Peter G. Tickle

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.

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.

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 influence of load carrying on the energetics and kinematics of terrestrial locomotion in a diving bird.

Summary The application of artificial loads to mammals and birds has been used to provide insight into the mechanics and energetic cost of terrestrial locomotion. However, only two species of bird have previously been used in loading experiments, the cursorial guinea fowl (Numida meleagris) and the locomotor-generalist barnacle goose (Branta leucopsis). Here, using respirometry and treadmill locomotion, we investigate the energetic cost of carrying trunk loads in a diving bird, the tufted duck (Aythya fuligula). Attachment of back loads equivalent to 10% and 20% of body mass increased the metabolic rate during locomotion (7.94% and 15.92%, respectively) while sternal loads of 5% and 10% had a greater proportional effect than the back loads (metabolic rate increased by 7.19% and 13.99%, respectively). No effect on locomotor kinematics was detected during any load carrying experiments. These results concur with previous reports of load carrying economy in birds, in that there is a less than proportional relationship between increasing load and metabolic rate (found previously in guinea fowl), while application of sternal loads causes an approximate doubling of metabolic rate compared to back loads (reported in an earlier study of barnacle geese). The increase in cost when carrying sternal loads may result from having to move this extra mass dorso-ventrally during respiration. Disparity in load carrying economy between species may arise from anatomical and physiological adaptations to different forms of locomotion, such as the varying uncinate process morphology and hindlimb tendon development in goose, guinea fowl and duck.

Barnacle Geese Achieve Significant Energetic Savings by Changing Posture

Here we report the resting metabolic rate in barnacle geese (Branta leucopsis) and provide evidence for the significant energetic effect of posture. Under laboratory conditions flow-through respirometry together with synchronous recording of behaviour enabled a calculation of how metabolic rate varies with posture. Our principal finding is that standing bipedally incurs a 25% increase in metabolic rate compared to birds sitting on the ground. In addition to the expected decrease in energy consumption of hindlimb postural muscles when sitting, we hypothesise that a change in breathing mechanics represents one potential mechanism for at least part of the observed difference in energetic cost. Due to the significant effect of posture, future studies of resting metabolic rates need to take into account and/or report differences in posture.

Uncinate Process Length in Birds Scales with Resting Metabolic Rate

A fundamental function of the respiratory system is the supply of oxygen to meet metabolic demand. Morphological constraints on the supply of oxygen, such as the structure of the lung, have previously been studied in birds. Recent research has shown that uncinate processes (UP) are important respiratory structures in birds, facilitating inspiratory and expiratory movements of the ribs and sternum. Uncinate process length (UPL) is important for determining the mechanical advantage for these respiratory movements. Here we report on the relationship between UPL, body size, metabolic demand and locomotor specialisation in birds. UPL was found to scale isometrically with body mass. Process length is greatest in specialist diving birds, shortest in walking birds and intermediate length in all others relative to body size. Examination of the interaction between the length of the UP and metabolic demand indicated that, relative to body size, species with high metabolic rates have corresponding elongated UP. We propose that elongated UP confer an advantage on the supply of oxygen, perhaps by improving the mechanical advantage and reducing the energetic cost of movements of the ribs and sternum.

The musculoskeletal anatomy of the reindeer (Rangifer tarandus): fore- and hindlimb

Reindeer are numerous and widespread across the northern Holarctic. They are efficient long distance migrants and are able to cope with variations in substrate, such as ice, snow, uneven forest floor, wetland and flat grassland. However, as with the vast majority of quadrupedal vertebrates, no quantitative musculoskeletal anatomical information exists for these animals making it difficult to analyse the biomechanics of their locomotor behaviour. In this paper, we describe the gross anatomy of the limb musculature and quantify muscle and tendon morphology. Reindeer show slight hindlimb dominance in muscle and tendon mass, with muscle mass primarily proximally situated and tendon distally situated. Extensor muscles are heavier than flexors, but tendon mass is broadly similar in both extensors and flexors. The only complete quadrupedal data sets available for comparison are for hares and greyhounds making it difficult to identify general patterns. There are no obvious body mass effects and reindeer often comes out as intermediate between hare and greyhound. However, greyhound seem less hindlimb dominated in terms of muscle but both greyhound and hare have much higher masses of tendon compared to reindeer, particularly in their hindlimbs. All these quadrupeds show the commonly observed trait of much larger tendons and less massive muscles in distal limb segments; this reduces the inertial cost of accelerating the limbs. Generally, there is a dearth of available quantitative anatomical data of complete animals. This lack of information is hindering attempts to gain a better understanding of musculoskeletal function in quadrupeds.

Ontogenetic development of the uncinate processes in the domestic turkey (Meleagris gallopavo)

Uncinate processes extend off the vertebral ribs in most species of bird. The processes are a crucial component of ventilatory mechanics, being involved in inspiration and expiration. Here we examine the pattern of ossification of the uncinate processes using histochemistry and biomechanical testing in developing domestic turkeys (Meleagris gallopavo). Ossification begins just before hatching, and the processes are fully ossified in the adult bird. We suggest that the development of these processes is linked to the onset of air breathing and the increase in sternal mass that occurs after hatching.