling. This study lays the foundations to understand the functional requirements for moving in both terrestrial and aquatic environments in Anatidae, and suggests morphological characteristics of the bird hindlimb skeleton that may help to predict the motions it is capable of

Extensive chondroid bone in juvenile duck limbs hints at accelerated growth mechanism in avian skeletogenesis

Modern altricial birds are the fastest growing vertebrates, whereas various degrees of precocity (functional maturity) result in slower growth. Diaphyseal osteohistology, the best proxy for inferring relative growth rates in fossils, suggests that in the earliest birds, posthatching growth rates were more variable than in modern representatives, with some showing considerably slow growth that was attributed to their assumed precocial flight abilities. For finding clues how precocial or altricial skeletogenesis and related growth acceleration could be traced in avian evolution, as a case study we investigated the growing limb diaphyseal histology in an ontogenetic series of ducks which, among several other avian taxa, show a combination of altricial wing and precocial leg development. Here we report the unexpected discovery that chondroid bone, a skeletal tissue family intermediate between cartilage and bone, extensively contributes to the development of limb bone shaft in ducks up to at least 30 days posthatching age. To our knowledge, chondroid bone has never been reported in such quantities and with an ontogenetically extended deposition period in post-embryonic, non-pathological periosteal bone formation of any tetrapod limb. It shows transitional cellular/lacunar morphologies and matrix staining properties between cartilage and woven bone and takes a significant part in the diametric growth of the limb bone shaft. Its amount and distribution through duckling ontogeny seems to be associated with the disparate functional and growth trajectories of the altricial wings vs. precocial legs characteristic of duck limb development. The presence of isogenous cell groups in the periosteal chondroid bone implies that cartilage-like interstitial growth took place before matrix mineralization complementing appositional bone growth. Based on these characteristics and on its fast formation rate in all previously reported normal as well as pathological cases, we suggest that chondroid bone in ducks significantly accelerates diametric limb bone growth. Related to this growth acceleration, we hypothesize that chondroid bone may be generally present in the growing limb bones of modern birds and hence may have key skeletogenic importance in achieving extreme avian growth rates and placing birds among the fastest growing vertebrates. Thus, we encourage future studies to test this hypothesis by investigating the occurrence of chondroid bone in a variety of precocial and altricial bird species, and to explore the presence of similar tissues in the growing limbs of other extant and extinct tetrapods in order to understand the evolutionary significance of chondroid bone in accelerated appendicular skeletogenesis

Scaling of avian bipedal locomotion reveals independent effects of body mass and leg posture on gait

This work was supported by a grant (‘Mechanics and energetics of stable bipedal locomotion in uneven terrain: Does a trade-off exist between economy and stability?’, BB/H005838/1) to M.A.D. from the Biotechnology and Biological Sciences Research Council (BBSRC)

Combining precision and power to maximize performance: a case study of the woodpecker's neck

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Modelling, design and control of a bird neck using tensegrity mechanisms

International audienceIn birds, the neck exhibits remarkable performances and serves as a dextrous arm for performing various tasks. Accordingly, it is an interesting bioinspiration for designing new manipulators with enhanced performances. This paper proposes a preliminary bird neck model using several stacked tensegrity crossed bar mechanisms. It addresses several issues regarding kinetostatic and dynamic modelling, design and control