The Reptilian and Amphibian Circulatory Systems: Form, Function, and Venipuncture Sites
Department of Biological Sciences, Florida Atlantic University, Boca Raton, FL, USA
Abstract
The circulatory system is the functional delivery and distribution system for the body’s heat, fluids, gases, nutrients, many ions, hormones, cellular waste products, and immune responses. Blood samples and analyses provide major insight into an animal’s near-term health. This overview of the circulatory system provides the framework to understand the major anatomical patterns, the pathways blood takes, as well as the functional relationships among the structures in amphibian and reptilian patients.
Introduction
There are fundamental differences in amphibian and reptilian circulatory systems. Amphibians and reptiles have hearts formed of a thin-walled sinus venosus, and two atria. Amphibian hearts have a single ventricle with outflow to the paired aortae and a pulmocutaneous system that supports gas exchange. Reptiles have a muscular ventricle that is partially divided as cava in chelonians, lizards, snakes, and tuataras and fully divided into right and left ventricular chambers in crocodilians. The basic pattern of arterial circulation leaving the heart is paired aortae and the aortic arches. The left and right aortae join as a single vessel in the coelomic cavity and supply the kidneys, gonads, hindlimbs, and tail (when a tail is present).
Amphibian Circulation
The location of the heart varies within lineages and even within taxa. The amphibian heart tends to be located just cranial to the shoulders and extends to the base of the neck in Anurans (frogs and toads) and Caudata (salamanders and newts). Because frogs, mudpuppies, and urodele salamanders (especially axolotls) were used for decades in biology labs and developmental and reproductive studies, there is a fairly rich array of descriptive and illustrated guides available; many are in the older literature, yet remain as sound references.1-5 There is relatively little information on the Gymnophiona (Caecilians).
Most amphibians undergo metamorphosis; consequently, the circulation of larval forms includes major branches of the aortic arches supplying the gills and tail. In anurans, both gills and tail regress, and limbs develop. Concurrent with these gross morphological changes is significant remodeling of the circulatory systems, particularly the aortic arches and the tributaries of the femoral arteries and caudal venous drainage. The changes in the larval to adult circulation in the Caudata usually are less extreme, largely due to the larval forms having legs and they retain a tail during metamorphosis. In most anurans and urodele larval forms, the paired aortae give off branches to three pairs of aortic arches to external gills and a pair of branches to each developing lung (the pulmonary arteries); cranial to the gills, the internal and external carotids extend into the head. The external carotid connects to the dorsal aorta. In adults, the pulmonary arteries and three aortic arches persist as systemic vessels, bypassing the now resorbed gills, and the external carotid loses its connection to the dorsal aorta. In adult frogs and toads, a cutaneous artery arises from the same aortic arch that gives rise to the pulmonary artery.5 Venous drainage in salamanders is via a caudal vein that is joined by external iliac and femoral veins. Blood can then return to the heart via several alternative routes. It can flow from femoral veins to pelvic veins and join the single ventral abdominal vein, which travels cranially. The ventral abdominal vein is joined by the hepatic portal vein, and both enter the liver. Alternatively, flow from the hindlimbs can enter the external iliac veins, which flow into the renal portal veins, and then blood either enters the kidneys and leaves through the postcava to the sinus venous, or it continues cranially to the posterior cardinal veins where flow from the subclavian arteries and the external and internal jugular veins flow into the sinus venosus.5
Reptilian Circulation
The reptilian heart tends to be positioned roughly along the axial midline. In chelonians, the shoulder joints and in radiographs the girdles provide good landmarks; the heart is typically just caudal to the level of the acromion processes and cranial to the distal procoracoid process-procoracoid cartilage junctions. Part of the heart is often dorsal to margins of the humeral-pectoral scutes; however, in some species, it is positioned more posteriorly, along the midline between humeral-pectoral and pectoral-abdominal scutes lines.10 In soft-shelled turtles (Trionychidae), the heart is displaced to the right.6
In lizards, the heart position can be almost in the gular regions (geckos of the genus Hemidactylus and bearded dragons, Pogona vitticeps) or more caudally within the rib cage (chamaeleonine, iguanine, and varanid lizards). In adult or large, immature iguanid and varanid lizards, the heart is located more caudally in the thorax; the caudal aspect of the ventricle is aligned with the level of elbow when the forelimbs are held retracted against the body. The heart may virtually fill much of the thoracic cavity in young lizards, especially Pogona vitticeps.
In snakes, the heart generally is located at a position that is 22–33% of the snout-vent length (15–25% of total length), caudal to the rostrum. However, the heart is often shifted caudally in totally aquatic snakes, to a position that is 25–45% of total length posterior to the rostrum.6-8
Reptilian cardiovascular anatomy varies with taxon. Typically, reptilian hearts are described by major structural patterns of organization and within taxonomic contexts. Because chambers of non-crocodilian ventricle normally are not morphologically partitioned into systemic and pulmonary circuits, structures are frequently described functionally by the relative condition of blood’s oxygenation (high- or low-oxygen blood).
The heart is located within the pericardium. The pericardial sac typically contains clear pericardial fluid that, at least in turtles, is rich in calcium and magnesium ions. The alkaline pericardial fluid that bathes the heart may play a minor role in protection from acidosis during apnea.9 The caudal aspect of the pericardium and apex of the ventricle are attached to the visceral peritoneum by a cord-like ligament, the gubernaculum cordis. This structure is present in most chelonians, most lizards, tuataras, and crocodilians.6,10 When present, the structure anchors the ventricle so that longitudinal tension develops during contraction; this tension is one possible mechanism by which the muscular walls and ridges may functionally divide the otherwise incompletely divided ventricle during contraction, rather than retracting the ventricle craniad.6 The gubernaculum cordis is not present in snakes or varanid lizards.6
The reptilian heart is more complex than its exterior suggests. The heart is composed of five or six functional chambers and compartments (blood flows into sinus venosus, right atria, and the compartments of the ventricle; then it either leaves through the pulmonary trunk to the lungs and via the paired aortae or during apnea, pulmonary flow is restricted and blood is routed to the system via the two aortae. Flow returning from lungs via the pulmonary vein enters the left atrium, which then leads to the ventricular compartment. There are three basic patterns of reptilian ventricular structure; most squamates (lizards and snakes), chelonians, and rhynchocephalians (tuataras) share one form. Varanid lizards and pythons show variants that are partially divided or functionally divided; that may be viewed as a second pattern. These two patterns are those in which the ventricle has three compartments that are incompletely separated from one another: cavum venosum, cavum pulmonale, and cavum arteriosum.5,6,9-11 A third pattern of a fully divided ventricle characterizes crocodilians.5,9,12 More recent comparative anatomic work illustrates the details of the cardiac muscle organization, valves, and functional implications in squamates, and a variety of lower to higher vertebrates with particular emphasis on reptiles.13-15
The first chamber receiving blood from the system in all reptiles is the sinus venosus—a thin sac-like structure that is often ignored when chambers are described and counted.11 It can be a large chamber, although it is usually smaller than the combined volume of the atria and ventricle in amphibians, chelonians, and squamates; it is more compact in crocodilians. The sinus venosus is located dorsal to the atria and ventricle.6 The walls are formed of cardiac muscle and connective tissues. Venous blood from the body drains into the sinus venosus from four major veins: the left precava (left superior vena cava), the right precava (superior vena cava), the left hepatic vein, and the postcava (posterior vena cava). It is connected to the muscular right atrium via a sinoatrial aperture. The sinus venosus is undivided in chelonians and tuataras; a partial septum divides it in squamates and in crocodilians.10,13
As in the amphibian, the major aortic vessels are derivatives of the aortic arches. There is some asymmetry in that the pulmonary trunk arises from a single vessel that bifurcates to form the left and right pulmonary arteries. Grossly, it arises alongside the right and left systemic arch from the ventricle. The right aorta gives rise to the carotid arteries as well as branches supplying the body. The left aorta supplies the viscera. The subclavian arteries may arise from the left and right aorta or from dorsal aorta.5,10,16-18,20
Venous flow in turtles and lizards is similar to that described for amphibians; however, chelonians have paired abdominal veins, and squamates have a single abdominal vein in most cases. In crocodilians, flow from the hindlimbs often enters the caudal vein or renal portal veins sufficiently caudal to the lateral abdominal veins that flow to the renal postal system may predominate over bypass flow.20
Venipuncture Sites
Venipuncture sites in both classes are diverse. Each has its benefits, risks, and biases. In anurans, maxillary (facial), femoral, subclavian, and abdominal veins, as well as cardiac puncture are used; the proximal caudal vein is available in salamanders. Reptilian venipuncture sites include proximal caudal, external jugular, subcarapacial, and brachial veins. Subocular sinus and palatal veins are options in some snakes and lizards, as is cardiac puncture. Consideration of sites selected may reflect potential for differing hematological results, potential for skin discoloration, and risk of accidental puncture of spinal canal. The audience will be requested to discuss their preferred and least favored venipuncture sites.
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Additional references are available from the author (jwyneken@fau.edu).