Linköping University | Department of Physics, Chemistry and Biology

Bachelor thesis, 16 hp | Educational Program: Biology

Spring 2023 | LITH-IFM-G-EX—23/4319--SE

The functional anatomy of the

crocodilian heart

Jennifer Karlsson

Examiner, Rie Henriksen

Supervisor, Jordi Altimiras
Table of contents
1. Abstract and keywords ........................................................................................................................ 1
2. Introduction ......................................................................................................................................... 1
3. Methods .............................................................................................................................................. 2
3.1. Laboratory work ............................................................................................................................... 2
3.2. Data collection .................................................................................................................................. 3
4. The anatomy of the crocodilian heart ................................................................................................. 3
4.1. Special anatomical features ............................................................................................................. 6
4.1.1 The right and the ‘extra’ left aorta ................................................................................................. 7
4.1.2. The foramen of Panizza ................................................................................................................. 7
4.1.3. The cog-teeth-like valves............................................................................................................... 8
5. Hemodynamics .................................................................................................................................... 8
5.1. Non-shunting conditions .................................................................................................................. 8
5.2. Shunting conditions ........................................................................................................................ 10
6. The functional role of the circulatory patterns found in crocodiles ................................................. 12
7. Conclusions ........................................................................................................................................ 14
8. Societal and ethical considerations ................................................................................................... 14
9. Acknowledgements ........................................................................................................................... 15
10. References ....................................................................................................................................... 16
1 Abstract and keywords
Crocodiles are ectothermic, intermittent breathing reptiles with low metabolic rates.
Additionally, they are diving animals that can stay submerged for long periods, which poses
special demands on their cardiovascular system. The crocodilian heart is four-chambered with
completely separated ventricles, making it unique among other reptiles. It has special
anatomical structures that give it the capability to shunt blood away from the lungs, which
results in mixing of deoxygenated and oxygenated blood. The purpose of this study was to
morphologically describe the heart and review its functions and the significance of its
circulatory patterns. Dissection of two crocodilian hearts was performed for morphological
characterization of the heart, including the special features that contribute to the shunting: the
left aorta, the foramen of Panizza and the cog-teeth-like valves. Obstruction of the pulmonary
outflow tract by the cog-teeth-like valves decreases pulmonary blood flow and generates an
increased right ventricular pressure, diverting venous blood into the ‘extra’ left aorta and the
systemic circulation. Thus, during shunting conditions, venous blood from the left aorta and
arterial blood from the right aorta is mixed. The functional significance of this shunting pattern
has been extensively discussed and several hypotheses have been proposed. A recent study
showed that the absence of the right-to-left shunt does not affect the diving physiology of
crocodiles negatively, but it did result in cardiac hypertrophy, indicating that the shunt might
have a significance for the circulation and physiology of extant crocodiles.
Keywords: Anatomy, Cardiac right-to-left shunt, Cog-teeth-like valves, Crocodilian heart,
Foramen of Panizza, Hemodynamics, Left aorta.
2 Introduction
The maintenance of oxygen (O2) homeostasis is essential for survival of most metazoans. A
constant supply of O2 must be delivered to all cells throughout the body in order for the
organism to meet its metabolic demands (Baik & Jain, 2020). Animals have developed different
solutions to cope with this necessity and one solution is the circulatory system (Stephenson et
al., 2017). The heart is a very important part of this system, and its primary role is to pump
blood consisting of respiratory gases and other nutrients to the lungs and the rest of the body
(Stephenson et al., 2017). The transport of blood between the heart and the lungs is called the
pulmonary circulation whereas the systemic circulation transports blood between the heart and
all other tissues in the body (Noordergraaf, 2012).
The anatomical organization of the heart varies depending on the animal group. Birds and
mammals, which are endothermic animals, have a four-chambered heart with two atria and two
ventricles (Wang, 2018). They do not rely on the environment to maintain their temperature,
instead they must produce their own heat, which poses high metabolic demands (Bennett &
Ruben, 1979). The metabolic rates of mammals and birds are therefore much higher than in
ectothermic animals (Bennett & Ruben, 1979), and having a four-chambered heart is an
evolutionary adaptation for this (Wang, 2018). It enables these animals to separate between
their oxygenated and deoxygenated blood, which ensures that the tissues and muscles receive
fully oxygenated blood (Wang, 2018). Conversely, the ectothermic non-crocodilian reptiles,
lizards, snakes, and turtles, have a three-chambered heart (Wang, 2018). Their heart consists of
two atria and one ventricle which is incompletely divided, making it possible for oxygenated
and deoxygenated blood to mix (White, 1968).
Crocodiles are an exception from other reptiles, while these animals are clearly ectothermic and
intermittent breathers, they possess a four-chambered heart like birds and mammals (Seymour

1
et al., 2004). Researchers have hypothesized that the ancestors of extant alligators and
crocodiles may have been active, land-living, endothermic animals that required a four-
chambered heart for separation between the systemic and pulmonary systems (Seymour et al.,
2004). The ancestors later evolved back to ectothermy when they acquired a fully aquatic
lifestyle as ambush predators, but retained the typical heart of endotherms with four chambers
(Seymour et al., 2004). However, structures that permit mixing of venous and arterial blood are
also present in the heart of extant crocodiles (White, 1968). These unique structural features are
the left aorta, the foramen of Panizza, the anastomosis and the cog-teeth-like valves (Axelsson
et al., 1996). The structures account for a shunting system that allows deoxygenated blood to
bypass the lungs and to be re-circulated in the systemic circulation (Franklin & Axelsson, 2000).
As the crocodilian ancestors adopted to the aquatic environment and employed the
characteristic of sit-and-wait predators with long dive-times, they may have benefited from this
shunting mechanism, also called a right-to-left shunt (Seymour et al., 2004).
The aim of this thesis is to morphologically describe the crocodilian heart and review its
function and the significance of its circulatory patterns. Two crocodilian hearts are examined
for anatomical characterization, with the support of earlier published literature. Particular
attention is given to three out of the four anatomical features that contribute to the shunting
mechanism of crocodiles: (1) the left aorta, (2) the foramen of Panizza, and (3) the cog-teeth-
like valves. The fourth structure, (4) the anastomosis, will be mentioned but not evaluated
further since it was not present in the material, I had available. Published research in this field
indicates that the morphology and hemodynamics are similar in both the orders Alligatoridae
and Crocodylidae (Axelsson & Franklin, 1997).
3 Methods
This thesis was a combination of a practical study and a literature review from publications in
scientific journals. Firstly, literature reviews were collected to get an overview of the subject.
Thereafter, laboratory work was interspersed with documentation and reading research articles
relevant to the topic.
3.1 Laboratory work
Two crocodilian hearts were examined, one heart from a Dwarf caiman (Paleosuchus
palpebrosus) and one heart from a Cuban crocodile (Crocodylus rhombifer). The Dwarf caiman
was a male with a body weight of 5 kg, with an unknown age. It was confiscated by
Västmanlands county administration. The Cuban crocodile had an unknown gender and
weighed 950 g. The crocodile hatched at Skansen aquarium on the 21st of August 2021. Both
animals were euthanized due to health concerns and their hearts were given for educational
purpose for this project.
On arrival to our lab, the hearts were stored in formalin. They were washed with a saline
solution for 24 h to remove excess formalin. The exchange was performed under a hood due to
the toxicity of formalin. Thereafter, the hearts were transferred into ethanol and were stored in
it during the whole project. The hearts were dissected to reveal relevant structures. Scalpels and
scissors were used, and photographs were taken with a phone camera. Occasionally, a stereo
microscope (Zeiss Stemi DV4) with a magnification of 8x-32x was used to identify the
structures and to generate better pictures.

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3.2 Data collection
The study was based on research articles that were collected from different databases such as
Google scholar, Science Direct, Elsevier, PubMed and JSTOR. Primary research articles from
peer-reviewed scientific journals were mainly used to ensure a high-quality standard and correct
information. The articles were also selected based on their abstract and key words to know that
they were relevant for the project. Search terms used to find the articles: crocodilian heart,
anatomy, circulatory system, right-to-left shunt, foramen of Panizza, left aorta, active valves,
hemodynamics, diving, apnea, evolution.
4 Main text
4.1 The anatomy of the crocodilian heart
Crocodiles have a heart with four separate chambers, two atria and two ventricles, as illustrated
in Figure 1 (White, 1956). The atria are situated on top of the ventricles and are separated by
an interatrial septum (Webb, 1979). I could observe in the hearts of the Cuban crocodile
(Crocodylus rhombifer) and Cuvier’s dwarf caiman (Paleosuchus palpebrosus), that the right
and the left atria are located on top of the corresponding right and left ventricles (Figure 2 and
3). The right atrium stretches from the ventral to the dorsal side on the heart of P. palpebrosus,
and the left atrium is situated entirely on the dorsal side. As shown in Figure 2, both atria of C.
rhombifer can be observed from the ventral as well as the dorsal side of the heart. The atria are
partly separated from the ventricles by the atrioventricular valves that can open and close in
response to different blood pressures (White, 1956). Each valve is bicuspid, meaning that it
consists of two cusps/flaps of connective tissue (Cook et al., 2017). The ventricles of crocodiles
are described by White (1956) to be completely separated by an interventricular septum,
dividing them into two separate chambers. The complete separation of these chambers makes
the hearts of crocodiles unique from other reptilian hearts, since other reptiles only have one
ventricular chamber which is incompletely divided (White, 1968). Furthermore, Burggren
(1987) pointed out that the left ventricle in crocodiles and alligators is thick-walled and larger
in size relative to the thinner-walled right ventricle, which was also observed in the examined
hearts.

Figure 1. A schematic illustration of the crocodilian heart and outflow tracts. CCA, common carotid artery; CoA,
coeliac artery; DA, dorsal aorta; LAo, left aorta; LV, left ventricle; LPA, left pulmonary artery; Rao, right aorta;
RV, right ventricle; RPA, right pulmonary artery; RS, right subclavian artery. Reused with permission from the
Journal of Experimental Biology (From Axelsson et al., 1996).

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 Figure 2. The heart of Cuvier’s dwarf caiman (Paleosuchus
palpebrosus). A, Ventral view. B, Dorsal view. LA, left atrium; PA,
pulmonary artery; RA, right atrium; red asterisks, sinus venosus.

Figure 3. The heart of the Cuban crocodile (Crocodylus rhombifer).

A, Ventral view. B, Dorsal view. PV, pulmonary vein.

The left and right pulmonary veins enter the left atrium anterodorsally in a common vessel
(Webb, 1979), identified in C. rhombifer (Figure 2B). Webb (1979) distinguished that these
veins merge dorsal to the interatrial septum and ventral to the left precaval vein in Crocodylus
porosus, and that there are no valves between the pulmonary vein and the atrium. He also
described that a structure called the sinus venosus is attached to the dorsal surface of the right
atrium, which is the confluence of the left and right precaval veins and the postcaval vein. As
can be seen in Figure 2B and 3B, I was able to observe the sinus venosus in both P. palpebrosus
and C. rhombifer during the examination.
Superior of the right ventricle arise both the pulmonary artery and the ‘extra’ left aorta (White,
1956) (Figure 4C and 5C). The position of the pulmonary artery is on the left side of the left
aorta (Figure 4B), and shortly after its emergence it branches into the right and left pulmonary
arteries that run to each lung (Figure 4C and 5C), corresponding with the described anatomy by
Axelsson et al. (1989). The right aortic arch emerges from the left ventricle and is described to
cross the left aortic arch at their base (Goodrich, 1916), therefore positioned on the right side
of the left aorta (Figure 4B and C). The right aortic arch is larger in size relative to the left aortic
arch in both species (Figure 5D). The asymmetry between the two systemic arches has been
pointed out earlier by Grigg (1992) and Webb (1979) as well. Furthermore, the right aortic trunk
branches into the right subclavian artery, the common carotid artery and the right aorta
(Axelsson et al., 1989), also distinguished in C. rhombifer (Figure 5C). Additionally, I observed
that the right and left aorta emerge from the heart tightly together with the pulmonary artery, as
one unit (Figure 4C and 5C). Webb (1979) wrote that the vessels are bound within a thick
connective tissue sheath in the heart of C. porosus and White (1956) described their emergence
from the heart of Caiman sclerops as “a great bulbous swelling”. The vessels are separated from

4
each other at some distance from the heart and as can be observed in Figure 6, both the right
and left aorta continue dorsally alongside the right and left lung (Axelsson et al., 1989).

Figure 4. The heart of P. palpebrosus. A, Side view of right atrium and ventricle. The dorsal side to the
left and the ventral side to the right. B, Side view of the left atrium, ventricle and the three major
arteries. The ventral side is to the left and the dorsal side to the right. C, Cranial view of the major
arteries. The ventral side is on the bottom and the dorsal side on the top.

Figure 5. The heart of C. rhombifer with the same orientations as in Figure 4. A, Side view of right atrium and
ventricle. B, Side view of the left atrium and ventricle. C, Cranial view of the major arteries. D, Closer section of
the major arteries in a cranial view.

Figure 6. Dorsal view of the lungs of C. rhombifer, with the right and
left aortas running alongside each lung.

The ostium of the right and left aorta and the pulmonary artery are guarded by semilunar valves
(White, 1956), which are typical of all vertebrate hearts (Axelsson et al., 1996). These valves
are also bicuspid like the atrioventricular valves (Grigg, 1992) and each flap is called the lateral
and medial cusp (Webb 1979), illustrated in Figure 7. The semilunar valves of the pulmonary
artery in C. rhombifer can be seen in Figure 8. Moreover, White (1956) wrote that the medial
cusp in Alligator mississippiensis is approximately three times larger than the lateral cusp. Webb
(1979) also confirmed this and added that the medial cusp in the right systemic artery of C.
porosus is larger than the one in the left aorta. Two other structures that were described by White
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(1956) to be closely connected with the aortic valves and which he emphasized to be important
for the circulatory dynamics of the crocodilian heart, are the cardiac cartilages. The presence of
these cartilages had been noted earlier by several scientist from a histological standpoint, where
the cartilage was found to be composed of hyalin (White, 1956). White (1956) designated them
the central and the right ventrolateral cartilage. The main body of the central cartilage is located
at the base of the left aortic arch and the role of this structure seems to be to provide rigidity to
the lateral cusp of the left aortic arch, constitute an attachment point for parts of the
interventricular septum and stabilize the foramen of Panizza (White, 1956). The right
ventrolateral cartilage is situated in the ventral base of the right ventricle and gives rigidity to
the medial valve of the left aortic arch and provides an attachment point for the right
atrioventricular valves (White, 1956).

Figure 7. Illustration of the bicuspid semilunar valves in the aortic arches, and the foramen of
Panizza embedded in between. The valves of the pulmonary artery are not shown. Copyright © (2023)
Wiley. Used with permission from (Webb, Comparative cardiac anatomy of the reptilia. III. The heart
of crocodilians and a hypothesis on the completion of the interventricular septum of crocodilians and
birds , The Journal of Morphology, John Wiley & Sons, In).

Figure 8. Cranial view of the right aorta (bottom left), the left aorta (bottom right)
and the pulmonary artery (top) showing its bicuspid valves, in C. rhombifer.

4.2 Special anatomical features

As mentioned previously, there are several special anatomical features that makes the heart of
crocodiles capable of mixing arterial and venous blood by a shunting mechanism (White, 1968).
Three of these structures are present in the crocodilian heart: the left aorta, the foramen of
Panizza and the cog-teeth like valves, whereas the anastomosis is situated outside the heart,
below its apex (Axelsson et al., 1996).

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4.2.1 The right and the ‘extra’ left aorta
An aorta is the main artery that supplies blood to the circulatory system, and in contrast to
mammals and birds which only have one aorta, crocodiles have two (White, 1956). As
mentioned earlier, they have both a right and a left aorta, and the former is the dominant
systemic artery with brachiocephalic distribution (blood supply to the upper body through the
common carotid artery and the right subclavian artery), whereas the latter is the ‘extra’ aorta
that contributes to the shunting mechanism of the heart (Greenfield & Morrow, 1961). Axelsson
et al. (1989) described that both the right and left aorta continues posteriorly to the abdominal
region of the crocodile, where they communicate through an anastomosis (Figure 1). This
structure was removed from the dissected hearts before they arrived at the laboratory, therefore
I was not able to observe the anastomosis in P. palpebrosus nor C. rhombifer. Nevertheless, it
has been described that downstream the anastomosis, the right aorta becomes the dorsal aorta,
and the left aorta becomes the coeliac artery, supplying the gastrointestinal tract (Axelsson et
al., 1989). Greenfield and Morrow (1961) wrote that the early research regarding the physiology
of crocodiles was based solely on anatomy, and as explained, the left aorta arises from the right
ventricle. Thus, it was early concluded that the left aorta receives right ventricular venous blood
during systole (Goodrich, 1916, 1919). However, further research has found that this is not the
main occurrence, it appears that the left and right aorta are supplied by a common pump during
normal air breathing, the left ventricle (Axelsson et al., 1989, 1996; Greenfield & Morrow,
1961; Grigg & Johansen, 1987; White, 1956, 1968, 1969).
4.2.2. The foramen of Panizza
In addition to the anastomosis in the gut, the right and left aorta are also in communication
through a passage called the foramen of Panizza (Panizza, 1833). It is situated in the common
wall between the right and left aorta, at the base of their arches, as illustrated in Figure 1
(Greenfield & Morrow, 1961). Additionally, Webb (1979) described that the foramen of Panizza
is located within the medial cusps of the right and left aorta (Figure 7). The diameter of this
opening has been estimated to be approximately 35-40% of the size of the right aorta (Axelsson
et al., 1996), since it is located deep down the arches it was only possible to display its presence
by pulling a thread through it, from the right to the left aorta (Figure 9). This structure provides
an alternative route for blood ejected into the right systemic artery, allowing it to pass over to
the left systemic artery during non-shunting conditions (Axelsson et al., 1989).

Figure 9. Cranial view. Thread through the foramen of Panizza in C. rhombifer.

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4.2.3. The cog-teeth-like valves
In addition to the semilunar valves that are present between the right ventricle and the
pulmonary artery, there are other types of valves located underneath them, called cog-teeth-like
valves (Figure 1) (Axelsson et al., 1996). These valves were firstly described by Greenfield and
Morrow (1961) as “rigid, serrated cartilaginous bars which project into the outflow tract” of the
pulmonary artery in A. mississippiensis. They speculated that the cog-teeth-like valves may
have a role in the distribution of right ventricular output. Webb (1979) found similar structures
in the heart of C. porosus and wrote that they were connective tissue outpushings that
histologically was found to be collagen fibers, and that fit together like the teeth of opposing
cogs. He also stated that the ostium of the pulmonary artery is almost entirely obstructed by the
outpushings and appear to be involved in the mechanical closure of the pulmonary artery. These
valves were identified in both C. rhombifer and P. palpebrosus (Figure 10), inferior to the
bicuspid semilunar valves in the arch of the pulmonary artery, as described by Webb (1979).

Figure 10. Cog-teeth-like valves. A, Section through the ventral side of the pulmonary artery
exposing the opposing outpushings. B, Cranial view of the cog-teeth-like valves in P. palpebrosus. C,
Cranial view of the cog-teeth-like valves in C. rhombifer.

4.3. Hemodynamics
Since the ventricles are completely separated by an interventricular septum, crocodiles are able
to separate between their systemic and pulmonary circuits (White, 1968). Thus, they are capable
of having different pressures in the two circuits during lung ventilation, as birds and mammals
(Burggren, 1987). As already pointed out, crocodiles can induce a pulmonary bypass shunt
where venous blood in the right side of the heart is diverted into the systemic circuit, resulting
in mixing of deoxygenated and oxygenated blood (White, 1968). This phenomenon gives
crocodiles the capability to match the blood flow to the lungs with the alveolar gas flow without
affecting the systemic circulation (Axelsson et al., 1996). The right-to-left shunt has often been
found to operate when crocodiles dive and hold their breath, whereas the non-shunting flow
pattern occurs the majority of time during normal breathing (Axelsson et al., 1989; Grigg &
Johansen, 1987; White, 1969).
4.3.1 Non-shunting conditions
Early research based on anatomy proposed that the left aorta would receive deoxygenated blood
since it originates from the right ventricle (Goodrich, 1919). Further research based on
physiological observations has revised that early interpretation. White (1956) measured blood-
oxygen contents in anesthetized C. sclerops and found that the O2 contents in the right and left
aortic arch and left atrium had high oxygen levels, whereas the levels in the pulmonary artery
and right atrium were low. The data indicated filling of the left aorta from the right aorta through

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the foramen of Panizza (White, 1956). This has also been confirmed in A. mississippiensis
(Greenfield & Morrow, 1961; White, 1969), C. porosus, Crocodylus johnstoni (Grigg &
Johansen, 1987) and in C. sclerops by Axelsson et al. (1989) as well. Nevertheless, the early
interpretations that the left aorta would receive blood from the right ventricle is not rejected,
since it occurs during shunting conditions (Axelsson et al., 1996; Franklin & Axelsson, 2000;
Shelton & Jones, 1991; White, 1969).
The crocodilian heart is functionally similar to the avian or mammalian heart during non-
shunting conditions (Axelsson et al., 1996). The right atrium receives deoxygenated blood from
the caval veins merging into sinus venosus (White, 1968). The blood then flows to the right
ventricle and gets ejected into the pulmonary trunk, which divides into the right and left
pulmonary arteries (Axelsson et al., 1996). The pulmonary arteries transport the venous blood
to the lungs, where it gets oxygenated (White, 1968). In order for venous blood to be ejected
into the left aorta, the left aortic semilunar valves must open (White, 1968). It occurs when the
pressure generated in the right ventricle exceeds the pressure in the left aortic arch (White,
1968). As can be observed in Figure 11, the pressure developed in the right ventricle during
normal breathing is lower than the pressure in the left aorta, therefore insufficient to open the
valves. The oxygenated blood from the lungs returns to the left atrium through the pulmonary
vein and then flows into the left ventricle (Greenfield & Morrow, 1961). It is ejected into the
right aorta and its branches, the common carotid artery and the subclavian arteries (Greenfield
& Morrow, 1961). Additionally, during left ventricular diastole when the cusp of the semilunar
valve is closed, the blood flows through the foramen of Panizza into the left aorta (Greenfield
& Morrow, 1961; Grigg & Johansen, 1987). The reason it occurs during diastole is that the
medial cusp of the right aortic valve covers the foramen of Panizza when it is in an opened state
under left ventricular systole, resulting in obstruction of flow through the foramen (Greenfield
& Morrow, 1961). Axelsson et al. (1996) confirmed this by using an angioscope to photograph
the right aortic valves and the foramen of Panizza at four different stages during the cardiac
cycle. They found that the medial cusp of the right aortic valve completely covered the foramen
of Panizza during systole but allowed free flow through it during diastole.

Figure 11. Pressure recordings from the heart and outflow tracts of C. porosus during non-shunting condition.
Used with permission from SNCSC (Grigg and Johansen, Cardiovascular dynamics in Crocodylus porosus
breathing air during voluntary aerobic dives, Journal of Comparative Physiology B: Biochemical, Systemic,
and Environmental Physiology, Springer Nature).

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Figure 11 shows the pressure tracings from the heart of a supine crocodile measured by Grigg
and Johansen (1987). There is a similarity in early systolic and in diastolic pressure between
the left and right aorta but at midsystole there is asynchrony. The initial small pressure rise in
the left aorta has been under discussion. During this part of the cycle, it has been measured that
there is no flow in the left aorta (Axelsson et al., 1989, 1996) which agrees with the foramen
being closed by the semilunar valve. It was suggested that the initial pressure could be a
transmural effect, which implies that the expanding right aorta is squeezing the left aorta, since
the outflow vessels are located together within a sheath of connective tissue (Axelsson et al.,
1989; Grigg & Johansen, 1987; Webb, 1979). Jones and Shelton (1993) also found that
occlusion of the anastomosis affected a part of the initial systolic pressure increase in the left
aorta, indicating that the anastomosis also contributes to the early systolic increase in this artery.
Additionally, Axelsson et al. (1996) observed that there is a small flow through the foramen
before the right aortic valves are fully open, which also could explain the initial pressure
increase. Later on Axelsson et al. (1997) measured the flow in the anastomosis and
demonstrated that there is flow from the right aorta into the left aorta via the anastomosis during
systole. They concluded that the small flow observed during early systole by Axelsson et al.
(1996) was unlikely to solely account for the initial pressure increase in the left aorta and that
it must be a combination of the small flow through the foramen, the transmural effect, and the
flow through the anastomosis (Axelsson et al., 1997). As previously described, the left aorta
becomes the coeliac artery supplying the gut (Axelsson et al., 1989). However, the flow through
the foramen during non-shunting conditions has been stated to be inadequate to support the
function of the gastrointestinal tract (Axelsson et al., 1996; Shelton & Jones, 1991). Instead, the
anastomosis between the right and left aorta allows the blood from the right aorta to support
this region (Axelsson et al., 1989). The small blood flow in the left aorta during non-shunting
conditions seems to be required to prevent blood clotting in the vessel (Shelton & Jones, 1991).
The second steep increase in left aortic pressure is called the foramen spike and occurs during
left ventricular diastole, when the foramen gets uncovered from the valve (Grigg & Johansen,
1987). The left and right aortic pressures are equal from that point and throughout diastole,
indicating free communication between the two aortas (Grigg & Johansen, 1987). This pattern
has also been described by Greenfield and Morrow (1961) as well as Axelsson et al. (1989).
There is also an evident pressure difference between the right aorta and the pulmonary artery
(Figure 11), which probably results from a constriction at the base of the pulmonary outflow
tract (Grigg & Johansen, 1987; White, 1969). After peak pressure is reached in the pulmonary
artery, there is a second peak on the right ventricular pressure trace, which is the result of the
cog-teeth-like valves that appose each other, which cause an obstruction (Axelsson et al., 1996;
Greenfield & Morrow, 1961; White, 1969).
4.3.2 Shunting conditions
Greenfield and Morrow (1961) speculated that right ventricular output may be distributed into
the left aorta when crocodiles dive and hold their breath. Since crocodiles can stay submerged
for almost an hour, the oxygen stores in their lungs will quickly be depleted if the pulmonary
blood flow remains the same as during normal breathing (Greenfield & Morrow, 1961). Thus,
Greenfield and Morrow (1961) hypothesized that during such circumstances, most of the right
ventricular output would be redistributed into left aorta. For this to occur, an increase in right
ventricular pressure would be necessary, otherwise the right aortic valves will not open
(Greenfield & Morrow, 1961). It has been confirmed to occur in A. mississippiensis when

10
forced to dive (White, 1969) and in C. porosus during voluntary aerobic dives (Grigg &
Johansen, 1987). White (1969) observed that the pressure gradient between the right ventricle
and the pulmonary artery increased when the crocodile was diving. The pressure developed in
the right ventricle eventually superimposed on the left aortic pressure and resulted in a right-to-
left shunt. The observations by White (1969) are similar to the traces shown in Figure 12,
measured by Grigg and Johansen (1987). As can be seen in the figure, there are three pulses in
the trace of the left aorta: the initial rise and the foramen spike as described in non-shunting
conditions, and the right ventricular surge in between.

Figure 12. Pressure recordings from the heart and outflow tracts of C. porosus during a right-to-left shunt. Used
with permission from SNCSC (Grigg and Johansen, Cardiovascular dynamics in Crocodylus porosus breathing
air during voluntary aerobic dives, Journal of Comparative Physiology B: Biochemical, Systemic, and
Environmental Physiology, Springer Nature).

Axelsson et al. (1996) studied the shunting mechanism in C. rhombifer by occluding the
pulmonary artery to induce a right-to-left shunt while observing the cog-teeth-like valves with
an angioscope. The valves were open during the early part of systole but as it progressed, the
outpushings converged and the diameter of the pulmonary outflow tract was clearly reduced by
the individual outpushings that fitted together. It was concluded that the initiation of a
pulmonary bypass shunt is due to the active cog-teeth-like valves and changes in resistance in
the pulmonary and/or systemic circuits (Axelsson et al., 1996). The cog-teeth-valves being
active rather than passive was suggested by Greenfield and Morrow (1961) and has been studied
in situ by Franklin and Axelsson (2000) in C. porosus. They perfused the heart with the β-
adrenergic antagonist sotalol which resulted in a large increase in resistance of the pulmonary
outflow tract and an initiation of a pulmonary bypass shunt. By injecting either the B-adrenergic
agonists adrenaline or isoprenaline the flow to the left aorta decreased, as the resistance in the
pulmonary trunk ceased. These results demonstrated that the cog-teeth-like valves are actively
regulated (Franklin & Axelsson, 2000). Additionally, there is research that has found that
acetylcholine can induce an increase in pulmonary resistance that leads to a cardiac right-to-left
shunt (Axelsson et al., 1989; Jones & Shelton, 1993; White, 1969). It seems likely that the
valves are of an active nature but the exact mechanism behind it would need further
investigation.

11
Another interesting observation by Axelsson et al. (1996) was that the medial cusp of the left
aortic valve did not cover the foramen of Panizza as the cusp of the right aortic valve does.
During the whole cardiac cycle there was a continuous reversed flow through the foramen, from
the left to the right aorta. The reversed flow has been speculated about earlier by Grigg (1992).
The finding by Axelsson et al. (1996) was significant because during a right-to-left cardiac
shunt, the perfusion of the systemic circuit is highly dependent on the right side of the heart,
while the flow from the left ventricle is reduced (Axelsson et al., 1996; White, 1969). Since the
common carotid artery and the subclavian arteries that supplies the brain and the upper body
originate from the left ventricle, they will not be perfused in the same extent as usually, but with
the reversed flow they could be supplied by the right ventricle instead. Additionally, regional
redistribution of blood during submergence, favoring flow to the heart and brain, occurs in most
diving vertebrates (Butler, 1988) and prolongs the time they can stay submerged (Axelsson et
al., 1996). This could also be the case for crocodiles since there are indications of selective
perfusion of their head during diving, the blood flow to the gut decreases more than the flow in
the carotid artery (Axelsson et al., 1991). Reversed foramen flow could be a possible
explanation (Axelsson et al., 1996).
4.4 The functional role of the circulatory patterns found in crocodiles
The functional significance of the shunting mechanism in crocodiles is not clearly established
but several hypotheses have been proposed. One hypothesis suggests that as apnea proceeds
when crocodiles are diving, and the oxygen partial pressure (PO2) in the lungs is decreasing
towards the venous levels in the pulmonary circuit, the continued lung perfusion “costs” more
than it gives (Burggren, 1987). Therefore, blood is not directed to the lungs if it cannot be
supplied with oxygen (Grigg & Johansen, 1987). By reducing the perfusion to the lungs, the
cardiac energy is preserved and the dive can be prolonged (Burggren, 1987). However,
Burggren (1987) wrote that shunting commonly starts quickly after lung ventilation has been
reduced. Thus, the PO2 in the lungs is still high and the metabolic costs of perfusing the lungs
is low relative to the benefit from it. It must also be emphasized that although perfusion of the
lungs decreases during a right-to-left shunt, it does not affect the O2 depletion from the lung O2
stores, which is the primary compartment for storing oxygen in reptiles (Hicks & Wang, 1996).
It should be noted that the majority of voluntary dives by crocodiles are within their aerobic
dive limit, meaning that crocodiles rely on their O2 stores and hardly use anerobic metabolism
(Wright, 1985). Thus, the subsequent explanations by Hicks and Wang (1996) are based on
dives and breath holding within the aerobic limits.
During apnea (in the absence of pulmonary bypass), the rate of depletion of the O2 stores (lungs
and blood) is dependent on the oxygen uptake of the tissues (Hicks & Wang, 1996). Primarily
the lung oxygen stores are utilized, provided that PO2 is high enough to saturate hemoglobin
(Hb) of the pulmonary venous blood (Hicks & Wang, 1996). When lung PO2 is reduced to the
levels in the pulmonary venous blood and not able to saturate the hemoglobin, the blood O2
stores are utilized as well (Hicks & Wang, 1996). This is also the case during a right-to-left-
shunt when held at a constant level, which is illustrated in Figure 13. It shows the pulmonary
venous (Cpv), systemic arterial (Ca) and mixed venous (Cv) oxygen content on an oxygen
dissociation curve, which is a graphical representation of the amount of O2 bound to Hb at
different PO2 in the blood (Hicks & Wang, 1996). At the right side of the figure, the systemic
(Qs) and pulmonary (Qp) blood flows are depicted. The oxygen uptake in the lungs (product of
Qp and (Ca-Cv) difference across the lung) and the systemic circuit (product of Qs and Ca-Cv

12
difference across the tissues) are presented as grey areas. During shunting conditions (Figure
13B) Ca is reduced, resulting in reduced Cv for a given Qs. Thus, the oxygen uptake at the
tissues remains constant even though it is at lower systemic O2 content levels. Furthermore, as
the pulmonary bypass reduces Cv, the blood returning to the lungs takes up even more O2.
Consequently, the oxygen uptake in the lungs remains constant, despite the lowered lung
perfusion (grey areas in A and B are identical) (Hicks & Wang, 1996).

Figure 13. Graphical illustration of the systemic oxygen transport and pulmonary oxygen uptake in the absence
(A) and presence (B) of right-to-left shunting. See text for extended explanation. Copyright © (2023) Wiley.
Used with permission from (Hicks and Wang, functional role of cardiac shunts in reptiles, The Journal of
Experimental Zoology Part A, John Wiley & Sons, In).

Another suggestion was proposed by Grigg and Johansen (1987) who thought that sequestration
of carbon dioxide (CO2) away from the lungs, which has been found to occur during shunting
conditions in turtles, will facilitate oxygen uptake due to the relative decrease in acidification
of the blood. This should therefore result in high O2 affinity of the pulmonary blood (Grigg &
Johansen, 1987). They also thought that it would enhance oxygen delivery and favor CO2
storage in the tissues by a right-shifted oxygen dissociation curve in the systemic circuit (Bohr
effect), since shunting results in retention of CO2 (Grigg & Johansen, 1987). Hicks and Wang
(1996) rejected this hypothesis and pointed out that the distribution of carbon dioxide between
different compartments is unaffected by a shunt. They explained that almost all CO2 produced
during apnea in all air-breathing vertebrates is not eliminated into the lungs, and that the tissues
and blood simply have a higher capacity to store it (Hicks & Wang, 1996). Hence, it is an
incorrect statement that right-to-left shunting would have significance on CO2 exchange during
breath holding (Hicks & Wang, 1996). Hicks and Wang also wrote that it is undoubtedly that a
right-shift of the oxygen equilibrium curve will occur due to the increase in tissue CO2, but that
one should remember that a right-to-left shunt also decreases arterial O2 levels. By observing
the changes in blood pH that occurs during breath holding, the magnitude of the right-shift is
not enough to outweigh the decrease in oxygen partial pressure and content in the arterial blood
due to shunting (Hicks & Wang, 1996).

13
There are even more suggestions as to why the special anatomical features that contribute to
the shunting pattern exists in crocodiles: that it reduces plasma filtration into the lungs,
facilitates warming, triggers hypometabolism and facilitates stomach acid secretion and
digestion, but strong evidence is lacking (Hicks, 2002). Could it be as Webb (1979) suggested,
that the anatomy gives the capacity for shunting, but the need for it is minimal in extant
crocodiles due to their behavior and physiology? That the structures are relics from their even
more aquatic ancestors? Hicks (2002) highlighted that there are many arguments based on a
belief that most traits are adaptive. It is important to find strong evidence that the physiological
performance and/or reproductive fitness is reduced by the absence of cardiac shunting, to
consider it as an adaptive feature (Hicks, 2002). A recent study performed on A. mississippiensis
tested the hypotheses that removal of the shunting mechanism would result in cardiac
remodeling and negatively affect the diving performance (Eme et al., 2009). They investigated
the effects of both acute (minutes to hours) and chronic (months) removal of the shunt by
surgically occluding the left aorta (Eme et al., 2009). The occlusion of the left aorta did not
affect the metabolism or the respiratory patterns of the alligators and Eme et al. (2009)
concluded that the right-to-left shunt is not an adaptive trait derived to support an aquatic
lifestyle. If the shunt was important for diving, the sham/’control’ animals should have
demonstrated a lower metabolic rate, a higher number of voluntary apneas with longer duration
and a greater average length of the apneas, which they did not (Eme et al., 2009). Eme et al.
suggested that it is an ancestral feature that does not affect the diving physiology of extant
reptiles (Eme et al., 2009). An important note is that they did hypothesize that there would be
cardiac remodeling in response to the absence of the shunt (Eme et al., 2009), since a common
response to increased afterload and preload in mammals is an increase in ventricular mass (Hill
& Olson, 2008). The results from the study by Eme et al. (2009) did show a doubling of right
ventricular pressure and a significant enlargement of the ventricles. Therefore, one could say
that the absence of the shunt does affect the physiology of crocodiles since they need to remodel
their heart to cope with the increased intraventricular pressure. Additionally, cardiac
hypertrophy can negatively affect the physiology since it does increase the risk of heart failure
and malignant arrythmias (Hill & Olson, 2008). It appears to me that the shunt does have a
significance for the circulation and physiology of extant crocodiles, but whether it is important
for their diving physiology remains unsaid.
5 Conclusions
This thesis has reviewed the anatomy of the crocodilian heart, its function and the functional
role of the special pattern found in the circulatory physiology of crocodiles. The heart is four-
chambered with a complete separation of its pulmonary and systemic circulation, making it
capable of producing different pressures in the two circuits. It has four special anatomical
features which are the foramen of Panizza, the left aorta, the anastomosis, and the cog-teeth-
like valves. These morphological traits make the heart capable of mixing pulmonary venous
blood with the systemic arterial blood by a right-to-left shunting mechanism. Venous blood
should be transported to the lungs but is instead diverted into the ‘extra’ left aorta that arises
from the right ventricle. This results in mixing venous blood with the arterial blood flowing
through the right aorta, in the systemic circulation. The cog-teeth-like valves situated in the
pulmonary outflow tract contribute to this pattern by active obstruction of the flow into the
pulmonary artery, which results in an increased right ventricular pressure, thus blood is ejected
into the left aorta. This pattern has been observed when crocodiles dive and hold their breath,
whereas the shunting is absent during normal breathing. However, blood is still distributed into
14
the left aorta during non-shunting conditions. This is achieved through the two communication
points between the right and left aorta: the foramen of Panizza and the anastomosis. Several
hypotheses have been suggested regarding the functional significance of the right-to-left
shunting mechanism. For example, the continued lung perfusion during diving would
metabolically “cost” more than it gives and the decreased blood flow to the lungs should save
cardiac energy. Another argument was that it would facilitate oxygen uptake for the pulmonary
venous blood by sequestering carbon dioxide away from the lungs and favor CO2 storage in the
tissues. However, there is no strong evidence for these hypotheses. Furthermore, the absence of
the shunting mechanism does not affect the diving physiology of crocodiles negatively since
neither the metabolism nor the respiratory rate are affected by it, indicating that it is not an
adaptive trait. However, removing the shunt does result in enlargement of the ventricles due to
an increased intraventricular pressure, which demonstrates that the right-to-left cardiac shunt
might have a significance for the circulation and physiology of extant crocodiles.
6 Societal and ethical considerations
By investigating the anatomy and physiology of the crocodilian heart, insights about how
another vertebrate circulatory system works are gained. This could give guidance in medicine,
since there are cardiac diseases that display similar patterns that are found in crocodiles. For
example, patients with left ventricular hypertrophic cardiomyopathy display the same biphasic
pressure development in the left ventricle and aorta, as in the right ventricle of crocodiles. This
is also observed in the right ventricle and pulmonary artery in humans diagnosed with
pulmonary stenosis (Axelsson et al., 1996). Thus, examination of other animals and their
physiology gives valuable information and opportunities for learning, which could contribute
to medical research. This would therefore contribute to achieving the third global goal “Good
health and well-being”. Additionally, it gives understandings of the evolution of crocodiles and
how their physiology has adapted to the environment they live in. Knowledge regarding animals
is important to be able to ensure preservation of existing species and biological diversity, which
contributes to achieve the 15th global goal “Life on land”.
Regarding the ethical aspects of this study, it should be borne in mind that the crocodiles were
euthanized due to health concerns and not for the conduction of this thesis. Therefore the
ethical dilemma can be considered mild. In addition, it contributes to education which, as
previously mentioned, can provide knowledge about these animals, thereby contributing to
conservation of the species. In the long run, it hopefully leads to something good.
7 Acknowledgements
I wish to thank my supervisor Jordi Altimiras for his guidance and support throughout the
project and Wilma Sohlén for our valuable discussions. Additionally, I am grateful to John
Wiley & Sons, Springer nature and The Company of Biologists for letting me reuse relevant
figures for this thesis.

15
8 References
Axelsson, M., & Franklin, C. E. (1997). From anatomy to angioscopy: 164 years of

crocodilian cardiovascular research, recent advances, and speculations. Comparative

Biochemistry and Physiology, 118, 51–62. https://doi.org/10.1016/S0300-

9629(96)00255-1

Axelsson, M., Franklin, C. E., Fritsche, R., Grigg, G. C., & Nilsson, S. (1997). The sub-

pulmonary conus and the arterial anastomosis as important sites of cardiovascular

regulation in the crocodile Crocodylus Porosus. Journal of Experimental Biology, 200,

807–814. https://doi.org/10.1242/jeb.200.4.807

Axelsson, M., Franklin, C. E., Löfman, C. O., Nilsson, S., & Grigg, G. C. (1996). Dynamic

anatomical study of cardiac shunting in crocodiles using high-resolution angioscopy.

Journal of Experimental Biology, 199(Pt 2), 359–365.

https://doi.org/10.1242/jeb.199.2.359

Axelsson, M., Fritsche, R., Holmgren, S., Grove, D. J., & Nilsson, S. (1991). Gut blood flow

in the estuarine crocodile, Crocodylus porosus. Acta Physiologica Scandinavica, 142,

509–516. https://doi.org/10.1111/j.1748-1716.1991.tb09187.x

Axelsson, M., Holm, S., & Nilsson, S. (1989). Flow dynamics of the crocodilian heart.

American Journal of Physiology, 4 Pt 2, R875–R879.

https://doi.org/10.1152/ajpregu.1989.256.4.R875

Baik, A. H., & Jain, I. H. (2020). Turning the oxygen dial: Balancing the highs and lows.

Trends in Cell Biology, 30, 516–536. https://doi.org/10.1016/j.tcb.2020.04.005

Bennett, A. F., & Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science, 206,

649–654. https://doi.org/10.1126/science.493968

Burggren, W. W. (1987). Form and function in reptilian circulations. American Zoologist, 27,

5–19.

16
Butler, P. J. (1988). The exercise response and the “classical” diving response during natural

submersion in birds and mammals. Canadian Journal of Zoology, 66, 29–39.

https://doi.org/10.1139/z88-004

Cook, A. C., Tran, V., Spicer, D. E., Rob, J. M. H., Sridharan, S., Taylor, A., Anderson, R. H.,

& Jensen, B. (2017). Sequential segmental analysis of the crocodilian heart. Journal of

Anatomy, 231, 484–499. https://doi.org/10.1111/joa.12661

Eme, J., Gwalthney, J., Blank, J. M., Owerkowicz, T., Barron, G., & Hicks, J. W. (2009).

Surgical removal of right-to-left cardiac shunt in the American alligator (Alligator

mississippiensis) causes ventricular enlargement but does not alter apnoea or

metabolism during diving. Journal of Experimental Biology, 212, 3553–3563.

https://doi.org/10.1242/jeb.034595

Franklin, C. E., & Axelsson, M. (2000). An actively controlled heart valve. Nature, 406, 847–

848. https://doi.org/10.1038/35022652

Goodrich, E. S. (1916). On the classification of the reptilia. Proceedings of the Royal Society

of London. Series B, Containing Papers of a Biological Character, 89, 261–276.

Goodrich, E. S. (1919). Note on the reptilian heart. Journal of Anatomy, 53, 298–304.

Greenfield, L. J., & Morrow, A. G. (1961). The cardiovascular hemodynamics of Crocodilia.

Journal of Surgical Research, 1, 97–103. https://doi.org/10.1016/S0022-

4804(61)80003-6

Grigg, G. (1992). Central cardiovascular anatomy and function in Crocodilia. In S. C. Wood,

R. E. Weber, A. R. Hargens, & R. W. Millard, Physiological Adaptations in

Vertebrates: Respiration, Circulation and Metabolism (pp. 339–354). Marcel Dekker.

Grigg, G., & Johansen, K. (1987). Cardiovascular dynamics in Crocodylus porosus breathing

air during voluntary aerobic dives. Journal of Comparative Physiology B, 157, 381–

392. https://doi.org/10.1007/BF00693365

17
Hicks, J. W. (2002). The physiological and evolutionary significance of cardiovascular

shunting patterns in reptiles. Physiology, 17, 241–245.

https://doi.org/10.1152/nips.01397.2002

Hicks, J. W., & Wang, T. (1996). Functional role of cardiac shunts in reptiles. Journal of

Experimental Zoology, 275, 204–216. https://doi.org/10.1002/(SICI)1097-

010X(19960601/15)275:2/3<204::AID-JEZ12>3.0.CO;2-J

Hill, J. A., & Olson, E. N. (2008). Cardiac Plasticity. New England Journal of Medicine, 358,

1370–1380. https://doi.org/10.1056/NEJMra072139

Jones, D. R., & Shelton, G. (1993). The physiology of the alligator heart: Left aortic flow

patterns and right-to-left shunts. Journal of Experimental Biology, 176, 247–270.

https://doi.org/10.1242/jeb.176.1.247

Noordergraaf, A. (2012). Circulatory system dynamics. Elsevier.

Panizza, B. (1833). Sulla struttura del cuore e sulla circolazione del sangue del Crocodilus

lucius. Biblioteca Italiana, 70, 87–91.

Seymour, R. S., Bennett‐Stamper, C. L., Johnston, S. D., Carrier, D. R., & Grigg, G. C.

(2004). Evidence for endothermic ancestors of crocodiles at the stem of Archosaur

evolution. Physiological and Biochemical Zoology: Ecological and Evolutionary

Approaches, 77, 1051–1067. https://doi.org/10.1086/422766

Shelton, G., & Jones, D. R. (1991). The physiology of the alligator heart: The cardiac cycle.

Journal of Experimental Biology, 158, 539–564. https://doi.org/10.1242/jeb.158.1.539

Stephenson, A., Adams, J. W., & Vaccarezza, M. (2017). The vertebrate heart: An

evolutionary perspective. Journal of Anatomy, 231, 787–797.

https://doi.org/10.1111/joa.12687

Wang, T. (2018). Evolution: The beat goes on. ELife, 7, e36882.

https://doi.org/10.7554/eLife.36882

18
Webb, G. J. W. (1979). Comparative cardiac anatomy of the reptilia. III. The heart of

crocodilians and an hypothesis on the completion of the interventricular septum of

crocodilians and birds. Journal of Morphology, 161, 221–240.

https://doi.org/10.1002/jmor.1051610209

White, F. N. (1956). Circulation in the reptilian heart (Caiman sclerops). The Anatomical

Record, 125, 417–431. https://doi.org/10.1002/ar.1091250302

White, F. N. (1968). Functional anatomy of the heart of reptiles. American Zoologist, 8, 211–

219. https://doi.org/10.1093/icb/8.2.211

White, F. N. (1969). Redistribution of cardiac output in the diving alligator. Copeia, 1969,

567–570. https://doi.org/10.2307/1441936

Wright, J. C. (1985). Diving and exercise physiology in the estuarine crocodile, Crocodylus

porosus [Ph.D Thesis]. In Diving and exercise physiology in the estuarine crocodile,

Crocodylus porosus. The University of Sidney.

19