Respiration, Metabolism, and Locomotion

David Carrier put together some simple but powerful ideas about the links between respiration, locomotion, and physiology.

Fishes have no problem maintaining high levels of exercise. Many sharks swim all their lives without rest, for example. Gill respiration gives all the oxygen exchange needed for such exercise levels, and with good hunting skills, the necessary food supply is readily available. The evolution of lungs did not change that relationship between anatomy and physiology. Air has to be pumped in and out of an internal body cavity, however, and living lungfishes may have rather low exercise levels because their oxygen exchange is not geared for high performance.

Tetrapods moving about on land face a much more serious problem. The shoulder girdle and the forelimbs in particular, powered in part by the muscles of the trunk, are largely devoted to supporting and moving the body over the ground. In the sprawling gait of amphibians and living reptiles, the trunk is twisted first to one side and then the other in walking and running. As the animal steps forward with its left front foot, the right side of the chest and the lung inside it are compressed while the left side expands (Figure 11.6). Then the cycle reverses with the next step. This distortion of the chest interferes with and essentially prevents normal breathing, in which the chest cavity and both lungs expand uniformly and then contract. If the animal is walking, it may be able to breathe between steps, but sprawling vertebrates cannot run and breathe at the same time. I shall call this problem Carrier's Constraint.

Animals can run for a while without breathing: for example, Olympic sprinters usually don't breathe during a 100-meter race. Animals can generate temporary energy by anaerobic glycolysis, breaking down food molecules in the blood supply without using oxygen. But this process soon builds up an oxygen debt and a dangerously high level of lactic acid in the blood. Mammalian runners (cheetahs and humans, for example) often use anaerobic glycolysis even though they can breathe while they run; it's a useful but essentially short-term emergency boost, like an afterburner in a jet fighter.

Living amphibians and reptiles, then, can hop or run fast for a short time, first using up the oxygen stored in their lungs and blood, then switching to anaerobic glycolysis. They cannot sprint for long, however. If lizards want to breathe, they have to stand still with feet symmetrical. Lizards run in short rushes, with frequent stops. By attaching recorders to the body, Carrier showed that the stops are for breathing, and that lizards don't breathe as they run. Therefore, all living amphibian and reptilian carnivores use ambush tactics to capture agile prey: chameleons and toads flip their tongues at passing insects, for example.

The giant varanid lizard, the ora or Komodo dragon, which eats deer, pigs, and tourists (most notably, Baron Rudolf von Reding on 18 July 1974), goes a little way toward solving Carrier's Constraint by pumping air into its lungs from a throat pouch; but that only gives it a small improvement in performance. The Komodo dragon has a short sprinting range, but it prefers to ambush prey from 1 meter away.

Amphibians and most living reptiles have a three-chambered heart, which has usually been regarded as inferior to the four-chambered heart of living mammals and birds. But the three-chambered heart is useful to a lizard. Lizards run to catch food or to get away from danger, so they must use their resources most efficiently at this time. In a run, it is useless and perhaps dangerous for the lizard to waste energy pumping blood to lungs that cannot work. The lizard thus uses all the heart and blood capacity it has to circulate its store of oxygen around the whole body. The price it pays is a longer recharging time when it has to resupply oxygen to the blood, but it is usually able to do this at a less critical moment. Early tetrapods all had sprawling gaits and faced a great problem. Their respiration and locomotion used much the same sets of muscles, and both systems could not operate at the same time. Imagine the laborious journey of Ichthyostega from the water to its breeding pools, with a few steps and a few gasps repeated for the whole journey. One can understand why so many early amphibians remained adapted to life spent largely in water, and why many early reptiles often looked amphibious.

Eryops, for example, swam with its tail (Figure 9.4) and would have had no major difficulty in devoting its rib-cage muscles to taking deep breaths at the surface. Horned nectrideans evolved ways to cut down undulation of their bodies as they swam, and perhaps they did this for air breathing rather than feeding (compare the discussion in Chapter 9).

When we see land animals such as pelycosaurs, with stiffened backbones and teeth designed for carnivorous and vegetarian diets rather than fish eating, we have to conclude that the problem had at least partially been solved. It's no good, for example, to raise metabolic rate by solar thermoregulation if there is no reliable oxygen supply to tissues.

I suggest that the secret of the pelycosaurs was the stiffening of the backbone. They simply did not twist the body much as they moved. They had long bodies and relatively short limbs compared with lizards, and in any case a short step would not have rotated the trunk very much or distorted the lungs. The stiffening of the body also meant that most of the forelimb rotation was taken up at the shoulder joint, rather than being transmitted to the trunk. Furthermore, pelycosaurs had wheelbarrow locomotion, and the front limbs were mainly reactive support props, so the muscles operating them did not exert forces on the chest wall except to support the shoulder joint. On the other hand, the driving muscles of the pelvic girdle attached far from the chest wall.

The pelycosaurs thus had a special synapsid mitigation of Carrier's Constraint: they evolved adaptations that went some way toward reducing its consequences. (If you understand that point, look back at the skeleton of Ichthyostega [Figure 8.15]. Perhaps there is an analogous reason for its peculiar rib structure?) But pelycosaurs could not solve Carrier's Constraint. There is no way that they were running freely, or breathing while they ran.

The reptilian idea of fun
Is to bask all day in the sun.
A physiological barrier,
Discovered by Carrier,
Says they can't breathe, if they run.

Fishes can swim in water with sustained energy because Carrier's Constraint does not apply to gill breathing. The same is probably true for the lung breathing of turtles, because their shell does not allow the lungs to be distorted as they swim and come to the surface to breathe.

Many living land vertebrates have evolved a beautiful answer to Carrier's Constraint. They have freed the mechanics of respiration from the mechanics of locomotion by evolving an erect stance. The body is suspended more freely from the shoulders, allowing the thorax to make its breathing movements with hardly any twisting.

The evolutionary solution to Carrier's Constraint that resulted from erect stance is shown best today in mammals. Mammals evolved the diaphragm, a set of muscles to pump air in and out of the chest cavity. Air is sucked in as the diaphragm contracts, and forced out by the reaction of the elastic tissues of the lung. At the same time, the locomotion in most mammals has evolved to encourage breathing on the run. The backbone flexes and straightens in an up-and-down direction with each stride, alternately expanding and compressing the rib cage evenly (Figure 11.7). This rhythmic pumping of the chest cavity in the running action can be synchronized with the action of the diaphragm to move air in and out of the lungs with little effort. Thus quadrupeds running at full speed‹ gerbils, jackrabbits, dogs, horses, and rhinoceroses‹take one breath per stride, and wallabies take one breath per hop (Figure 11.7). Trotting is far more complex, but that doesn't harm the line of argument presented here. Human runners usually take a breath every other stride. It is such a natural action that we don't notice it: runners should try to breathe out of phase to get some idea of the mechanism.

Animal locomotion often involves cyclic movements such as the strides and strokes of running or swimming limbs, or wingbeats in flight. Breathing may be made more efficient if it is synchronized with certain phases of limb movement. This is particularly important in human swimming, but it is a general principle. Flying insects synchronize their respiration with their wingbeats: the same muscular actions that raise and lower the wings also act to expand and compress the body, forcing air in and out of the spiracles. Birds do much the same thing (Chapter 14).

These principles are pieces of basic animal physiology, and they should be as true for extinct animals as they are for modern ones. Therefore, erect stance might be necessary for sustained running in any land animal, and its evolution should represent a great breakthrough in any tetrapod lineage, giving the basis for greatly improved running speed and stamina. Living reptiles are successful, but they are limited in the ecological roles they can perform because they have a sprawling gait and cannot sustain fast movement for very long.

Diapsids living today, such as lizards, don't have erect stance or sustained energy output, but we must not be fooled into thinking that all diapsids have always lacked those capabilities. David Carrier suggests that the Triassic diapsids‹the archosauromorphs in particular‹were the first tetrapods to make the breakthrough to erect gait and rapid, sustained locomotion. That breakthrough is preserved in the fossil record in the structure of the limbs and shoulder girdles of the early archosauromorphs. Erect gait and sustained locomotion was most likely the key innovation that made possible the diapsid, and in particular the archosaur, takeover of the Late Triassic.

I suggest here that an accident of history played an important role in forming the differences between Triassic diapsids and synapsids. Therapsids evolved largely in cool climates of the late Permian, in northern Laurasia and southern Gondwanaland, while Permian diapsids evolved in warmer climates. Part of a heat-retaining syndrome in cool climates is to have stocky, compact bodies and short limbs and appendages, and therapsids are characteristically built that way (for example, Figure 10.14).

Diapsids, on the other hand, had long, strong tails, and much of their body weight was on the hind limbs. Many diapsids became partly or totally bipedal, and it may have been comparatively easy for them to evolve erect limbs from a bipedal stance. Therapsids, with short tails, did not have that option, and all of them were quadrupeds with a good deal of weight on the front feet. It may have been difficult to escape from the wheelbarrow locomotion that the therapsids inherited from the pelycosaurs, especially at larger body size. Truly erect gait‹the solution to Carrier's Constraint‹did not evolve among synapsids until the mammals of the Early Jurassic.