Once an animal gets beyond a few millimetres in size, simple diffusion is no longer enough to provide an adequate oxygen supply to cells. The need for the first complex animals to match increased oxygen demand with greater supply saw the advent of a convective circulatory system. Since this origin, different animal groups have evolved a variety of cardiovascular strategies to meet their metabolic and respiratory requirements. Evolutionary advancements, for example the evolution of endothermy, have necessitated an increase in efficiency of oxygen transport. This is mirrored by a gradual change from the single circuit ‘piscine design’ to the more complex cardiovascular systems of tetrapods. This article seeks to provide an overview of cardiac physiology across the vertebrate phylogeny.
Both cartilaginous (sharks and rays) and bony (teleost) fish have a single circuit cardiovascular system, with only one atrium and one ventricle. Teleosts, the most speciose group of fish, have a heart which comprises of four chambers. Venous blood returns to the sinus venosus, from where it subsequently enters the atrium. Blood then flows through atrioventricular valves into the single ventricle. During systole, blood is ejected through the bulbus arteriosus, where it passes into the systemic circulation. The blood then crosses the gills where it is oxygenated by a countercurrent exchanger.
This single circuit system attracts some interesting questions. Counterintuitively, the heart receives its oxygen supply from oxygen-poor venous blood. This means that at high temperatures, when other organs remove more oxygen from the blood, cardiac oxygen supply falls further. Indeed, some empirical data support the claim that high temperature decreases performance in certain fish, which may be attributed to the reduced myocardial oxygenation (Poertner and Knust, 2007; Wang and Overgaard, 2007). In an age of climate change, such research has clear conservational value. The extent to which performance is influenced by temperature in other species, however, is much debated. Indeed many active fish, such as tuna, have evolved advanced coronary circulation to provide oxygen-rich blood to their compact myocardium. It has even been suggested that lungs first evolved in fish to supply oxygen to the myocardium (Farmer, 1997).
Amphibians (frogs, salamanders & caecilians) represent the most basal extant tetrapod class, and it is here where we will first consider the importance of a pulmonary circulation. This is accompanied by a big cardiac morphological change; one atrium becomes two, albeit still with a single ventricle. Now, venous blood returns to the right atrium before entering the ventricle. From there, oxygen-poor blood is ejected through the pulmocutaneous artery. This vessel delivers blood to the two main amphibian respiratory organs, the lungs and skin, from where it returns to the left atrium (from the lungs) or straight into the systemic circulation (from the skin). From the left atrium the oxygen-rich blood enters the ventricle and during systole it is ejected into the systemic circulation. The proportion of blood being sent to the skin, as opposed to the lungs, is flexible and is determined by environmental factors such as hypoxia. Oxygen-rich and oxygen-poor blood are kept surprisingly separate in the ventricle. This is partly achieved by the presence of a spiral valve in the outflow tract (the conus arteriosus).
Squamates (snakes, lizards & tuataras) and testudines (turtles), like amphibians, have a heart composed of two atria with a single ventricle. The ventricle, however, is subdivided into 3 chambers; the cavum venosum, cavum pulmonale and cavum arteriosum. Oxygen-poor blood from the right atrium enters the cavum venosum before passing into the cavum pulmonale, from where it is pumped through the pulmonary artery to the lungs during systole. Oxygen-rich blood returns to the left atrium, then enters the cavum arteriosum, before being ejected into the systemic circulation through the dual aortic arches via the cavum venosum. This means, on the whole, oxygen-poor and oxygen-rich blood are kept separate. The whole story, however, is rather more complex.
A fascinating aspect of this cardiac design is the ability to mix, and control the mixing of, oxygen-rich and oxygen-poor blood. This process is known as cardiac shunting. In reptiles with a three chambered heart, vascular resistances determine the preferential route of blood flow. This is largely controlled by parasympathetic tone, as the vagus nerve innervates the pulmonary artery. We may distinguish between left-to-right and right-to-left shunting as follows:
To further understand shunting,we must review the anatomy of the crocodilian heart.
Crocodiles, like mammals and birds, have a more familiar four chambered heart with two atria and two ventricles. Rather less familiarly, crocodiles retain the two aortae, with the left aorta emerging from the right ventricle, whilst the right aorta originates at the left ventricle. The aortae connect at two locations; the foramen of Panizza immediately outside the heart, along with an abdominal anastomosis. This means that despite the ventricular septum, crocodiles can still achieve a right-to-left shunt by infusing oxygen-poor blood into the systemic circulation at these connections.
The evolutionary significance of cardiac shunting has been one of the most controversial topics in comparative physiology for the past 50 years. Although early views saw the mixing of blood as a fault (congenital heart disease with incomplete division of the heart is devastating in mammals), a multitude of functions have since been proposed. These have been comprehensively reviewed by Hicks (2002). Some of the most notable ideas include aiding thermoregulation, digestion and increasing diving performance. Attempts have been made to test these hypotheses, but thus far there is little conclusive data (and some of the more promising studies still attract controversy).
The previously described crocodile heart lends itself particularly well to surgical manipulation and an experimental approach. The left aortic arch can be occluded, preventing their ability to shunt. By using this technique, Eme et al. (2010) showed no difference in growth rate between alligators that can and can't shunt. This, along with other similar studies, has supported a view that shunts are not necessarily selected for, but rather have not been selected against (Hicks, 2002). Indeed, it is also possible that shunting has an adaptive benefit in embryos not seen in adult reptiles; a right-to-left shunt is functionally similar to the pulmonary bypass achieved in mammalian foetuses via the foramen ovale and ductus arteriosus. This embryonic state may be retained into adulthood because it is not maladaptive in these animals with low metabolic rates.
The non-avian reptiles also give insight into the importance of ventricular septation (i.e. whether the ventricle is divided or undivided). This is particularly important in respect to pressure separation: the ability to pump blood at different pressures in the systemic and pulmonary circulations. Pressure separation allows blood to be pumped at high pressure around the body, allowing for an increased oxygen supply, whilst keeping pulmonary pressure low, facilitating a thinner, and more efficient, blood gas barrier. Turtles, along with most snakes and lizards, cannot separate these pressures. Crocodiles have a ventricular septum so can pressure separate, as in mammals and birds. However, pythons and varanid lizards have an extraordinary ability to functionally pressure separate in the undivided ventricle. This occurs because two incomplete septae, the muscular ridge and the bulbuslamelle, meet during systole, thus functionally dividing the heart (Jensen et al., 2010). This ability may be crucial for varanid lizards particularly, which are renowned for their high aerobic performance.
Like their fellow endotherms, the mammals, birds have a four chambered heart with two atria and two ventricles. This design has evolved at least two times convergently; in mammals and at the base of archosaurs (in the common ancestor of crocodiles and birds). It is also possible that ventricular septation evolved separately in crocodiles and birds, but this would need confirmation by evidence from non-avian dinosaurs and stem archosaurs.
Having both evolved from ancestors with two aortae, mammals and birds have independently lost the second aorta. This happened differently in the groups; mammals lost the right aorta, birds lost the left aorta.
Birds achieve heart rates and blood pressures as high as mammals. The heart rate of hummingbirds, for example, can exceed 1000bpm. However, as a group, birds have been arguably understudied with respect to cardiovascular physiology, perhaps because they are more difficult to maintain in laboratories than other vertebrates.
The mammalian heart, particularly the human heart, is probably the most familiar to those who study biology or medicine. This does not, however, mean that mammals as a group can be overlooked by comparative physiologists. Mammals, from whales to shrews, show a diverse range of refinements on the same basic plan.
Giraffes, for example, maintain the highest blood pressure of any extant animal, which gives important insight into medical importance of hypertension. For blood to reach the giraffes head whilst standing, the systolic blood pressure reaches around 250 mmHg (healthy human systolic blood pressure would be less than half this). This presents a serious problem when the giraffe bends its neck down to drink. This action would be predicted to rapidly increase cranial blood pressure, causing a fatal, instantaneous haemorrhage. To avoid this problem, the jugular vein expands and acts as a volume reservoir (Brondum et al., 2009). Simultaneously, cerebrospinal fluid rushes to the head. This causes an increase in pressure that acts to reduce the pressure difference between outside and inside the blood vessels, thus preventing the vessels from rupturing.
Mammals are also particularly good thermoregulators. The cardiovascular system can act to prevent both dangerously high and low temperatures in vulnerable organs. A sprinting gazelle will generate so much heat that its brain would be at serious risk from suffering damage. This problem, however, is avoided due to an elegant counter current system of blood vessels (Taylor and Lyman, 1972). Evaporative water loss around the gazelles nose cools down venous blood before it returns to the heart. The carotid arteries that serve the brain, meanwhile, pass through a venous sinus containing this cooler blood. Therefore the blood that reaches the brain is cooled to tolerable levels.
A similar principle underlies the opposite problem that marine mammals encounter. In order to reduce heat loss at flippers, dolphins and other marine mammals have convergently evolved a similar counter current system. Here, arteries supplying the flipper are cooled by returning venous blood. But here, the heat is not being lost; it is simply transferred to the venous blood! This ability is not confined to mammals, however, and a similar process has evolved independently in penguin’s feet.
In order to understand cardiovascular physiology as a whole, it is vital to take a step back and see how other animals have solved their own problems. It is only then, that we can fully appreciate the intricacies of our own circulation. Ultimately, this can then advance medical knowledge. However, in the short term, it is perhaps most important to humbly appreciate different animals in their own right.
Brondum, E., Hasenkam, J. M., Secher, N. H., Bertelsen, M. F., Grondahl, C., Petersen, K. K., Buhl, R., Aalkjaer, C., Baandrup, U., Nygaard, H. et al. (2009). Jugular venous pooling during lowering of the head affects blood pressure of the anesthetized giraffe. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 297, R1058-R1065.
Farmer, C. (1997). Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates? Paleobiology 23, 358-372.
Hicks, J. W. (2002). The physiological and evolutionary significance of cardiovascular shunting patterns in reptiles. News in Physiological Sciences 17.
Jensen, B., Nielsen, J. M., Axelsson, M., Pedersen, M., Lofman, C. and Wang, T. (2010). How the python heart separates pulmonary and systemic blood pressures and blood flows. Journal of Experimental Biology 213.
Poertner, H. O. and Knust, R. (2007). Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95-97.
Taylor, C. R. and Lyman, C. P. (1972). HEAT STORAGE IN RUNNING ANTELOPES - INDEPENDENCE OF BRAIN AND BODY TEMPERATURES. American Journal of Physiology 222, 114-&.
Wang, T. and Overgaard, J. (2007). The heartbreak of adapting to global warming. Science 315, 49-50.
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