JOURNAL OF MORPHOLOGY 234:37–50 (1997)

The Arterial System of the Sperm Whale

(Physeter macrocephalus)
V.V. MELNIKOV*
Pacific Oceanological Institute, Far East Branch of the Russian Academy
of Science, 690031 Vladivostok, Russia

ABSTRACT The angioarchitecture of the sperm whale is basically similar to

that of other mammals, but it has specific attributes associated with the
aquatic environment of this animal and its tolerance for deep and long diving.
Specialized features include an expansive aortic arch, unusually far anterior
localization of the arch, symmetrical branching of common carotid and subcla-
vian arteries from the aorta, the absence of direct connection between internal
carotid arteries and brain arteries, the absence of a costocervical artery, and
the presence of a well-developed occipital artery. The sperm whale has
extraordinarily well-developed retia mirabilia, distributed in the cranial
cavity, vertebral canal, neck and thoracic cavity, around the optic nerve, and
in the walls of the uterus. These retia are more extensively developed in the
sperm whale than in any other cetacean previously studied. J. Morphol.
234:37–50, 1997. r 1997 Wiley-Liss, Inc.

Although many morphological features of mens with material collected from adults
the circulatory system of cetaceans have been during the dissection of carcasses on deck.
reported by previous investigators, there are This comparison revealed that the fetal and
very few publications on the arterial system adult vascular systems are similar, which
of the sperm whale Physeter macrocephalus. agrees with the data of other researchers
The first mention of the vasculature of this (Ommanney, ’32; Walmsley, ’38). Arteries
species was made by J. Hanter (1787) in a were studied by gross dissection, corrosion,
paper in which he described the main ves- and serial section and radiography. By these
sels of whales and also noted a proliferation methods 25 individuals were studied by ex-
of twisted arteries. This work was followed amination: 12 macrospecimens, corrosion
by a long hiatus in research on sperm whale preparation from nine specimens, two x-ray
blood circulation, not broken until White photographs, and 41 serial sections from two
and Kerr (’15) published their description of individuals.
the heart and its vessels. Morphology of the Gross dissection was a primary means of
main vessels of the venous system was re- investigation and consisted of clearing ves-
ported by Beddard (’24). In addition, angio- sels of environmental tissue. From dissec-
genesis during early embryogenesis has been tion the relation of the vessels to soft tissues
reported by Golub et al. (’68), and Leontjuk and skeleton could be determined.
(’69, ’71). Herein we describe the arterial For reception corrosion preparations we
system of P. macrocephalus. used a plastic applied in adhesion of den-
tures (polymers of the akril acid AKR-7,
MATERIALS AND METHODS AKR-15 in Russia) for injection of blood ves-
The material for this study was collected sels. Initially we tried to use celluloidin and
by the author during expeditions of the whal- neoprene latex; however, they were not suit-
ing fleet Vladivostok in 1974–1977. Exami- able. For injections a glass cannula was in-
nation of the arterial adult sperm whale is serted into the beginning of the aortic arch
difficult because of the huge size of these through the left ventricles of the heart. The
animals. Thus, the vascular anatomy of these injection was carried out in two or three
animals described here is based predomi-
nantly on material obtained from fetuses. In
order to study age-related changes in the *Correspondence to: Vladimir V. Melnikov, 43 Baltiyskaya
vascular system, we compared fetal speci- Street 690031 Vladivostok Russia. E-mail: [email protected]

r 1997 WILEY-LISS, INC.

38 V.V. MELNIKOV

doses, thus allowing maximum filling of ves- fetus, the ductus arteriosus leads up to the
sels. The vascular system is best filled after top of the arch from below.
thawing of individuals, allowing disintegra- The right brachiocephalic artery is a very
tion of the thrombus of blood. For tissue short thick vessel, which immediately after
maceration the body of the fetus was placed its origin near the anterior edge of the first
in a covered bath containing concentrated rib divides into its terminal branches, the
alkalis (NaOH or KOH). This bath is safer right common carotid and the right subcla-
than a traditional acid bath and decomposes vian artery. The right common carotid ar-
all tissues including fat. Acid does not decom-
tery is somewhat shorter than the left com-
pose fat tissue sufficiently. After a few days
the preparation was gently washed in run- mon carotid, which originates directly from
ning water for some hours. the aortic arch. Both right and left common
For reception x-ray photographs we used carotid arteries course along the ventrolat-
red lead for filling vessels. eral surface of the trachea and, upon reach-
For serial sections we used frozen fetuses ing the caudal edge of the thyroid cartilage,
1.6 and 4.3 m in length. The knowledge divide into an external carotid and internal
obtained from these preparations made it carotid artery. On its way the common ca-
possible to visualize the course of vessels in rotid gives rise to numerous variable
relation to each other and to the bony and branches that proceed to the thoracic and
soft structures. occipital retia mirabilia. The largest and
RESULTS
most constant branch is the thyroid artery
Aorta and its branches supplying the thyroid gland. On the left the
artery begins most often as two independent
The aortic arch of the sperm whale branches but on the right as a single short
emerges from the left ventricle of the heart trunk.
at the level of the first intercostal interval The fetal internal carotid artery runs cra-
and continues dorsal at the level of the first nially through the jugular incisure and
rib. It then curves left and descends to the
through it penetrates into the tympanic an-
level of fourth thoracic vertebra, where it
proceeds as the thoracic aorta (Figs. 1, 3, 4). trum. It then passes through the foramen
At its point of origin, the aortic arch gives lacer and enters the caves cranii, where it
off a right and left coronary artery, after participates in the formation of the carotid
which it becomes appreciably larger, more rete mirabile. Along its course the internal
than 1.5 times its diameter at its origin carotid does not give off any branches. How-
(Table 1). From the convex surface of the ever, this fetal pattern differs from that in
arch, the right brachiocephalic artery, the adults. In adult animals, the internal ca-
left common carotid artery, and the left sub- rotid artery has a beginning diameter of
clavian artery branch off (Figs. 1, 4). In the 37–46 mm, but the artery then quickly nar-

Fig. 1. Scheme of the arterial system of the sperm maxillary artery; 17, infraorbital artery; 18, intercostal
whale Physeter macrocephalus viewed from the left side. arteries; 19, internal thoracic artery; 20, thoracic rete
1, aortic arch; 2, right brachiocephalic artery; 3, left mirabile; 21, dorsal cervical rete mirabile; 22, thoracic
subclavian artery; 4, internal carotid artery; 5, left exter- rete mirabile; 23, thoracic aorta; 24, abdominal aorta;
nal carotid artery; 6, thyroid artery; 7, laryngeal artery; 25, celiac artery; 26, mesenteric cranial artery; 27, renal
8, occipital artery; 9, lingual artery; 10, deep temporal artery; 28, internal spermatic artery; 29, common iliac
artery; 11, external orbital artery; 12, inferior alveolar artery; 30, caudal epigastric artery; 31, branches for
artery; 13, major palatine artery; 14, buccinatory artery; urogenital organs; 32, branch for anal sphincter; 33,
15, buccal branch of the buccinatory artery; 16, internal caudal artery.
 ARTERIAL SYSTEM OF SPERM WHALE 39

Fig. 2. (top) Scheme of the arterial system of the alveolar artery; 21, major palatine artery.
head of the sperm whale Physeter macrocephalus. Para-
saggital section, view from right side. 1, right common Fig. 3. (bottom) Schematic view of the heart and
carotid artery; 2, thyroid artery; 3, internal carotid ar- associated arteries of the sperm whale Physeter macro-
tery; 4, laryngeal artery; 5, external carotid artery; 6, cephalus fetus. Frontal section of ventral portion of the
surface branch of the occipital artery; 7, external orbital anterior thoracic region of the body. 1, heart; 2, left
artery; 8, deep temporal artery; 9, vertebral rete mira- external carotid artery; 3, right external carotid artery;
bile; 10, occipital rete mirabile; 11, carotid rete mirabile; 4, right atrium; 5, left atrium; 6, pulmonary artery; 7,
12, infraorbital rete mirabile; 13, lingual artery; 14, thoracic rete mirabile; 8, thoracic rete mirabile; 9,
internal maxillary artery; 15, pterigo-palatine artery; scapula; 10, ribs; 11, thyroid cartilage; 12, thymus gland;
16, infraorbital artery; 17, branch of the occipital artery; 13, muscles of thoracic girdle; 14, right brachiocephalic
18, dorsal branch of the intermaxillary artery; 19, ven- artery; 15, right subclavian artery; 16, diaphragm; 17,
tral branch of the intermaxillary artery; 20, inferior scalenus muscles.
40 V.V. MELNIKOV

Fig. 4. Corrosive preparation of the head and trunk Fig. 5. Corrosive preparation of head and trunk arteries
arteries of the sperm whale Physeter macrocephalus. View of the sperm whale Physeter macrocephalus fetus. View
from left side of female, 85 cm, scale 1:2. 1, aortic arch; 2, from above of female, 85 cm, scale 1:2. 1, carotid rete mira-
thoracic aorta; 3, thoracic aorta; 4, left subclavian artery; 5, bile aorta arch; 2, vertebral rete mirabile; 3, infraorbital rete
internal carotid artery; 6, external carotid artery; 7, internal mirabile; 4, dorsal cervical rete mirabile; 5, thoracic rete
maxillary artery; 8, infraorbital artery; 9, laryngeal artery; mirabile; 6, internal thoracic artery; 7, pulmonary artery; 8,
10, lingual artery; 11, inferior alveolar artery; 12, carotid thoracic aorta; 9, abdominal aorta; 10, intercostal arteries;
rete mirabile; 13, infraorbital rete mirabile; 14, external 11, left subclavian artery; 12, occipital rete mirabile; 13,
orbital artery; 15, dorsal cervical rete mirabile; 16, occipital internal maxillary artery; 14, infraorbital artery; 15, inter-
rete mirabile; 17, intercostal arteries; 18, thoracic rete mira- maxillary artery.
bile; 19, right and left internal thoracic artery; 20, celiac
artery; 21, mesenteric cranial artery; 22, abdominal aorta;
23, vertebral rete mirabile.

rows and ends before reaching the jugular 4). In all specimens, these branches begin
incisure. separately and run dorsally near the caudal
The external carotid artery is the second surface of the occipital bones. The laryngeal
terminal branch of the common carotid ar- artery splits at its origin into a lateral and a
tery and constitutes its continuation. Near ventral branch. The large ventral branch
the lateral edge of the occipital bone it termi- branches extensively in the great sternohy-
nates by bifurcating into lingual and inter- oid muscle, while the lateral branch sup-
nal maxillary arteries. From the external plies the sternocephalic muscle.
carotid artery spring 1) numerous, variable The lingual artery is a terminal branch of
small-sized branches to the occipital rete the external carotid artery. It runs anteri-
mirabile, 2) branches supplying the muscles orly and supplies the muscles of the root and
of the larynx and pharynx, and 3) the large, body of the tongue.
consistently present occipital and laryngeal The internal maxillary artery is the other
arteries. The occipital artery consists of a terminal branch of the external carotid ar-
deep branch and a surface branch (Figs. 1, tery and is its continuation. Initially, this
 ARTERIAL SYSTEM OF SPERM WHALE 41
TABLE 1. Caliber of arteries of adult sperm whales penetrates the fat body located here. An-
Physeter macrocephalus teriorly the inferior alveolar artery is sur-
Male, 11.4 m rounded by a crown of veins and appears
Male, 16 m, Thickness as a typical complex vessel (Tomilin, ’50,
Diameter Diameter of wall ’51).
Point of measure (cm) (cm) (cm) 5. The buccinatory artery, which arises near
Aortic arch distal to the forepart of the orbit and usually di-
aortic valve 16.5 15.0 1.2 vides at once into two separate
Aortic arch beyond branches—the buccal and the orbital.
right brachioce- These branches arise independently. The
phalic artery 23.0 20.0 1.4
Origin of thoracic buccal branch supplies the buccinatory
aorta 10.0 8.9 0.26 muscles and the surface of the masseter.
Origin of abdominal The orbital branch goes into the front of
aorta 7.3 6.7 0.22
Origin of caudal
the orbital muscles.
artery 5.0 4.1 0.22 In addition to the above branches, the
Origin of left subcla-
vian artery 6.1 4.8 0.25
internal maxillary artery gives off a variable
Origin of right number of small-sized vessels to all the or-
common carotid gans and tissues it passes. Of these small
artery 6.7 6.3 0.5 arteries, branches to the palate and the large
Origin of left
external carotid masseters are the most consistent.
artery — 3.3 0.31 The infraorbital artery of the sperm whale
Origin of left infra- is well developed. After exiting the infraor-
orbital artery — 3.8 0.15 bital aperture on the facial surface of the
Origin of left inter-
maxillary artery — 3.1 0.05 rostrum, the infraorbital artery divides into
two equal-sized branches, which run in oppo-
site directions above the rostrum and dorsal
appendix of the maxillary bone. From these
artery lies on the bottom surface of the bulla main vessels numerous parallel arteries
tympanica and then, near the zygomatic arise, running anteriorly between the
arch, proceeds to the infraorbital channel, muscles in the muscle-tendon layer of the
from where it continues as the infraorbital spermaceti organ, parallel to its muscle fi-
artery. The internal maxillary artery gives bers (Figs. 1, 2, 4, 5). In addition to the
off five branches: terminal parallel branches, the right infraor-
1. The external orbital artery that arises bital artery gives off a large intermaxillary
near the edge of the zygomatic process of artery and two smaller branches of the ma-
the temporal bone lies on the bottom of jor palatine artery in the cavity of the infra-
the orbital cavity but then curves to the orbital channel (Figs. 2, 5).
infraorbital rete mirabile. It is the main The intermaxillary artery (an unpaired
contributing artery to the rete. artery) is always a branch of the right infra-
2. The deep temporal artery, separated inde- orbital artery. It splits off in the infraorbital
pendently, goes together with the exter- channel and runs in a separate channel to
nal orbital artery or with the pterygoid- the middle of the rostrum, where it leaves
palatine artery into the temporal cavity. through the intermaxillary foramen and runs
3. The pterygo-palatine artery arises as a on to the surface of the right intermaxillary
common trunk with the deep temporal bone. Upon exiting, it divides into two
artery, with the inferior alveolar artery, branches—dorsal and ventral (Fig. 2). The
or independently. It is present as a short dorsal branch, reaches the level of the hori-
vessel, which branches extensively into zontal part of the left nasal passage, and
the basis cranii venous plexus located in then curves and follows it lengthwise to ter-
the pterigoid sinus area. minate in the shut muscles of the hole. The
4. The inferior alveolar artery usually arises ventral branch gives off branches near its
by a common trunk with the pterygo- origin that supply the muscle of the anterior
palatine artery, sometimes together with wall of the frontal air cavity. It then extends
the buccal artery or independently. It anteriorly to the end of the rostrum above
passes into the mandibular canal. In the the rostral cartilage.
caudal canal the inferior alveolar artery The major palatine artery (a paired ar-
passes through the plexus of veins that tery) runs in the palatine channel. The right
42 V.V. MELNIKOV

major palatine artery is appreciably bigger the rete and supply the intercostal
then the left. The right artery immediately muscles.
splits into two branches, which run anteri- The omooccipital artery, which arises from
orly in a separate channel to the end of the the subclavian artery at the frontal edge of
rostrum. The left major palatine artery does the first rib, divides into numerous branches
not split. The left and right major palatine that supply the occipital rete mirabile and
arteries in the channels are surrounded by a hypaxial cervical musculature.
characteristic nimbus of thin-walled veins The axillary artery is the continuation of
which is typical for complex vessels. the subclavian artery. At its start in the
The subclavian artery starts out asymmet- axillary hollow it gives off branches to the
rically. To the right it is a branch of the axillary musculature and occipital rete mira-
brachicephalic trunk, and to the left it sepa- bile. The axillary artery then travels to the
rates directly from the aortic arch (Figs. 1, pectoral fin, where it ends by diverging into
2). The right subclavian artery runs dorsally numerous branches. These arterial branches
under the frontal edge of the first rib. It together with accompanying veins form com-
gives off the internal thoracic artery and plex vessels.
then, much reduced in size, curves around The thoracic aorta initially lies on the left
the edge of the first rib and gives off the ventral surface of the vertebral column (Figs.
brachio-occipital artery. The subclavian con- 1, 4) and continues caudally to the right
tinues as the axillary artery which goes to under the spine. Branches of the thoracic
the pectoral fin. The left subclavian artery, aorta are:
after separating from the lateral wall of the
1. Three to five esophageal branches sepa-
aortic arch, travels ventrolaterally. At the
rately leave the dorsal wall of the aorta at
level of the middle of the second rib, it gives
the level of the fourth thoracic vertebra.
rise to the internal thoracic artery. The sub- These branches run anteriorly and
clavian artery then curves forward abruptly quickly form a small rete between the
around the first rib, where it gives of the esophagus and vertebral column.
brachio-occipital artery and then goes to the 2. There are seven pairs of intercostal arter-
pectoral fin. ies. Each pair leaves the aorta separately.
The internal thoracic artery arises on the The first pair, larger than the others,
right at the level of the first rib and on the passes dorsally between the capita of the
left at the level of the second rib. Covered by fourth and fifth ribs to the apex of the
the costal pleura, it runs caudally along the spinous processes, abruptly turns anteri-
internal surface of the lateral wall of the orly, and divides into a large number of
thoracic cavity (Figs. 1, 4). Cranially, the twisted vessels of the dorsal cervical rete
internal thoracic artery supplies the tho- mirabile. All the other intercostal arter-
racic retie mirabilie. Behind the sternum it ies form small areas of retia at the level of
continues as the cranio-epigastric artery. The the intervertebral foramina. These arte-
internal thoracic artery gives off numerous rial retia surround the roots of the corre-
and variable branches to the thoracic rete sponding nerves and anastomose with
mirabile and intercostal muscles and two the vertebral arterial retia. The two to
arteries: seven pairs of intercostal arteries branch
1. The musculophrenic artery arises from out, supplying the retia, and divide into
the internal thoracic artery at its point of the intercostal and epaxial branches at
origin and sends branches to the pericar- the level of the intervertebral foramina.
dium, which continue on to the dia- The abdominal aorta of the sperm whale
phragm. In addition, the musculophrenic begins somewhat more anteriorly than in
artery gives off many vessels to the tho- most mammals because of the steep inclina-
racic rete mirabile. tion of the diaphragm. Typical branches (e.g.,
2. The cranial intercostal artery arises as the celiac and cranial mesenteric arteries)
one or two branches either craniad or pierce the diaphragm. The abdominal aorta
caudal to the musculophrenic artery from divides into 1) parietal branches supplying
the internal thoracic artery. At its origin the epiaxial muscles and wall of the abdomi-
it divides into a large number of branches nal cavity and 2) a visceral branch to the
to the thoracic rete mirabile. Some of viscera (Figs. 1, 4, 7). The parietal branches
these branches pass the caudal border of consist of seven to eight pairs of lumbar
 ARTERIAL SYSTEM OF SPERM WHALE 43

Fig. 6. (top) Corrosive preparation of the arterial Fig. 7. (bottom) Corrosive preparation of caudal part
system of a sperm whale Physeter macrocephalus fetus. of the arterial system of the sperm whale Physeter
View from above of male, 150 cm, scale 1:2.5, with macrocephalus fetus. View from above, female, 85 cm,
maximum filling of the complex of the retia mirabilia of scale 1:2. 1, thoracic aorta; 2, abdominal aorta; 3, caudal
head and trunk. 1, thoracic aorta; 2, internal maxillary artery; 4, common iliac artery; 5, celiac artery; 6, mesen-
artery; 3, infraorbital artery; 4, carotid rete mirabile; 5, teric cranial artery; 7, renal artery; 8, uterine rete mira-
infraorbital rete mirabile; 6, vertebral rete mirabile; 7, bile; 9, umbilical artery; 10, caudal epigastric artery; 11,
dorsal cervical rete mirabile; 8, thoracic rete mirabile; 9, branches for urogenital organs; 12, parietal segmental
occipital rete mirabile. branches; 13, branch for anal sphincter; 14, ventral
segmental branches of the caudal artery; 15, dorsal
segmental branches of the caudal artery.
44 V.V. MELNIKOV

arteries. The first two pairs arise separately, ing off branches supplying the muscles. The
whereas the others have short common umbilical artery (paired) functions only in
trunks. Similarly to the intercostal arteries, the fetus and is similar to that of other
the lumbar arteries go to the intercostal mammals.
foramina, where they divide into the abdomi- The caudal artery travels within the tail
nal wall and epaxial branches at the level of in the hemal channel, in which it extends to
the intervertebral foramina. They do not the last tail vertebra (Figs. 1, 7). In the
form retia. hemal channel it is surrounded by an areola
Visceral branches of the abdominal aorta of small-sized anastomosing arteries and
are as follows: veins. In transverse section, the caudal ar-
1. The celiac artery (unpaired) arises off tery has the structure of a typical complex
near the last thoracic vertebra, also pen- vessel (Tomilin, ’50, ’51). In addition to nu-
etrates the diaphragm, and supplies the merous peripheral branches that surround
stomach, liver, and spleen. the caudal artery, it also gives rise to the
2. The mesenteric cranial artery (unpaired) dorsal and ventral segmental branches, and
arises just caudal to the celiac artery, the largest—the branch supplying the anal
penetrates the diaphragm, and ramifies sphincter.
in the mesentery and walls of the intes- The dorsal segmental branches (paired) of
tine and colon. the caudal artery are arranged similarly to
3. The renal artery (paired) begins under the intercostal arteries. The ventral segmen-
the second lumbar vertebra and supplies tal branches arise from the caudal artery
the kidney. between the hemal arches. They run ven-
4. The suprarenal artery (paired) arises from trally in a bundle of six or seven vessels and
the abdominal aorta or the renal artery supply the ventral muscles of the tail. The
as one or two small branches. branch supplying the sphincter of the anus
5. The internal spermatic artery (paired) arises from the caudal artery between the
begins caudal to the sixth lumbar verte- second and third hemal arches. In addition
bra and proceeds dissimilarly structure to supplying the anal muscles, it also sup-
in the male and female. In the male, this plies part of the hypaxial muscles of the tail.
artery runs ventrally along the medial Arterial retia mirabilia
surface of the large ventral muscles and A distinctive feature of the vascular sys-
supplies the ventral muscles, the ure- tem of cetaceans is the presence of numer-
thra, the reproductive glands, and the ous, widely spread arterial networks called
urinary bladder. In the female, the inter- retia mirabilia (miraculous networks) be-
nal spermatic artery consists of numer- cause of their unusual appearance. The ex-
ous branches, which leave the aorta inde- tensiveness of retia mirabilia and the poorly
pendently. These interweaving branches delineated areas of arterial retia mirabilia
run ventrally through the wide uterine in the sperm whale prohibit defining exact
ligament and penetrate the walls of the borderlines (Fig. 6). Consequently, the classi-
uterus, where they form a rete mirabile. fication of the retia is difficult, and their
Some branches, as in the male, supply division is to a certain degree arbitrary. Anas-
the ventral muscles, urethra, and uri- tomoses between retia also make it difficult
nary bladder. to delineate where one rete ends and an-
The common iliac artery (paired) is one of other begins, as they seem at times to merge.
the terminal branches of the aorta (Figs. 1, Arterial retia mirabilia are best developed
7). It begins caudal of the seventh lumbar in the thoracic cavity, in the cervical area,
vertebra, runs caudo-ventrally, and ends by and in the cranial cavity.
dividing into the caudal epigastric and um- The paired thoracic retia mirabilia lie in
bilical arteries. The caudal epigastric artery the area of the anterior thoracic aperture
is the continuation of the common iliac ar- (Figs. 1, 4–6, 8). At the level of the first rib,
tery. It runs caudo-ventrally along the inter- the rete is thickest and most extensive, de-
nal surface of the abdominal wall. Before scending from the vertebral column along
reaching the anus, it gives rise to a series of the internal surface of the thoracic wall down
branches supplying the urogenital organs. to the sternum. Caudally, the rete gradually
Afterwards, it curves abruptly forward into flattens and extends to the fourth rib in the
the abdominal wall muscles, where it runs form of a semicircle. Cranially, it extends to
anteriorly to the level of the fourth rib, giv- the occipital rete mirabile. The thoracic rete
 ARTERIAL SYSTEM OF SPERM WHALE 45

Fig. 8. Cross-section through the body of sperm whale subclavian artery; 6, left common jugular vein; 7, right
Physeter macrocephalus fetus at level of first thoracic common jugular vein; 8, thoracic rete mirabile; 9, tra-
vertebra. Viev from anterior female, 360 cm, scale 1:10. chea; 10, esophagus; 11, thymus; 12, vertebral rete mira-
1, aorta arch; 2, left common carotid artery; 3, right bile.
brachiocephalic artery; 4, right subclavian artery; 5, left

mirabile is formed by a large number of bile, together with the dorsal cervical rete
small-caliber, twisted, anastomosing, thick- and thoracic rete, connects with the verte-
walled vessels located in the fat tissue. The bral arterial rete through the intervertebral
blood to this rete arrives predominantly from foramina. The occipital rete mirabile con-
the subclavian artery and its branches. From sists of a large number of small-caliber,
the rete, through anastomoses in the inter- twisted, anastomosing, thick-walled vessels
verebral foramina, blood goes to the verte- located in the fat tissue. Dorsally, the arter-
bral rete mirabile. Branches from the costo- ies of the rete are oriented mainly toward
cervical vein penetrate this rete but do not the intervertebral foramina. The primary
form a venous plexus. sources of blood supply to the occipital rete
The paired occipital retia mirabilia are mirabile are the common carotid artery, the
located in the fascias of the ventral neck external carotid artery and its branches,
muscles between the lateral occipital bones and the occipital artery. The relatively small
and the first ribs (Figs. 2, 4, 6). The main number of veins in this rete cannot be char-
mass of the rete is concentrated between the acterized as a venous plexus.
sternocranial and brachiacranial muscles The dorsal cervical rete mirabile (paired)
and the trachea and anterior portion of the is located symmetrically above the vertebral
scalene muscle. Anteriorly, the rete is lim- column in the fascias of the left and right
ited by the bones of the skull. Posteriorly, it epiaxial cervical muscles (Figs. 1, 4, 6). Ante-
fills the axillary hollow and extends to the riorly, it is limited by the parietal region of
thoracic rete mirabile. Inferiorly, this rete is the skull. Posteriorly the rete reaches the
bordered by the surface of the sterno-lingual level of the fourth thoracic vertebra. Inferi-
muscle. Superiorly, the occipital rete mira- orly, the layers of the dorsal cervical rete lie
46 V.V. MELNIKOV

on the surface of the vertebral column be- Anteriorly, it connects with the paired infra-
tween the separate epiaxial muscles. These orbital rete mirabile near the optic chiasma.
layers are interconnected among themselves The vascular configuration of the carotid
and with the thoracic and occipital retia. All rete mirabile changes with location. In the
of these retia are also connected with the area of the hypophyseal fossa, it consists of a
vertebral column rete at the intervertebral mass of twisted anastomosing vessels. On
foramen. The dorsal cervical rete mirabile the surface of the cerebral hemispheres, the
consists of a large number of small-caliber, rete consists of straight, thin-walled, paral-
twisted, anastomosing, thick-walled vessels lel vessels, which form a flat network. Cover-
located in the fat tissue. Blood to the dorsal ing the cerebellum and myelencephalon, it is
cervical rete mirabile flows from the parietal a network of small-caliber, slightly twisted,
branches of the occipital artery and the first thin-walled vessels. The blood flows mainly
pair of intercostal arteries. Blood from this from the vertebral rete and in part from
rete flows to the vertebral rete through anas- infraorbital rete mirabile that connect with
tomoses in the intervertebral foramina. the internal maxillary artery through the
The vertebral rete mirabile (unpaired) lies external orbital artery. The brain is supplied
epidurally in the vertebral canal and sur- by vessels arising from retia located on the
rounds most of the spinal cord, leaving only bottom of the cranial cavity in the hypophy-
a narrow slit on its dorsal surface (Figs. 2, seal fossa. Between the arteries of the ca-
4–6, 8). Anteriorly, it enters the skull cavity rotid rete mirabile is a venous network of
through the great occipital foramen and con- thin-walled vessels.
tinues as the carotid arterial rete. Caudally, The infraorbital rete mirabile (paired) sur-
it gradually decreases in size and extends to rounds the entire length of the optic nerve
the middle of the vertebral column. In the (Figs. 2, 4–6). The external orbital artery
lumbar region, segmentation of the rete is enters the rete after exiting the optical fora-
men. Vessels of the rete are mostly longitudi-
more and more obvious, as it enlarges in the
nal, small caliber, and only slightly twisted.
zone of the intervertebral foramina, where
Blood flows from the external orbital artery
branches of the lumbar arteries flow into the and from the carotid rete mirabile to the
vertebral rete. The vertebral rete mirabile is infraorbital rete.
formed of a large number of small-caliber, The uterine rete mirabile is located in the
longitudinal anastomosing vessels. The vascular layer of the walls of the uterine
twisting of the arteries gradually decreases horns and body (Figs. 1, 7). The rete consist
caudally until they are almost straight in mainly of twisted thick-walled arteries. No
the lumbar area of the vertebral column. No fat tissue is present. The uterine rete mira-
differentiation of the meningeal artery is bile of the cetacean has not been described
observed. Blood flows from the thoracic and previously in the literature available to us.
occipital retia to the vertebral rete through However, the vascular networks of the iliac
anastomoses in the intervertebral foramina. region, the ovaries, and testicles have been
Blood also flows from the vertebral branch of described (Slijper, ’36; Ivanova, ’75).
the intercostal and lumbar arteries into the
vertebral rete. The general topography of all DISCUSSION
arterial retia mirabilia indicates that the The results of this study show that the
vertebral rete mirabile is a collector for all arterial system of the sperm whale is similar
arterial retia of the thoracic and cervical in many ways to that of other mammals.
part of the body of the sperm whale. However, it also shows that the sperm whale
The carotid rete mirabile (unpaired) lies arterial system has many specific vascular
epidurally in the cranial cavity between the structures associated with the aquatic envi-
dura mater and the periosteum (Figs. 2, 4, 5, ronment of this animal.
6). The main mass of the rete is located on In some marine mammals, a bulbous ex-
the bottom of the cranial cavity in the hy- pansion of the aortic arch has been de-
pophyseal fossa. Two expansions of this rete scribed (Drabec, ’75; Galantsev, ’77). How-
ascend dorsally along the lateral and dorsal ever, in Stenella longirostris, Phocenoides
surface of the cerebral hemispheres. Cau- dalli, and Lagenorhinchus obliquidens an
dally, the carotid rete mirabile covers the aortic arch expansion is absent (Melnikov,
cerebellum on either side and the myelen- ’81). In the Bryde whale, expansion of the
cephalon; passing through the occipital fora- aortal arch is slight or completely absent
men, it connects with the vertebral rete. (Melnikov, ’94). It appears that this bulbous
 ARTERIAL SYSTEM OF SPERM WHALE 47

expansion of the aortic arch of the sperm Slijper, ’36; Galliano et al., ’66). The sperm
whale may be an adaptation to the aquatic whale is thus an exception. No homologue of
environment. the costocervical artery was found, although
One peculiarity of the arterial system of this term might be used to describe the first
odontoceti whales is the cranial displace- pair of intercostal arteries. However, they
ment of the aortic arch (Slijper, ’36). In ter- appear to be typical segmented branches off
restrial mammals, the arch reaches the level the thoracic aorta. It is also possible to con-
of the third to the fifth intercostal intervals, sider one of the branches of the occipital
but in Bryde whales it reaches the level of artery as a homologue, but the occipital ar-
the third rib (Melnikov, ’94), and in sperm tery always arises from the external carotid
whales and dolphins the aortic arch reaches artery.
the level of the first intercostal interval and One distinctive feature of the arterial sys-
first rib. This cranial displacement of the tem of cetaceans is the presence of a well-
aortic arch may be related to the shortening developed occipital artery. The sperm whale
of the cervical and anterior thoracic spinal even has two occipital arteries on each side.
column, which displaces all the organs of the In some terrestrial mammals (Artiodactyla
neck and thorax anteriorly (Schulte, ’16; Sli- and some Carnivora), this artery supplies
jper, ’36). the brain through anastomoses (Daniel et
The branches off the aortic arch of the al., ’53; Ivanova, ’75). In the sperm whale, as
sperm whale arise symmetrically, as in other in other cetaceans, such anastomotic connec-
cetaceans (Slijper, ’36). In most terrestrial tions have not been observed, and the occipi-
mammals the right and left common carotid tal artery supplies blood mainly to the occipi-
artery arises from a brachiocephalic trunk. tal and dorsal cervical retia mirabilia.
In the sperm whale the magistrals for the During the last 10 years there has been
left and right side of head arise from aortic intensive study of the echo-sounding mecha-
nism of the toothed whales. In the sperm
arch separately, and, similarly to other ceta-
whale the spermaceti body is assumed to
ceans, neither the left brachiocephalic nor
play a significant role. Thus, it seems appro-
the right common carotid artery gives rise to
priate to mention the large number of well-
a paired common carotid artery. The branch-
developed arterial vessels present in the
ing of the aortal arch in cetaceans is (from
muscle-tendon layer of the spermaceti body.
right to left) the right subclavian artery, the
There is no comparable concentration of ar-
right common carotid artery, the left com-
teries in any other muscle or organ of the
mon carotid artery, and the left subclavian sperm whale, and the fat tissue of the sper-
artery. As similar symmetric branching of maceti body has only small-caliber, diffuse
the aortic arch is rare among mammals and vessels.
only found in the Hyroptera (Lassila, ’28). Asymetrical development of arterial ves-
Our observations show that the internal sels is typical of the sperm whale. The ves-
carotid artery of the sperm whale does not sels of the right half of the body are larger
supply blood to the brain. A functional con- than those of the left half, and only the right
nection between the internal carotid artery intermaxillary artery is present.
and the vessels of the brain is absent. This Around the branches of the palatine ar-
absence has been described for all cetaceans tery and the inferior alveolar artery is a
studied and has been widely discussed in the corona of veins typical of complex vessels.
literature (Howell, ’30; Ommanney, ’32; Sli- The corona around the caudal artery of the
jper, ’36; Galliano et al., ’66; Melnikov, ’94; sperm whale contains arterial branches as
others). The absence of functional connec- well as veins. In dolphins Slijper (’36) inter-
tion is peculiar not only for cetaceans but preted similar vessels as a rete mirabile, but
also for the Artiodactyla and some Car- in the sperm whale they appear to be typical
nivora, in which the carotid rete mirabile is complex vessels (Tomilin, ’50, ’51).
present (Daniel et al., ’63; Ivanova, ’75). The arterial system of the sperm whale is
A costocervical artery is absent in the characterized by extraordinary development
sperm whale, which is unusual for ceta- of arterial retia mirabilia. These retia are
ceans. In the all whales studied previously, widely distributed in the thoracic cavity,
the costocervical artery supplies the tho- neck, vertebral canal, and cranial cavity and
racic rete mirabile (Breshcet, 1836; Stan- around the optic nerve and in the walls of
nius, 1841; Barkov, 1851; Ommanney, ’32; the uterus. With the exception of the uterine
48 V.V. MELNIKOV

rete, all other arterial retia are intercon- column, whereas in dolphins this rete ends
nected by anastomoses and form a single anterior to the lumbar spine. In Balaenop-
vascular complex, located between the main terida, the rete is limited to the thoracic part
trunks (the common carotid and subclavian of the spine.
arteries and their branches) and the vessels The thoracic rete mirabile is present in all
of the spinal cord and brain. The vessels of species of Cetacea. The most extensively de-
this complex of arterial retia mirabilia have veloped rete is present in the Delphinopteri-
thick walls, are twisted, and frequently anas- dae, in which it extends lengthwise along
tomose among themselves. Venous networks the entire ventral part of the thoracic spine
are absent among the arteries of the tho- (Slijper, ’36; Galliano et al., ’66; Ivanova,
racic, occipital, and dorsal cervical retia mi- ’71). In sperm whales the thoracic rete mira-
rabilia. The arteries of these complex retia bile is found only on the internal lateral
are embedded in fat tissue. surface of the anterior part of the thoracic
In the last 10 years, detailed studies were cavity. On the ventral surface of the thoracic
conducted on the system of blood flow to the spine, the thoracic rete is small, reaching
brain of cetaceans (Daniel et al., ’63; Via- only to the level of the first three thoracic
monte et al., ’68; Nagel et al., ’68). In sperm vertebrae.
whales the brain is supplied mainly from the An occipital rete mirabile is most devel-
carotid rete. This rete is a continuation of oped in the sperm whale. In addition, a
the vertebral rete, which serves as a collec- massive dorsal cervical retia is characteris-
tor of blood from the retia mirabilia of the tic of the sperm whales.
thoracic and neck area. A second route for Although the arterial system of the sperm
blood to the brain of the sperm whale is whales had not been studied in any detail,
through the external orbital artery and infra- the literature suggests that the retia mira-
orbital rete. bilia is most developed in dolphins (Slijper,
In the arterial system of the brain of the
’36; Ivanova, ’75). Because the location of the
sperm whale and other cetaceans, the arter-
retia differs in various species of cetacean,
ies or sections of arteries that form the circu-
comparison of retia is difficult. However, we
lus arteriosus are absent, as is the basillaris
can assert that the complex arterial retia
cerebri artery, which is the main artery of
mirabilia in sperm whales is larger and more
the brain in other mammals. It must be
extensive than that of any cetacean previ-
noted that a carotid rete as extensive as that
ously studied.
of sperm whales has not been described for
any cetacean or mammal investigated thus Vascular networks and retia are not spe-
far. cific to cetaceans but are fairly widely distrib-
The sperm whale and other cetaceans pre- uted among mammals. Vascular networks
viously studied have a well-developed infra- are present in the extremities of Bradipus,
orbital rete. It and the accompanying infra- Lemur, Tarsius, Manis, Dasypus, and
orbital venous plexus form the coronal Myrmecophaga (Wislocki and Straus, ’32;
vessels covering the optic nerve. In terres- Fawcett, ’42). In all these species, it is pos-
trial mammals, the internal ophthalmic ar- sible to distinguish two types of networks.
tery accompanies the optic nerve. This ar- The first type is a simple profusion of anasto-
tery connects vessels of the brain with the mosing vessels in the form of networks (ex-
internal maxillary artery (Birikh and Ud- tremities of Dasypus and Lemur). The sec-
ovin, 1972). The reticular form of this artery ond type of network has a main vessel, which
is rare in mammals (Slijper, ’36). ends in 13–14 smaller parallel arteries, alter-
The vertebral rete mirabile in the verte- nating with various numbers of veins; the
bral canal of the sperm whale is located whole bundle of vessels has a common tunic
below and to each side of the spinal cord. In (Fawcett, ’42). Vascular networks and forma-
dolphins, this rete lies dorsal to the spinal tions similar to this are present in the upper
cord (Slijper, ’36). Moreover, the sperm whale extremities and between muscles of the tho-
does not have longitudinal meningeal arter- rax, neck, and thoracic girdle in manatees,
ies that are characteristic of the dolphins. Trichechus manatus (Murie, 1874; Fawcett,
Sperm whales have a more extensively devel- ’42). In manatees the networks have a bundle
oped vertebral rete than in any mammal of vessels consisting of numerous parallel
studied to date. Their vertebral rete reaches arteries of identical diameter, with each ar-
the posterior part of the lumbar vertebral tery accompanied by two veins. These
 ARTERIAL SYSTEM OF SPERM WHALE 49

bundles are of considerable length and ex- LITERATURE CITED

tend without any change in diameter. Barkow, H.C.L. (1851) Ueber die Arterien von Delphinus
It is noteworthy that vascular networks in phocoena. Anat. Abhand. Breslau 18:94–100.
most mammals are usually located in the Beddard, F.E. (1924) On some points in the structure of
the venous system and blood-glands of the neck in the
extremities, or periphery of the body be- cachelot. Ann. Mag. Nat Hist. 13:274–282.
tween muscles, where they are represented Birikh, B.K., and G.M. Udovin (1972) Vozrostnaja mor-
by a panicle of straight vessels that end in phologija krupnogo rogatogo skota [Age Morphology of
the Cattle]. Perm: Selhosisdat, pp. 1–248.
peripheral arteries. On the other hand, the Breschet, M.G. (1836) Histoire anatomigue et physiolo-
arterial retia mirabilia of Cetacea are close gigue d’un organe de nature vasculaire decouvert dans
to the head and the anterior part of the les cétacés. Paris: J. Bechet, pp. 1–83.
vertebral column and have an intermediate Daniel, P.M., J.D.K. Dawes, and M.M.S. Prichard (1963)
Studies of the carotid rete and its associated arteries.
position between extraneural and the intra- Philos. Trans. R. Soc. London 237:137–202.
neural arteries of the central nervous sys- Drabec, C.M. (1975) Some anatomical aspects of the
tem. In Sirenes and some Primates each cardiovascular system of Antarctic seals and their
artery in this type of vascular formation is possible functional significance in diving. J. Morph.
145:85–105.
accompanied by two to 14 veins (Fawcett, Fawcett, D.W. (1942) A comparative study of blood-
’42), whereas in the rete mirabilia of the vascular bundles in the Florida manatee and in cer-
Cetacea the arteries are not accompanied by tain cetaceans and edentates. J. Morph. 1:105–117.
Galantsev, V.P. (1977) Evolutsija adaptatcij nirjajuschih
veins. The distinctive differences between zivotnih [Adaptive Evolution of the Diving Animals].
the usual mammalian vascular networks, Leningrad: Nauka; 190 pp.
with the exception of the carotid rete, indi- Galliano, R.E., P.J. Morgane, W.L. McFarland, E.L. Na-
cate that these two types of arterial forma- gel, and R.L. Catherman (1966) The anatomy of the
cervicothoracic arterial system in bottlenose dolphin
tions are not analogous. However, we regard Tursiops truncatus with a surgical approach suitable
the special vascular networks of Sirenes and for guided angiography. Anat. Rec. 155:325–338.
some Primates as analogous to the arteries Golub, D.M., A.S. Leontjuk, and I.I. Novikov (1968)
in the channels of the maxilla, mandible, Materiali po embriologii kitoobrasnikh. Zarodish
kashalota 8.5 mm dlini [Materials on embryology of
and palatine bone and in the hemal canal Cetacea. Embryo of cachelot 8.5 mm long] Sool. Jour-
and extremities of sperm whales. nal 5:953–958.
In summary, the arterial circulation of the Hanter, J. (1787) Observations on the structure and
sperm whales is similar in many ways to oeconomy of the whales. Philos. Trans. R. Soc. London
77:371–450.
that of other mammals. However, it has some Howell, A.B. (1930) Aquatic Mammals, Their Adapta-
specific attributes associated with the tions to Life in the Water. Springfield, IL: Thomas, 338
aquatic mode of life. Such specializations pp.
include an expansion of the aortic arch, the Ivanova, E.I. (1971) K morfolologii sosudistoj systemi
kitoobrasnih I lastonogih [To morphology of Cetacea
symmetrical position of the arteries leaving and Pinnipedia]. In K.K. Chapsky (ed): Issledovanija
the arch, absence of a direct functional con- morskih mlekopitajuschih [Investigations of Marine
nection between the internal carotid artery Mammals], Vol. 39. Trudi Atlant NIRO, pp. 179–192.
Ivanova, E.I. (1975) Funkcionalnaja morphologija cocud-
and the vessels of the brain, absence of a istoj cictemi mlekopitajuscih [Functional morphology
costocervical artery, and the presence of a of vascular system of the Mammalia]. Moscow: Nauka,
well-developed occipital artery. In addition, pp. 1–55.
the arterial system of the sperm whale is Lassila, V. (1928) Der Aortenbogen und die sich ihm
abzveigenden grossen Arterienstamme, nebst deren
characterized by extraordinary development Verhaltnis zu den Nervi Symparicus, vagus und recur-
of arterial retia mirabilia that are widely rens bei den Saugern. Ann. Acad. Sci. Fenn. [A], 27:1–
distributed in the thoracic cavity, neck, ver- 130.
tebral canal, and cranial cavity and around Leontjuk, A.S. (1969) Adaptivnie osobennosty krovenos-
noj systemy v rannem embriogenese kitoobrasnih
the optic nerve and in the walls of the uterus. [Adaptive peculiarity of the vascular system in early
The complex arterial retia mirabilia of the embryogenesis of the Cetacea]. In: 4-e Vsesojusnoe
sperm whale are more extensive and larger sovechanie po isucheniju morskih mlekopitajuschih.
than those of any cetacean studied to date. Moscow, VNIRO, pp. 80–83.
Leontjuk, A.S. (1971) Osobenosty rasvitija krovenosnoj
sistemi v rannem embriogenese kitoobrasnikh [The
ACKNOWLEDGMENTS peculiarity of development of the vascular system in
early embryogenesis of the Cetacea]. In K.K. Chapsky
Our thanks to North Slope Borough, De- Issledovanija morskih (ed): mlekopitajuschih [Investi-
partment of Wildlife Management, Barrow, gation of Marine Mammals]. Kaliningrad: Atlant-
Alaska, and especially to N.S. Strelkova for NIRO, pp. 198–205.
Melnikov, V.V. (1981) Krovenosnoe ruslo golovi shei I
help in preparing this article for publication spinnogrudnogo otdela tulovicha kitoobrasnih [The
in English. Vascular System of the Head and Anterior Truncal
50 V.V. MELNIKOV

Part of Cetacea]. Dissertation abstract, Vladivostok, Stannius, H. (1841) Ueber den verlauf der Arterien bei
pp. 1–23. Delphinus phocoena. Arch. Anat. Physiol. Jarb., 1:379–
Melnikov, V.V. (1994) The arterial system of the head 402.
and anterior truncal part of Balaenoptera edeni. In G. Tomilin, A.G. (1950) Plavniki—organy termoregulatsiji
Pilleri (ed): Investigation on Cetacea, Vol. 25. Paciano, u kitoobraznikh [Flippers are organs of thermoregula-
Museum of Natural History, pp. 309–318. tion of Cetacea]. Ribnoe Khosaystvo, 12:49–50.
Murie, J. (1874) On the form and structure of the mana- Tomilin, A.G. (1951) O termoreguljatsii u kitoobraznikh
tee (Manatus americanus). Trans. Zool. Soc. London [Thermoregulation in Cetacea]. Priroda 6:55–59.
8:127–150. Viamonte, M., P.J. Morgane, R.E. Galliano, E.L. Nagel,
Nagel, E.J., P.J. Morgane, W.L. McFarland, and R.E. and W.L. McFarland (1968) Angiography in living
Galliano (1968) Rete mirabile of dolphin: Its pressure- dolphin and observations on blood supply to the brain.
dumping effect on the cerebral circulation. Science Am. J. Physiol. 214:1225–1249.
161:898–900. Walmsley, R. (1938) Some observations on the vascular
Ommanney, F.D. (1932) The vascular networks (retia system of a female foetus finback. Contr. Embr. Carn-
mirabilia) of the fin-whale (Balaenoptera physalus) egie Inst. Washington 27:109–178.
Discovery Rep. 1:327–362. White, P.D., and W.I. Kerr (1915) The heart of the sperm
Schulte, H.W. (1916) The sei whale (Balaenoptera bore- whale with special reference to the A-V-conducting
alis Lesson). Anatomy of a foetus of Balaenoptera system. Heart 6:206–216.
borealis. Mem. Amer. Nat. Hist., N.S. 1:389–499. Wislocki, G.B., and W.L. Straus (1932) On the blood-
Slijper, E.J. (1936) Die Cetaceen. Capita Zoologica. 7 vascular bundles in the limbs of certain edentates and
(1–2):1–590. lemurs. Bull. Mus. Comp. Zool. Harv. Univ. 74:1–32.