Jonathan R. Codd

Avian-like breathing mechanics in maniraptoran dinosaurs

In 1868 Thomas Huxley first proposed that dinosaurs were the direct ancestors of birds and subsequent analyses have identified a suite of ‘avian’ characteristics in theropod dinosaurs. Ossified uncinate processes are found in most species of extant birds and also occur in extinct non-avian maniraptoran dinosaurs. Their presence in these dinosaurs represents another morphological character linking them to Aves, and further supports the presence of an avian-like air-sac respiratory system in theropod dinosaurs, prior to the evolution of flight. Here we report a phylogenetic analysis of the presence of uncinate processes in Aves and non-avian maniraptoran dinosaurs indicating that these were homologous structures. Furthermore, recent work on Canada geese has demonstrated that uncinate processes are integral to the mechanics of avian ventilation, facilitating both inspiration and expiration. In extant birds, uncinate processes function to increase the mechanical advantage for movements of the ribs and sternum during respiration. Our study presents a mechanism whereby uncinate processes, in conjunction with lateral and ventral movements of the sternum and gastral basket, affected avian-like breathing mechanics in extinct non-avian maniraptoran dinosaurs.

Functional significance of the uncinate processes in birds

SUMMARY The functional significance of the uncinate processes to the ventilatory mechanics of birds was examined by combining analytical modeling with morphological techniques. A geometric model was derived to determine the function of the uncinate processes and relate their action to morphological differences associated with locomotor specializations. The model demonstrates that uncinates act as levers, which improve the mechanical advantage for the forward rotation of the dorsal ribs and therefore lowering of the sternum during respiration. The length of these processes is functionally important; longer uncinate processes increasing the mechanical advantage of the Mm. appendicocostales muscle during inspiration. Morphological studies of four bird species showed that the uncinate process increased the mechanical advantage by factors of 2–4. Using canonical variate analysis and analysis of variance we then examined the variation in skeletal parameters in birds with different primary modes of locomotion (non-specialists, walking and diving). Birds clustered together in distinct groups, indicating that uncinate length is more similar in birds that have the same functional constraint, i.e. specialization to a locomotor mode. Uncinate processes are short in walking birds, long in diving species and of intermediate length in non-specialist birds. These results demonstrate that differences in the breathing mechanics of birds may be linked to the morphological adaptations of the ribs and rib cage associated with different modes of locomotion.

Evidence for energy savings from aerial running in the Svalbard rock ptarmigan (Lagopus muta hyperborea)

Svalbard rock ptarmigans were walked and run upon a treadmill and their energy expenditure measured using respirometry. The ptarmigan used three different gaits: a walking gait at slow speeds (less than or equal to 0.75 m s−1), grounded running at intermediate speeds (0.75 m s−1 < U < 1.67 m s−1) and aerial running at high speeds (greater than or equal to 1.67 m s−1). Changes of gait were associated with reductions in the gross cost of transport (COT; J kg−1 m−1), providing the first evidence for energy savings with gait change in a small crouched-postured vertebrate. In addition, for the first time (excluding humans) a decrease in absolute metabolic energy expenditure (rate of O2 consumption) in aerial running when compared with grounded running was identified. The COT versus U curve varies between species and the COT was cheaper during aerial running than grounded running, posing the question of why grounded running should be used at all. Existing explanations (e.g. stability during running over rocky terrain) amount to just so stories with no current evidence to support them. It may be that grounded running is just an artefact of treadmill studies. Research investigating the speeds used by animals in the field is sorely needed.

The evolutionary origin of the mammalian diaphragm.

The comparatively low compliance of the mammalian lung results in an evolutionary dilemma: the origin and evolution of this bronchoalveolar lung into a high-performance gas-exchange organ results in a high work of breathing that cannot be achieved without the coupled evolution of a muscular diaphragm. However, despite over 400 years of research into respiratory biology, the origin of this exclusively mammalian structure remains elusive. Here we examine the basic structure of the body wall muscles in vertebrates and discuss the mechanics of costal breathing and functional significance of accessory breathing muscles in non-mammalian amniotes. We then critically examine the mammalian diaphragm and compare hypotheses on its ontogenetic and phylogenetic origin. A closer look at the structure and function across various mammalian groups reveals the evolutionary significance of collateral functions of the diaphragm as a visceral organizer and its role in producing high intra-abdominal pressure.

Load carrying during locomotion in the barnacle goose (Branta leucopsis): The effect of load placement and size☆

Load carrying has been used to study the energetics and mechanics of locomotion in a range of taxa. Here we investigated the energetic and kinematic effects of trunk and limb loading in walking barnacle geese (Branta leucopsis). A directly proportional relationship between increasing back-load mass and metabolic rate was established, indicating that the barnacle goose can carry back loads (up to 20% of body mass) more economically than the majority of mammals. The increased cost of supporting and propelling the body during locomotion is likely to account for a major proportion of the extra metabolic cost. Sternal loads up to 15% of body mass were approximately twice as expensive to carry as back loads. Given the key role in dorso-ventral movement of the sternum during respiration we suggest that moving this extra mass may account for the elevated metabolic rate. Loading the distal limb with 5% extra mass incurred the greatest proportional rise in metabolism, and also caused increases in stride length, swing duration and stride frequency during locomotion. The increased work required to move the loaded limb may explain the high cost of walking.

Periodic Fluctuations in the Pulmonary Surfactant System in Gould’s Wattled Bat (Chalinolobus gouldii)

Pulmonary surfactant is a mixture of phospholipids, neutral lipids, and proteins that controls the surface tension of the fluid lining the lung. Surfactant amounts and composition are influenced by such physiological parameters as metabolic rate, activity, body temperature, and ventilation. Microchiropteran bats experience fluctuations in these parameters throughout their natural daily cycle of activity and torpor. The activity cycle of the microchiropteran bat Chalinolobus gouldii was studied over a 24‐h period. Bats were maintained in a room at constant ambient temperature (24°C) on an 8L:16D cycle. Diurnal changes in the amount and composition of surfactant were measured at 4‐h intervals throughout a 24‐h period. The C. gouldii were most active at 2 a.m. and were torpid at 2 p.m. Alveolar surfactant increased 1.5‐fold immediately after arousal. The proportion of disaturated phospholipid remained constant, while surfactant cholesterol levels increased 1.5‐fold during torpor. Alveolar cholesterol in C. gouldii was six times lower than in other mammals. Cholesterol appears to function in maintaining surfactant fluidity during torpor in this species of bat.

Implications of an avian-style respiratory system for gigantism in sauropod dinosaurs.

In light of evidence for avian-like lungs in saurischian dinosaurs, the physiological implications of cross-current gas exchange and voluminous, highly heterogeneous lungs for sauropod gigantism are critically examined. At 12 ton the predicted body temperature and metabolic rate of a growing sauropod would be similar to that of a bird scaled to the same body weight, but would increase exponentially as body mass increases. Although avian-like lung structure would be consistent with either a tachymetabolic-endothermic or a bradymetabolic-gigantothermic model, increasing body temperature requires adjustments to avoid overheating. We suggest that a unique sauropod structure/function unit facilitated the evolution of gigantism. This unit consisted of (1) a reduction in metabolic rate below that predicted by the body temperature, akin to thermal adaptation as seen in extant squamates, (2) presence of air-filled diverticula in the long neck and in the visceral cavity, and (3) low activity of respiratory muscles coupled with the high efficiency of cross-current gas exchange.

Understanding sex differences in the cost of terrestrial locomotion

Little is known regarding the physiological consequences of the behavioural and morphological differences that result from sexual selection in birds. Male and female Svalbard rock ptarmigans (Lagopus muta hyperborea) exhibit distinctive behavioural differences during the breeding season. In particular, males continuously compete for and defend territories in order to breed successfully, placing large demands on their locomotor system. Here, we demonstrate that male birds have improved locomotor performance compared with females, showing both a lower cost of locomotion (CoL) and a higher top speed. We propose that the observed sex differences in locomotor capability may be due to sexual selection for improved male performance. While the mechanisms underlying these energetic differences are unclear, future studies should be wary when pooling male and female data.

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.

A potential role for bat tail membranes in flight control.

Wind tunnel tests conducted on a model based on the long-eared bat Plecotus auritus indicated that the positioning of the tail membrane (uropatagium) can significantly influence flight control. Adjusting tail position by increasing the angle of the legs ventrally relative to the body has a two-fold effect; increasing leg-induced wing camber (i.e., locally increased camber of the inner wing surface) and increasing the angle of attack of the tail membrane. We also used our model to examine the effects of flying with and without a tail membrane. For the bat model with a tail membrane increasing leg angle increased the lift, drag and pitching moment (nose-down) produced. However, removing the tail membrane significantly reduced the change in pitching moment with increasing leg angle, but it had no significant effect on the level of lift produced. The drag on the model also significantly increased with the removal of the tail membrane. The tail membrane, therefore, is potentially important for controlling the level of pitching moment produced by bats and an aid to flight control, specifically improving agility and manoeuvrability. Although the tail of bats is different from that of birds, in that it is only divided from the wings by the legs, it nonetheless, may, in addition to its prey capturing function, fulfil a similar role in aiding flight control.