Crocodiles are beasts with an odd mix of features: they are ectothermic (meaning that they derive their body heat from their environment) reptiles, like lizards and snakes, but unlike those smaller critters, they have a fairly sophisticated, high performance cardiovascular system: they have a true four-chambered heart, just like us mammals and birds, and they also have a diaphragmaticus, a muscle analogous to our diaphragm that is used to inflate the lungs. At the same time, their hearts are relatively small—heart mass is roughly 0.15% of body mass, compared to 0.4%-0.7% of body mass for mammals—and generates relatively low systemic blood pressure.

It's weird. It's like they have this fancy, sophisticated engine in low-tech chassis, that the animal never revs up to its full potential. How did it get in there, and why do crocodiles have such fancy hearts?

The answer may be that they inherited it from more active, endothermic ancestors.

Here's what a crocodile heart looks like. Look at all that plumbing! It has a few features that we don't have, that I'll get to in a moment, and that are special adaptations for the life of an ectothermic, diving ambush predator.

The key feature, and one that I recall being brought up in comparative physiology courses, is that unlike other reptiles, they have complete four-chambered hearts. What this means is that their heart, like ours, is a double-circuit pump, essentially two pumps in one. Each side has an atrium that receives venous, blood under low pressure, and pumps it into a ventricle, which drives blood under higher pressure to the periphery. In a double-circuit pump, the right side is specialized to handle just the pulmonary circulation: it pumps deoxygenated blood to the lungs. The left side is the more powerful side, which has the job of pumping blood to all the rest of the body.

Lizards and snakes have a three-chambered heart. One atrium receives venous, oxygenated blood from the lungs, one receives venous, deoxygenated blood from the body, and both pump them into the single ventricle. When the ventricle contracts, it drives blood simultaneously to both the lungs and the body. This is inefficient in some ways, because there is the potential for mixing oxygenated and deoxygenated blood, and pumping some blood that is already carrying its oxygen load to the lungs, and some blood that hasn't been oxygenated yet to the tissues—although the animals may also have other features in the design of their hearts to minimize mixing.

A common kind of human birth defect is the "hole in the heart", such as the Tetralogy of Fallot, in which there is leakage between the pulmonary and systemic circulation. This reduces the efficiency of the heart. It's not quite kosher to compare a congenital defect to the well-adapted arrangement of another organism's heart, but that'll give you a feel for the nature of the problem. The animals with three-chambered hearts tend to have much lower metabolic rates, so the loss of efficiency is tolerable.

I was always taught that the most important function of the separate pulmonary and systemic circulation was to prevent mixing of oxygenated and deoxygenated blood. Seymour et al. mention another very important reason, though: it also allows the two pumps to generate different blood pressures. In us mammals, our systemic pressure is relatively high (120/80 mm Hg, on average), but our pulmonary pressure is much, much lower—more like 20-40 mm Hg. Pumping blood at systemic pressures through the thin, delicate membranes of the lung would not be a good thing. More plasma would be forced out into the spaces of the lung, drowning us.

(Note: in modern crocodilians, but the systemic and pulmonary pressures are in the region of the pulmonary range for mammals and birds)

So here's the idea: a major force driving the evolution of the four-chambered heart was selection for a high-pressure systemic circulation that could support an active lifestyle and endothermy, while isolating the pulmonary circulation from that damaging high pressure. Crocodilians don't need this now—their systemic and pulmonary pressures are roughly in the same range—but maybe their ancestors did.

In addition to the completely divided heart, the authors note other curiously sophisticated properties of the crocodile. They have complex, bird-like lung structure, and birds are the pulmonary champions among the vertebrates, with amazingly efficient respiratory surfaces. They have muscular specializations for lung inflation during active locomotion which seem superfluous in a sit-and-wait ambush predator. Their bones have the characteristic richly vascularized structure of fibrolamellar bone, one of the hallmarks of endothermy and one of the pieces of evidence that dinosaurs were warm blooded. Interestingly, one bit of counter evidence used against the hot-blooded dino hypothesis was the fact that crocodilians have the same structure…maybe there's another reason for the similarity, that crocs are also descended from hot-blooded ancestors.

One particularly interesting piece of evidence to me was the analysis of development of the crocodile heart. Despite being four-chambered, the crocodile heart also has a couple of specializations that reduce its efficiency, although they seem to be important for endurance in diving. There is a hole in the heart called the foramen of Panizza, which allows blood to be shunted from the right side of the heart to the systemic circulation, introducing deoxygenated blood. There is also a special valve called the cog-tooth valve in the right ventricle; when constricted, it increases the pressure in the right chamber of the heart and promotes circulatory shunting into the left aorta and foramen of Panizza. The animal can regulate shunting, increasing it during dives to send more hypoxic blood to the tissues, inducing a hypometabolic state—just the thing when you want to lurk underwater for a good long while.

The result of the developmental analysis was to find that these specialized diving features are all late add-ons. The heart initially develops a complete separation, and then secondarily punches the foramen of Panizza through. All this suggests that the crocodile heart evolved to support an active, endothermic lifestyle, and only in the modern lineages did they secondarily acquire features to adapt themselves to a more sluggish, conservative metabolic pattern.

The authors do concede that none of the evidence is definitive, and even that there is some counter-evidence: the absence of evidence for any kind of thermal insulation, and the absence of nasal turbinates, which form the convoluted outflow surfaces of the respiratory system and are important in conserving temperature and water.

Still, it's cool to imagine that 10-ton Sarcosuchus, the super-crocodile of the Cretaceous, might also have been an endotherm…which would have meant that it was hungry all the time, and would have had the high-powered, fast-moving metabolism of a mammal, a bird, or a dinosaur.

Alternatively, it could have already made the transition to a cold-blooded, slower-moving killer, and it was its smaller ancestral stem archosaurs that were endothermic. That's interesting, too, because it makes endothermy a primitive condition in this large and successful clade of reptiles.

Seymour RS, Bennet-Stamper CL, Johnston SD, Carrier DR, Grigg GC (2004) Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiological and Biochemical Zoology 77(6):1051-1067.