Gait-specific energetics contributes to economical walking and running in emus and ostriches.

A widely held assumption is that metabolic rate (E(met)) during legged locomotion is linked to the mechanics of different gaits and this linkage helps explain the preferred speeds of animals in nature. However, despite several prominent exceptions, E(met) of walking and running vertebrates has been nearly uniformly characterized as increasing linearly with speed across all gaits. This description of locomotor energetics does not predict energetically optimal speeds for minimal cost of transport (E(cot)). We tested whether large bipedal ratite birds (emus and ostriches) have gait-specific energetics during walking and running similar to those found in humans. We found that during locomotion, emus showed a curvilinear relationship between E(met) and speed during walking, and both emus and ostriches demonstrated an abrupt change in the slope of E(met) versus speed at the gait transition with a linear increase during running. Similar to human locomotion, the minimum net E(cot) calculated after subtracting resting metabolism was lower in walking than in running in both species. However, the difference in net E(cot) between walking and running was less than is found in humans because of a greater change in the slope of E(met) versus speed at the gait transition, which lowers the cost of running for the avian bipeds. For emus, we also show that animals moving freely overground avoid a range of speeds surrounding the gait-transition speed within which the E(cot) is large. These data suggest that deviations from a linear relation of metabolic rate and speed and variations in transport costs with speed are more widespread than is often assumed, and provide new evidence that locomotor energetics influences the choice of speed in bipedal animals. The low cost of transport for walking is probably ecologically important for emus and ostriches because they spend the majority of their active day walking, and thus the energy used for locomotion is a large part of their daily energy budget.

Minimal distensibility of pulmonary capillaries in avian lungs compared with mammalian lungs.

Previous physiological studies suggest that avian pulmonary capillaries behave like almost rigid tubes. We made morphometric measurements to determine the diameter of the capillaries in chicken lungs when the transmural pressure was altered over a wide range. The diameter of avian pulmonary capillaries increased by only 13% when the pressure inside them was raised from 0 to 25 cmH(2)O. In contrast, other studies have shown that the mean width of the pulmonary capillaries in dogs increased by about 125% and in cats by 128% for the same pressure change. Furthermore, raising the pressure 35 cmH(2)O outside the capillaries compared to the pressure inside the capillaries in chicken lungs caused little change in diameter whereas under the same conditions in mammal lungs the capillaries are completely collapsed. We conclude that the epithelial bridges between the blood capillaries in the bird lung provide strong support to the capillaries both in expansion and compression.

Major differences in the pulmonary circulation between birds and mammals.

The lungs of domestic chickens were perfused with blood or dextran/saline and the pulmonary artery pressure (P(a)) and venous pressure (P(v)) were varied in relation to air capillary pressure (P(A)). In Zone 3 conditions, pulmonary vascular resistance (PVR) was virtually unchanged with increases in either P(a) or P(v). This is very different behavior from mammals where the same interventions greatly reduce PVR. In Zone 2 conditions blood flow was essentially independent of P(v) as in mammalian lungs but all the capillaries appeared to be open, apparently incompatible with a Starling resistor mechanism. In Zone 1 the capillaries were open even when P(A) exceeded P(a) by over 30 cm H(2)O which is very different behavior from that of the mammalian lung. We conclude that the air capillaries that surround the blood capillaries provide rigid support in both compression and expansion of the vessels. The work suggests a pathogenesis for pulmonary hypertension syndrome in chickens which costs the broiler industry $1 billion per year.

Volume density and distribution of mitochondria in harbor seal (Phoca vitulina) skeletal muscle.

Recent studies have shown that harbor seals (Phoca vitulina) have an increased skeletal muscle mitochondrial volume density that may be an adaptation for maintaining aerobic metabolism during diving. However, these studies were based on single samples taken from locomotory muscles. In this study, we took multiple samples from a transverse section of the epaxial (primary locomotory) muscles and single samples from the m. pectoralis (secondary locomotory) muscle of five wild harbor seals. Average mitochondrial volume density of the epaxial muscles was 5.6%, which was 36.6% higher than predicted for a terrestrial mammal of similar mass, and most (82.1%) of the mitochondria were interfibrillar, unlike athletic terrestrial mammals. In the epaxial muscles, the total mitochondrial volume density was significantly greater in samples collected from the deep (6.0%) compared with superficial (5.0%) regions. Volume density of mitochondria in the pectoralis muscle was similar (5.2%) to that of the epaxial muscles. Taken together, these adaptations reduce the intracellular distance between mitochondria and oxymyoglobin and increase the mitochondrial diffusion surface area. This, in combination with elevated myoglobin concentrations, potentially increases the rate of oxygen diffusion into mitochondria and prevents diffusion limitation so that aerobic metabolism can be maintained under low oxygen partial pressure that develops during diving.

Morphometry of the extremely thin pulmonary blood-gas barrier in the chicken lung.

The gas exchanging region in the avian lung, although proportionally smaller than that of the mammalian lung, efficiently manages respiration to meet the high energetic requirements of flapping flight. Gas exchange in the bird lung is enhanced, in part, by an extremely thin blood-gas barrier (BGB). We measured the arithmetic mean thickness of the different components (endothelium, interstitium, and epithelium) of the BGB in the domestic chicken lung and compared the results with three mammals. Morphometric analysis showed that the total BGB of the chicken lung was significantly thinner than that of the rabbit, dog, and horse (54, 66, and 70% thinner, respectively) and that all layers of the BGB were significantly thinner in the chicken compared with the mammals. The interstitial layer was strikingly thin in the chicken lung ( approximately 86% thinner than the dog and horse, and 75% thinner than rabbit) which is a paradox because the strength of the BGB is believed to come from the interstitium. In addition, the thickness of the interstitium was remarkably uniform, unlike the mammalian interstitium. The uniformity of the interstitial layer in the chicken is attributable to a lack of the supportive type I collagen cable that is found in mammalian alveolar lungs. We propose that the surrounding air capillaries provide additional structural support for the pulmonary capillaries in the bird lung, thus allowing the barrier to be both very thin and extremely uniform. The net result is to improve gas exchanging efficiency.

The honeycomb-like structure of the bird lung allows a uniquely thin blood-gas barrier.

Flying requires enormous energy and some birds have higher mass-specific maximal oxygen consumptions than any mammal. The bird lung is very efficient partly because of an extremely thin blood-gas barrier so that some birds have thinner barriers than any mammals. We show here that in addition to the total barrier being very thin, the interstitium which is responsible for the barrier's strength is extraordinarily thin. This observation is paradoxical because intense exercise raises the pressure in pulmonary capillaries and results in large stresses in the capillary walls thus predisposing them to structural failure. For example, all galloping racehorses break their pulmonary capillaries. We propose that the explanation for how the bird can be so highly energetic yet also have such apparently fragile capillaries is the mechanical support provided by the dense packing of rigid air capillaries around the blood capillaries in the gas exchanging region of the lung. This architecture is very different from that in the mammalian lung.

Immunohistochemical fiber typing of harbor seal skeletal muscle.

There is strong evidence that pinnipeds maintain a lipid-based, aerobic metabolism during diving. However, the few fiber-typing studies performed on pinniped skeletal muscles are not consistent with an aerobic physiological profile. The objective of this study was to reexamine the fiber type distribution throughout the primary locomotory muscles of the harbor seal Phoca vitulina. Results from immunohistochemical (IHC) fiber typing indicated that harbor seal swimming muscles (the epaxial muscles) are composed of 47.4% type I (slow twitch, oxidative) fibers and 52.8% IIa (fast twitch, oxidative) fibers, which are homogeneously distributed throughout the muscle. Harbor seal pectoralis, a secondary swimming muscle, was composed of 16.2% type I and 84.3% type IIa fibers. No fast twitch, glycolytic (type IIb) fibers were detected in either muscle, in contrast to published data on fiber typing of harbor seal epaxial muscles using traditional histochemical techniques. The extreme specificity inherent in the IHC fiber typing procedure leads us to conclude that harbor seal swimming muscle is entirely composed of oxidative fibers. Our results are consistent with the enzymatic analyses of pinniped skeletal muscle that support the use of lipid-derived aerobic catabolism to fuel working muscle during diving in these marine mammals.