C. Richard Taylor

Design of the mammalian respiratory system. I. Problem and strategy

This paper introduces a series of reports on the structure and function of the respiratory system of mammals. We propose and justify the hypothesis that structural design is a limiting factor for O2 flow at each level of the respiratory system. The background, the reasons, and the plan for the studies are described. The main approach is to compare the size of respiratory structures with maximal O2 consumption in a series of mammals spanning several orders of magnitude in body size. The papers that follow present the methods and results for maximal O2 consumption, pulmonary diffusing capacity, mitochondrial volume, and capillary density in muscles.

Design of the mammalian respiratory system. V. Scaling morphometric pulmonary diffusing capacity to body mass: wild and domestic mammals.

This paper utilizes a comparative approach to establish the relationship between morphometric diffusing capacity for oxygen (DLo2) and maximal oxygen consumption (Vo2max). DLo2 and Vo2max were determined on the same 21 individuals in African mammals spanning a range in body mass from 0.4 to 240kg. We confirmed earlier findings that Dlo2 was proportional to Mb0.99 while Vo2max was proportional to Mb0.79. Thus, the ratio of Dlo2/Vo2 is approximately proportional to Mb0.20. We conclude that large animals require a larger pulmonary diffusing capacity to transfer oxygen at the same rate from air to blood.

Running Up and Down Hills: Some Consequences of Size

Small mammals are able to run at about the same maximum speed vertically as horizontally, but larger mammals cannot do this. During level running a mouse weighing 30 grams uses about eight times as much energy per unit of body weight as does a chimpanzee weighing 17.5 kilograms (42.6 joules per kilogram meter versus 5.17 joules per kilogram meter). The additional energy required to lift 1 kilogram of body weight 1 meter while running uphill was similar for the two species (about 15.5 joules per kilogram meter). Therefore the increment in energy expenditure for mice to run uphill compared to running horizontally is about one-eighth that for a chimpanzee. Both mice and chimpanzees were able to recover about 90 percent of the energy stored running uphill on the way down.

Adaptive variation in the mammalian respiratory system in relation to energetic demand: I. Introduction to problem and strategy

Abstract This paper introduces a series of reports on structural and functional variations of the respiratory system of ‘athletic’ dogs and ponies as compared to ‘normal’ goats and calves. The pathway for oxygen from lungs to skeletal muscle mitochondria is analyzed in an integrated fashion to determine how the athletic species combine variations in structural and functional design parameters of the lungs, the heart, the muscle microvasculature and their mitochondria to adapt the respiratory system to the needs of a 2.5-fold higher level of aerobic performance capacity. The hypothesis of symmorphosis stating that the structural design is commensurate with functional needs is tested.

Running on Two or on Four Legs: Which Consumes More Energy?

Disagreement exists over whether mans bipedal form of locomotion evolved as an economical means for covering long distances. There is also some disagreement about the energetic price man had to pay to free his hands. In an investigation of the relative energetic cost of bipedal and quadrupedal locomotion in primates, chimpanzees (Pan troglodytes) and capuchin monkeys (Cebus capucinus) were trained to run on a treadmill either on two or on four legs while their oxygen consumption was being measured. Both primates expend the same amount of energy whether running on two or on four legs. The relative energy cost of bipedal versus quadrupedal running should not be used in arguments about the evolution of bipedal locomotion in man.

Design of the mammalian respiratory system. VII. Scaling mitochondrial volume in skeletal muscle to body mass

Since O2 is mainly consumed in muscle mitochondria during heavy physical work, one would expect to find a relationship between the volume density of mitochondria in skeletal muscles and maximal O2 uptake. We analyzed the volume density of mitochondria, Vv(mt,f) in four muscles of a series of African mammals ranging in body mass from 0.4 to 251 kg. Vv(mt,f) scaled as Mb-0.231, Mb-0.163, Mb-0.139 and Mb-0.055 in Mm. semitendinosus, longissimus dorsi, vastus medialis and diaphragm, respectively. The mass or volume of diaphragm was found to scale as Mb0.865, whereas for Mm. semitendinosus and vastus medialis, muscle volume (Vmu) scaled as Mb1.030 and Mb0.956 respectively. Scaling the absolute volume of mitochondria Vmt, in these muscles (Vmt = Vv (mt,f) x Vmu) against Mb gives regression lines whose slopes closely parallel that obtained for Vo2max against body mass. Therefore the ratio of volume of mitochondria in these muscles to Vo2max is body mass independent.

Design of the mammalian respiratory system. IX. Functional and structural limits for oxygen flow.

This paper presents the synthesis and interpretation of a series of correlated studies of the mammalian respiratory system--measurements of maximal rate of O2 consumption, the lungs diffusing capacity, the mitochondrial volume, and the capillary number and length in skeletal muscle. It discusses the results with respect to the principle of symmorphosis, i.e. of morphogenesis adapted to functional needs. We find that the accumulated evidence supports this principle at all organizational levels considered, although the models used for structure-function correlation need further refinement.

Adaptive variation in the mammalian respiratory system in relation to energetic demand: II. Reaching the limits to oxygen flow

Abstract We address the quesion of how animals adjust steady-state rates of oxygen transport from the lungs to the mitochondria over a range of exercise intensities from rest to the upper limit (V O 2 max). Convective transport of oxygen in the circulation is central to this process, establishing the boundary condition for the pressure heads for diffusion of O 2 in the lung and in the tissues. Athletic dogs and ponies are compared to less athletic animals of the same size, goats and calves. We find: (1) V O 2 max is reached after a 29-fold increase from predicted resting levels in the athletic species, while the goat and calf are capable of only a 12-fold increase; (2) cardiac output is the most important variable controlling flow of oxygen through the circulation; (3) adjustments of cardiac output are brought about primarily by changing heart rate; (4) the difference in arteriovenous oxygen content is also a dynamic regulator of oxygen flow, increasing with exercise intensity due to both an increase in concentration of circulating erythrocytes and more of the blood flowing to active models; and (5) the pressure head for oxygen diffusion in the lung and tissues increases durign exercise as a result of increased blood flow and hyperventilation.

Adaptive variation in the mammalian respiratory system in relation to energetic demand: IV. Capillaries and their relationship to oxidative capacity

Abstract We analyzed the capillarity of the heart, diaphragm, M. vastus medialis and M. semitendinosus of dogs, goats, ponies and calves ( n = 3 each). Blocks of tissue were preserved, processed and photographed bye electron microscopy. Using morphometric techniques we estimated capillary density, capillary lenght density and total capillary length in these muscles. The highly aerobic dogs and ponies had greater total capillary lenghts and larger muscles than the less aerobic goats and calves. A significant correlation was found between capillary length density (J V (c,f)) and mitochondrial volume density (V V (mt,f)) which was: J V (c,f) = 258 + 1.25·10 4 V V (mt,f). From this correlation we calculated an average of 14 km or 0.22 ml of capillaries per milliliter of mitochondria. With these values and data from blood gas analysis (Karas et al. , 1987), we calculated a mean minimum transit time for blood in capillaries of approximately 0.5 sec for all four species. At the tissue level, the greater aerobic metabolic capacity of dogs and ponies was supported in equal parts by the larger capillary supply of the muscle tissue and by the higher oxygen carrying capacity of the blood.

Variations in function and design: Testing symmorphosis in the respiratory system

We explore the question of whether and to what extent the large variation in energy requirements observed among mammals is related to variations in the design of the respiratory system, from the lung to the mitochondria in muscle cells. Resting metabolic rate is determined by body size (allometric variation). Maximal rates of O2 consumption (VO2 max) also vary in a regular manner with body size, but adaptive variation allows some species to achieve much higher values than others of the same body size. We, therefore, consider adaptive variation as modulation of structures and functions above those determined by allometric variation. A model is presented that separates functional and design parameters at four steps of the respiratory cascade: the pulmonary gas exchanger, heart and blood, microvasculature, and mitochondria. The variations observed in these parameters are analyzed with respect to those in energy demand and are discussed in relation to the hypothesis of symmorphosis. We conclude that the design of the internal steps of the respiratory system (mitochondria, capillaries, blood, and heart) is matched to functional demand, whereas the lung maintains a variable excess of morphometric diffusing capacity which may be related to the facts that the lung has limited malleability and that it forms the interface with the environment.