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Citation: Molpeceres-Diego, I.;
Martín-Orti, R.; Loureiro, J.-P.;
Tostado-Marcos, C.;
Tendillo-Domínguez, E.;
Santos-Álvarez, I.; Pérez-Lloret, P.;
González-Soriano, J. The Respiratory
System of the Arctocephalus australis
in Comparison to the Dog as a
Land-Carnivore: Are There
Adaptations to Marine Life? Animals
2023,13, 199. https://doi.org/
10.3390/ani13020199
Academic Editors: Matilde
Lombardero and Mar Yllera
Fernández
Received: 1 December 2022
Revised: 23 December 2022
Accepted: 3 January 2023
Published: 5 January 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
animals
Article
The Respiratory System of the Arctocephalus australis in
Comparison to the Dog as a Land-Carnivore: Are There
Adaptations to Marine Life?
Ignacio Molpeceres-Diego 1, Rosario Martín-Orti 2, Juan-Pablo Loureiro 1, Carlos Tostado-Marcos 1,
Enrique Tendillo-Domínguez 1, Inmaculada Santos-Álvarez 2, Pilar Pérez-Lloret 2
and Juncal González-Soriano 2, *
1Fundación Mundo Marino, Av. X 157, San Clemente del TuyúB7105, Provincia de Buenos Aires, Argentina
2Departamento de Anatomía y Embriología, Sección Departamental de Anatomía y Embriología Veterinaria,
Facultad de Veterinaria, Universidad Complutense, Avenida Puerta de Hierro s/n, 28040 Madrid, Spain
*Correspondence: juncalgs@vet.ucm.es
Simple Summary:
It is normally recognized that anatomy is crucial for an improved knowledge of
many physiological adaptations. In the case of marine mammals, their ability to dive for long periods
of time is especially striking. They spend most of their lives in water, although in general terms, they
behave and have characteristics very similar to those of land mammals. Our results demonstrate
that, due to its capacity to stay under water, the respiratory apparatus of the South American fur
seal shows specific characteristics. Yet, in general terms, being a carnivore seems to be the main
characteristic of this species, and the adaptations to the aquatic environment being less important.
Abstract:
Marine mammals are divided into three groups, with similar adaptations resulting from
their aquatic lifestyle: sirenians, pinnipeds, and cetaceans. The present work focused on the South
American fur seal, or Arctocephalus australis, a carnivore included in the pinnipeds group. We as-
sessed whether the anatomical features of the
Arctocephalus australis’
respiratory system are com-
parable to those of other land-carnivores or whether these individuals show anatomical adapta-
tions related to their ability to dive or their breath-holding capacities. We studied 11 cadavers of
Arctocephalus australis
, which included adult (n= 2) and juvenile (n= 9) individuals, by anatomically
dissecting their isolated entire respiratory system. Although it is generally similar to that in land-
carnivores, we demonstrated that the Arctocephalus australis’s respiratory apparatus shows several
specific characteristics. Therefore, our results are of great importance for clinical diagnostic and
wildlife conservation purposes.
Keywords: Arctocephalus australis; anatomy; respiratory system; land-carnivore; dog
1. Introduction
Marine mammals have evolved from common ancestors that changed from a terrestrial
life to an aquatic environment. Yet, aquatic life presents numerous challenges for those
mammals originally adapted for life on land. Most of them develop their life, at least in part,
in an aquatic environment; therefore, it is supposed that some of their morphological and
physiological characteristics are linked to an organized evolution to marine-life adaptation.
However, despite all these changes, marine mammals still share some basic charac-
teristics with terrestrial mammals, such as breathing through lungs, being warm-blooded,
having fur (periodically in life), and producing milk to nurse their young [
1
–
3
]. As marine
mammals do not breathe in water, modifications to the respiratory tract are needed to
protect a system designed to function on land. Many of these adaptations have already
been described, for example, valvular nostrils that exclude water, or an intranarial larynx
in odontoceti that, while swallowing, further protects the respiratory tract from water
Animals 2023,13, 199. https://doi.org/10.3390/ani13020199 https://www.mdpi.com/journal/animals
Animals 2023,13, 199 2 of 15
inundation [
4
]. In addition, diving presents additional challenges, as ambient pressure
rises with depth, potentially causing the lungs to collapse [5].
The present study focused on the South American fur seal or Arctocephalus australis,
an otariid included in the taxonomic family of pinnipeds (Order Carnivora), such as the
dog or the cat [
6
,
7
]. Surprisingly, although it is generally accepted that anatomy is crucial
to a better understanding of different physiological adaptations [
2
], and although studies
on the physiology of diving are numerous [
1
,
8
–
19
], only a small number of them analyze
the anatomical characteristics of marine mammals [
5
,
20
–
24
], and even fewer are focused
on the anatomy of the respiratory system [2,3,25–27].
In the South American fur seal, its capability to remain submerged for some time is
well known. However, previous studies on the anatomy of the South American fur seal
are scarce. Thus, the possible anatomical adaptations of its respiratory system are yet to
be described. In other words, the question remains whether the respiratory system of
the Arctocephalus australis is similar to that in other carnivores or if there are significant
anatomical adaptations that allow the South American fur seal to dive.
In this work, we tried to answer this question. Thus, the objective of the present paper
was to perform an anatomical, systematic, and descriptive study of the South American
fur seal’s respiratory system and then compare it to the respiratory apparatus of another
carnivore model, the dog.
2. Materials and Methods
The study was performed on 11 cadavers of the species Arctocephalus australis, includ-
ing adult (n= 2) and juvenile (n= 9) individuals. All animals were found stranded on the
coast and taken to the Rescue and Rehabilitation Center Fundación Mundo Marino (FMM),
where they died. It is important to highlight that none of the individuals were euthanized.
They were all frozen until their dissection. After thawing for a period of 24/48 h, animals
were placed in dorsal recumbency and dissected by veterinarians.
As a first step, the skin and part of the blubber and muscle were removed. With
a scalpel blade, we made a first incision under the chin and continued down the midline
(linea mediana ventralis) to the xiphoid cartilage (cartilago xiphoidea). To make the internal
tissues visible, we extended the cut laterally along the costal arch.
Before cutting the ribs, we perforated the diaphragm. To open the thoracic cavity, we
cut through each thoracic rib mid-articulation (genu costae), which is the cartilaginous flex
point, and removed the rib cage..
For exposing the trachea and esophagus, the superficial musculature of the neck area
(regio collis ventralis) was removed. Then, we made a triangular incision along the inner sides
of the mandible body. The hyoid apparatus was cut, and the tongue was extracted through
the intermandibular space. The respiratory system was then progressively separated.
As the present study included both juvenile and adult individuals, each with a different
degree of development, the corresponding arithmetic means of the data obtained were
calculated separately.
Pictures were taken with a Canon EOS 500D (Tokyo, Japan) camera equipped with
an 18–55 mm lens.
As a complementary study, we prepared additional material:
-
Sample 1. An exhaustive washout period of the trachea, bronchi and lungs was
performed by leaking liquid for several days. Once cleaned, the empty ducts were
filled by injecting compressed air.
-
Sample 2. To obtain a template of the whole bronchial tree, expansive polyurethane
was inserted through the trachea. Once polyurethane was expanded and cured, the
sample was incubated with flies and larvae for tissue digestion to obtain the polymeric
template of the lower respiratory tract.
Animals 2023,13, 199 3 of 15
3. Results
3.1. Nose and Nares
The nose is completely coated with hairy skin except the apex, where nares are placed
and joined with the upper lip to give a higher functional mobility. The bones of the dorsal
and lateral nasal walls are formed by the facial bones, except in the rostral region. This
rostral region contains the dorsal and ventral lateral nasal cartilages. They are the bilateral
extension of the dorsal and ventral borders of the cartilaginous nasal septum. The nares
are placed in the nose apex. They are “boomerang”-shaped openings (Figure 1). The nose
apex, the nasal mimetic muscles, and the nares are fixed by a cartilaginous skeleton. The
surrounding skin, as well as the skin between the nares, is hairless and pigmented. It
forms the nasal plane, which presents small superficial furrows. The middle furrow or
philtrum extends all along the nasal plane, dividing it partially and not reaching the upper
lip (Figure 1).
Animals 2023, 13, x FOR PEER REVIEW 3 of 16
- Sample 2. To obtain a template of the whole bronchial tree, expansive polyurethane
was inserted through the trachea. Once polyurethane was expanded and cured, the
sample was incubated with flies and larvae for tissue digestion to obtain the poly-
meric template of the lower respiratory tract.
3. Results
3.1. Nose and Nares
The nose is completely coated with hairy skin except the apex, where nares are placed
and joined with the upper lip to give a higher functional mobility. The bones of the dorsal
and lateral nasal walls are formed by the facial bones, except in the rostral region. This
rostral region contains the dorsal and ventral lateral nasal cartilages. They are the bilateral
extension of the dorsal and ventral borders of the cartilaginous nasal septum. The nares
are placed in the nose apex. They are “boomerang”-shaped openings (Figure 1). The nose
apex, the nasal mimetic muscles, and the nares are fixed by a cartilaginous skeleton. The
surrounding skin, as well as the skin between the nares, is hairless and pigmented. It
forms the nasal plane, which presents small superficial furrows. The middle furrow or
philtrum extends all along the nasal plane, dividing it partially and not reaching the upper
lip (Figure 1).
Figure 1. Frontal view of the nares: opened (a) and slightly closed (b). Note the presence of different
furrows, (1) middle furrow or philtrum.
3.2. Nasal Cavity
The nasal cavity of the South American fur seal is narrow and long. It is divided into
two halves (right and left) by the nasal septum. In both halves, the ventral part is bony,
whereas the dorsal and rostral parts are cartilaginous. The perpendicular plate of the eth-
moid bone and the vomer forms the bony portion. Caudally, it does not reach the lower
part of the nasal cavity; thus, both nasal cavity halves are communicated. The cartilagi-
nous segment expands from the perpendicular plate of the ethmoid bone to the incisive
bones.
Caudally to the nasal cavity, the choanae connects the nasal cavity to the nasophar-
ynx. Each nasal cavity is mainly filled by the nasal conchae (dorsal, middle, and ventral
conchae), extending from the walls until nearly the nasal septum. The dorsal nasal con-
chae are relatively long and narrow, with a smooth surface, whereas the ventral is shorter
and wider and forms little parallel folds (plicae parallelis). The medial nasal conchae are
placed in between the other two.
The conchae divide each nasal cavity into subsequent parts called meatus. The dorsal
nasal meatus is narrow and short. It is placed between the dorsal nasal conchae and the roof
of the nasal cavity. The middle nasal meatus is located between the dorsal and ventral nasal
conchae. It is also short and narrow. The ventral nasal meatus is longer than the other two. It
Figure 1.
Frontal view of the nares: opened (
a
) and slightly closed (
b
). Note the presence of different
furrows, (1) middle furrow or philtrum.
3.2. Nasal Cavity
The nasal cavity of the South American fur seal is narrow and long. It is divided
into two halves (right and left) by the nasal septum. In both halves, the ventral part is
bony, whereas the dorsal and rostral parts are cartilaginous. The perpendicular plate of the
ethmoid bone and the vomer forms the bony portion. Caudally, it does not reach the lower
part of the nasal cavity; thus, both nasal cavity halves are communicated. The cartilaginous
segment expands from the perpendicular plate of the ethmoid bone to the incisive bones.
Caudally to the nasal cavity, the choanae connects the nasal cavity to the nasopharynx.
Each nasal cavity is mainly filled by the nasal conchae (dorsal, middle, and ventral conchae),
extending from the walls until nearly the nasal septum. The dorsal nasal conchae are
relatively long and narrow, with a smooth surface, whereas the ventral is shorter and wider
and forms little parallel folds (plicae parallelis). The medial nasal conchae are placed in
between the other two.
The conchae divide each nasal cavity into subsequent parts called meatus. The dorsal
nasal meatus is narrow and short. It is placed between the dorsal nasal conchae and the roof
of the nasal cavity. The middle nasal meatus is located between the dorsal and ventral nasal
conchae. It is also short and narrow. The ventral nasal meatus is longer than the other two.
It extends from the bottom of the nasal cavity to the nasal ventral conchae and leads into
the nasopharynx. Therefore, the ventral meatus represents a direct passage of air into the
larynx and lower respiratory tract. The common nasal meatus is the narrow space between
the nasal septum and the conchae, and it continues laterally with the other meatuses.
In fact, the choanae represent a direct path from the nasal cavity into the nasopharynx.
They are bounded rostrally by the horizontal portion of the palatine bone, laterally by the
Animals 2023,13, 199 4 of 15
pterygoid bone and the perpendicular plate of the palatine bone, and caudally by the vomer
bone. Interestingly, there are no paranasal sinuses in the Arctocephalus australis (Figure 2).
Animals 2023, 13, x FOR PEER REVIEW 4 of 16
extends from the bottom of the nasal cavity to the nasal ventral conchae and leads into the
nasopharynx. Therefore, the ventral meatus represents a direct passage of air into the larynx
and lower respiratory tract. The common nasal meatus is the narrow space between the nasal
septum and the conchae, and it continues laterally with the other meatuses.
In fact, the choanae represent a direct path from the nasal cavity into the nasophar-
ynx. They are bounded rostrally by the horizontal portion of the palatine bone, laterally
by the pterygoid bone and the perpendicular plate of the palatine bone, and caudally by
the vomer bone. Interestingly, there are no paranasal sinuses in the Arctocephalus australis
(Figure 2).
Figure 2. Lateral view of the left nasal cavity: (1) ventral nasal meatus; (2) choana; (3) nasopharynx;
(4) ventral nasal conchae with parallel folds (plicae parallelis); (5) middle nasal conchae; (6) dorsal
nasal conchae; (7) middle nasal meatus; (8) dorsal nasal meatus.
3.3. Pharynx
The pharynx is divided into the oropharynx, nasopharynx, and laryngopharynx. The
most noteworthy detail is the length of the soft palate, with a significant amount of peri-
pharyngeal soft tissue.
3.4. Larynx
The larynx is relatively short and wide (Figure 3). It is located underneath the skin, ven-
tral to the CI and CII vertebral body. It is dorsally related to the pharynx and the esophagus,
ventrally to the sternohyoid muscle, and laterally to the sternothyroid muscle and the man-
dibular gland. The cartilages are cricoid, thyroid, arytenoid, and epiglottis (Figure 4).
Figure 3. Larynx of Arctocephalus australis: (a) oblique view of the rostral larynx; (b) oblique view of
the caudal larynx.
Figure 2.
Lateral view of the left nasal cavity: (1) ventral nasal meatus; (2) choana; (3) nasopharynx;
(4) ventral nasal conchae with parallel folds (plicae parallelis); (5) middle nasal conchae; (6) dorsal
nasal conchae; (7) middle nasal meatus; (8) dorsal nasal meatus.
3.3. Pharynx
The pharynx is divided into the oropharynx, nasopharynx, and laryngopharynx.
The most noteworthy detail is the length of the soft palate, with a significant amount of
peripharyngeal soft tissue.
3.4. Larynx
The larynx is relatively short and wide (Figure 3). It is located underneath the skin,
ventral to the CI and CII vertebral body. It is dorsally related to the pharynx and the
esophagus, ventrally to the sternohyoid muscle, and laterally to the sternothyroid muscle
and the mandibular gland. The cartilages are cricoid, thyroid, arytenoid, and epiglottis
(Figure 4).
Animals 2023, 13, x FOR PEER REVIEW 4 of 16
extends from the bottom of the nasal cavity to the nasal ventral conchae and leads into the
nasopharynx. Therefore, the ventral meatus represents a direct passage of air into the larynx
and lower respiratory tract. The common nasal meatus is the narrow space between the nasal
septum and the conchae, and it continues laterally with the other meatuses.
In fact, the choanae represent a direct path from the nasal cavity into the nasophar-
ynx. They are bounded rostrally by the horizontal portion of the palatine bone, laterally
by the pterygoid bone and the perpendicular plate of the palatine bone, and caudally by
the vomer bone. Interestingly, there are no paranasal sinuses in the Arctocephalus australis
(Figure 2).
Figure 2. Lateral view of the left nasal cavity: (1) ventral nasal meatus; (2) choana; (3) nasopharynx;
(4) ventral nasal conchae with parallel folds (plicae parallelis); (5) middle nasal conchae; (6) dorsal
nasal conchae; (7) middle nasal meatus; (8) dorsal nasal meatus.
3.3. Pharynx
The pharynx is divided into the oropharynx, nasopharynx, and laryngopharynx. The
most noteworthy detail is the length of the soft palate, with a significant amount of peri-
pharyngeal soft tissue.
3.4. Larynx
The larynx is relatively short and wide (Figure 3). It is located underneath the skin, ven-
tral to the CI and CII vertebral body. It is dorsally related to the pharynx and the esophagus,
ventrally to the sternohyoid muscle, and laterally to the sternothyroid muscle and the man-
dibular gland. The cartilages are cricoid, thyroid, arytenoid, and epiglottis (Figure 4).
Figure 3. Larynx of Arctocephalus australis: (a) oblique view of the rostral larynx; (b) oblique view of
the caudal larynx.
Figure 3.
Larynx of Arctocephalus australis: (
a
) oblique view of the rostral larynx; (
b
) oblique view of
the caudal larynx.
Animals 2023,13, 199 5 of 15
Animals 2023, 13, x FOR PEER REVIEW 5 of 16
Figure 4. Larynx cartilaginous structure of Arctocephalus australis: (a) rostral view, (b) caudal-ventral
view, (1) epiglottis, (2) thyroid cartilage, (3) cricoid cartilages, (4) arytenoid cartilages.
3.5. Trachea
The trachea is a membranous and cartilaginous flexible duct that forms the proximal
part of the lower respiratory airways. It extends from the larynx to the tracheal bifurcation
(bifurcate tracheae). In young individuals, the trachea reaches the area below the sternal
manubrium. On the other hand, it does not go that far in adults. Additionally, in adults,
the trachea splits into two main bronchi (left and right) immediately cranial to the tip of
the manubrium (Figure 5a). In the South American fur seal, the trachea shows only a cer-
vical portion, whereas it is not possible to identify a thoracic portion. The tracheal length
average is around 8 cm in juveniles and 13 cm in adults, whereas the width in juveniles
has a value of approximately 2 cm and 3 cm in adults (Table 1).
Figure 4.
Larynx cartilaginous structure of Arctocephalus australis: (
a
) rostral view, (
b
) caudal-ventral
view, (1) epiglottis, (2) thyroid cartilage, (3) cricoid cartilages, (4) arytenoid cartilages.
3.5. Trachea
The trachea is a membranous and cartilaginous flexible duct that forms the proximal
part of the lower respiratory airways. It extends from the larynx to the tracheal bifurcation
(bifurcate tracheae). In young individuals, the trachea reaches the area below the sternal
manubrium. On the other hand, it does not go that far in adults. Additionally, in adults,
the trachea splits into two main bronchi (left and right) immediately cranial to the tip of the
manubrium (Figure 5a). In the South American fur seal, the trachea shows only a cervical
portion, whereas it is not possible to identify a thoracic portion. The tracheal length average
is around 8 cm in juveniles and 13 cm in adults, whereas the width in juveniles has a value
of approximately 2 cm and 3 cm in adults (Table 1).
Animals 2023, 13, x FOR PEER REVIEW 5 of 16
Figure 4. Larynx cartilaginous structure of Arctocephalus australis: (a) rostral view, (b) caudal-ventral
view, (1) epiglottis, (2) thyroid cartilage, (3) cricoid cartilages, (4) arytenoid cartilages.
3.5. Trachea
The trachea is a membranous and cartilaginous flexible duct that forms the proximal
part of the lower respiratory airways. It extends from the larynx to the tracheal bifurcation
(bifurcate tracheae). In young individuals, the trachea reaches the area below the sternal
manubrium. On the other hand, it does not go that far in adults. Additionally, in adults,
the trachea splits into two main bronchi (left and right) immediately cranial to the tip of
the manubrium (Figure 5a). In the South American fur seal, the trachea shows only a cer-
vical portion, whereas it is not possible to identify a thoracic portion. The tracheal length
average is around 8 cm in juveniles and 13 cm in adults, whereas the width in juveniles
has a value of approximately 2 cm and 3 cm in adults (Table 1).
Animals 2023, 13, x FOR PEER REVIEW 6 of 16
Figure 5. Dorsal view of the neck: (a) superficial view, (b) deeper view with the carotid sheath in
detail, (1) larynx; (2) trachea; (3) bronchi; (4) sternal manubrium; (5) thyroid gland; (6) carotid sheath
(opened); (7) common carotid artery; (8) vagosympathetic trunk; (9) internal jugular vein.
Table 1. Morphometric data of the trachea from the 11 individuals of Arctocephalus australis investi-
gated in the present study. A: adult; J: juvenile.
ID Age
Group Sex Length
(cm)
Width
(cm)
Lumen
Tracheal
Diameter
(cm)
Tracheal
Circumference
(cm)
N°
Cartilaginous
Rings
M9719 J F 6.9 1.6 1.2 5.4 12 + 1
M7419 J M 7.3 1.7 1.3 5.6 12 + 1
M7019 J M 7.8 1.9 1.4 5.9 13 + 1
M8419 J F 8 1.8 1.4 6 14 + 1
M8319 J M 8 2 1.5 6 13 + 1
M10019 J F 8.1 2 1.5 6.1 12 + 1
M7919 J M 8.3 2 1.5 6.2 12 + 1
M8219 J F 8.7 2.1 1.6 6.2 12 + 1
M10419 J M 9.1 2.2 1.7 6.2 12 + 1
M7319 A F 12.8 2.7 2.4 6.5 13 + 1
M9919 A F 14 3 2.5 6.7 12 + 1
Mean J - 8 1.9 1.5 6 12–14
Mean A - 13.4 2.9 2.5 6.6 12–14
As mentioned before, the trachea of the Arctocephalus australis has only a cervical por-
tion, practically in the midline (Figures 5 and 6). The common carotid artery, the internal
jugular vein, and the vagosympathetic trunk are included in the carotid sheath. The re-
current laryngeal nerve is located on the dorsolateral portions of the trachea, either close
to its dorsolateral side, in the cranial half of the neck, or close to its lateral side, in the
caudal half of the neck. (Figure 5b). The lobes of the thyroid gland and the small parathy-
roid glands are related to the lateral aspects of the cranial part of the trachea. The trachea
is also related to different lymphatic structures and to the external jugular vein, at the
thoracic entrance.
Figure 5.
Dorsal view of the neck: (
a
) superficial view, (
b
) deeper view with the carotid sheath in
detail, (1) larynx; (2) trachea; (3) bronchi; (4) sternal manubrium; (5) thyroid gland; (6) carotid sheath
(opened); (7) common carotid artery; (8) vagosympathetic trunk; (9) internal jugular vein.
Animals 2023,13, 199 6 of 15
Table 1.
Morphometric data of the trachea from the 11 individuals of Arctocephalus australis investi-
gated in the present study. A: adult; J: juvenile.
ID Age
Group Sex Length
(cm)
Width
(cm)
Lumen
Tracheal
Diameter
(cm)
Tracheal
Circumference
(cm)
N◦
Cartilaginous
Rings
M9719 J F 6.9 1.6 1.2 5.4 12 + 1
M7419 J M 7.3 1.7 1.3 5.6 12 + 1
M7019 J M 7.8 1.9 1.4 5.9 13 + 1
M8419 J F 8 1.8 1.4 6 14 + 1
M8319 J M 8 2 1.5 6 13 + 1
M10019 J F 8.1 2 1.5 6.1 12 + 1
M7919 J M 8.3 2 1.5 6.2 12 + 1
M8219 J F 8.7 2.1 1.6 6.2 12 + 1
M10419 J M 9.1 2.2 1.7 6.2 12 + 1
M7319 A F 12.8 2.7 2.4 6.5 13 + 1
M9919 A F 14 3 2.5 6.7 12 + 1
Mean J - 8 1.9 1.5 6 12–14
Mean A - 13.4 2.9 2.5 6.6 12–14
As mentioned before, the trachea of the Arctocephalus australis has only a cervical
portion, practically in the midline (Figures 5and 6). The common carotid artery, the
internal jugular vein, and the vagosympathetic trunk are included in the carotid sheath.
The recurrent laryngeal nerve is located on the dorsolateral portions of the trachea, either
close to its dorsolateral side, in the cranial half of the neck, or close to its lateral side, in
the caudal half of the neck. (Figure 5b). The lobes of the thyroid gland and the small
parathyroid glands are related to the lateral aspects of the cranial part of the trachea. The
trachea is also related to different lymphatic structures and to the external jugular vein, at
the thoracic entrance.
Animals 2023, 13, x FOR PEER REVIEW 7 of 16
Figure 6. Ventral view of the neck and the thorax (a) and the neck and thoracic and abdominal
cavities (b): (1) larynx; (2) trachea; (3) esophagus; (4) sternal manubrium; (5) thorax; (6) thyroid
gland; (7) main bronchi; (8) right lung; (9) left lung; (10) heart; (11) diaphragm.
There are 12–14 incomplete cartilaginous rings, U-shaped, that constitute the trachea
of the South American fur seal, plus one more as a transition between the trachea and the
bronchi (Table 1). Their dorsal part is free but attached by tracheal muscles that form the
dorsal part of the tracheal wall. It is known as the membranous portion (Figure 7).
Figure 7. Trachea section, ventral view: (1) cartilaginous rings; (2) membranous part.
The diameter of the tracheal lumen is 1.5 cm in juveniles and 2.5 cm in adults,
whereas the tracheal circumference is about 6 cm in the former and 6.8 cm in the latter
(Table 1).
3.6. Bronchi
As previously described, the trachea of the South American fur seal early bifurcates
into the two main bronchi at the level of the caudal third of the neck, practically at the
Figure 6.
Ventral view of the neck and the thorax (
a
) and the neck and thoracic and abdominal
cavities (
b
): (1) larynx; (2) trachea; (3) esophagus; (4) sternal manubrium; (5) thorax; (6) thyroid gland;
(7) main bronchi; (8) right lung; (9) left lung; (10) heart; (11) diaphragm.
There are 12–14 incomplete cartilaginous rings, U-shaped, that constitute the trachea
of the South American fur seal, plus one more as a transition between the trachea and the
Animals 2023,13, 199 7 of 15
bronchi (Table 1). Their dorsal part is free but attached by tracheal muscles that form the
dorsal part of the tracheal wall. It is known as the membranous portion (Figure 7).
Animals 2023, 13, x FOR PEER REVIEW 7 of 16
Figure 6. Ventral view of the neck and the thorax (a) and the neck and thoracic and abdominal
cavities (b): (1) larynx; (2) trachea; (3) esophagus; (4) sternal manubrium; (5) thorax; (6) thyroid
gland; (7) main bronchi; (8) right lung; (9) left lung; (10) heart; (11) diaphragm.
There are 12–14 incomplete cartilaginous rings, U-shaped, that constitute the trachea
of the South American fur seal, plus one more as a transition between the trachea and the
bronchi (Table 1). Their dorsal part is free but attached by tracheal muscles that form the
dorsal part of the tracheal wall. It is known as the membranous portion (Figure 7).
Figure 7. Trachea section, ventral view: (1) cartilaginous rings; (2) membranous part.
The diameter of the tracheal lumen is 1.5 cm in juveniles and 2.5 cm in adults,
whereas the tracheal circumference is about 6 cm in the former and 6.8 cm in the latter
(Table 1).
3.6. Bronchi
As previously described, the trachea of the South American fur seal early bifurcates
into the two main bronchi at the level of the caudal third of the neck, practically at the
Figure 7. Trachea section, ventral view: (1) cartilaginous rings; (2) membranous part.
The diameter of the tracheal lumen is 1.5 cm in juveniles and 2.5 cm in adults, whereas
the tracheal circumference is about 6 cm in the former and 6.8 cm in the latter (Table 1).
3.6. Bronchi
As previously described, the trachea of the South American fur seal early bifurcates
into the two main bronchi at the level of the caudal third of the neck, practically at the
sternal manubrium. The right and left main bronchi are in close contact with some of the
great thoracic vessels, such as the cranial vena cava or the aortic arch. The first branch is
the right main bronchus (Figure 8).
Animals 2023, 13, x FOR PEER REVIEW 8 of 16
sternal manubrium. The right and left main bronchi are in close contact with some of the
great thoracic vessels, such as the cranial vena cava or the aortic arch. The first branch is
the right main bronchus (Figure 8).
Figure 8. Polyurethane bronchial tree: (a) dorsal view; (b) ventral view; (1) trachea; (2) right main
bronchus; (3) left main bronchus; (4) right cranial lobar bronchus; (5) right mid lobar bronchus; (6)
right caudal lobar bronchus; (7) accessory lobar bronchus; (8) left cranial lobar bronchus; (9) left
caudal lobar bronchus.
After traveling about 8 cm in juveniles and about 14 cm in adults, a second bronchial
branch emerges. It is the right cranial lobar bronchus, which ventilates the cranial lobe of
the right lung. This right main bronchus continues traveling about 5 cm more, inside the
thoracic cavity, until the lung hilus, where the other three branches of the right main bron-
chus arise almost simultaneously.
The first of these three branches is the so-called right middle lobar bronchus, which
ventilates the middle lobe of the right lung. This bronchus extends throughout the entire
middle lobe, branching into several collateral bronchi (bronchi segmentalis). Immediately
after the right middle lobar bronchus, the caudal right lobar bronchus emerges, which
ventilates the caudal right lobe. The right accessory lobar bronchus appears practically at
the same level, which enters the accessory lobe of the right lung.
The left main bronchus gives rise only to two branches, both located at the level of
the pulmonary hilus. This second left bronchial generation arises to about 11 cm from the
tracheal bifurcation in juveniles and approximately 16 cm in adults, cranially to the triple
branching of the right main bronchus. The left main bronchus branches into two second-
ary bronchi: the left cranial bronchus and the left caudal bronchus. The left cranial
Figure 8.
Polyurethane bronchial tree: (
a
) dorsal view; (
b
) ventral view; (1) trachea; (2) right main
bronchus; (3) left main bronchus; (4) right cranial lobar bronchus; (5) right mid lobar bronchus;
(6) right caudal lobar bronchus; (7) accessory lobar bronchus; (8) left cranial lobar bronchus; (9) left
caudal lobar bronchus.
Animals 2023,13, 199 8 of 15
After traveling about 8 cm in juveniles and about 14 cm in adults, a second bronchial
branch emerges. It is the right cranial lobar bronchus, which ventilates the cranial lobe
of the right lung. This right main bronchus continues traveling about 5 cm more, inside
the thoracic cavity, until the lung hilus, where the other three branches of the right main
bronchus arise almost simultaneously.
The first of these three branches is the so-called right middle lobar bronchus, which
ventilates the middle lobe of the right lung. This bronchus extends throughout the entire
middle lobe, branching into several collateral bronchi (bronchi segmentalis). Immediately
after the right middle lobar bronchus, the caudal right lobar bronchus emerges, which
ventilates the caudal right lobe. The right accessory lobar bronchus appears practically at
the same level, which enters the accessory lobe of the right lung.
The left main bronchus gives rise only to two branches, both located at the level of
the pulmonary hilus. This second left bronchial generation arises to about 11 cm from the
tracheal bifurcation in juveniles and approximately 16 cm in adults, cranially to the triple
branching of the right main bronchus. The left main bronchus branches into two secondary
bronchi: the left cranial bronchus and the left caudal bronchus. The left cranial bronchus
ventilates the left cranial lobe, while the left caudal bronchus ventilates the left caudal lobe.
Each of these secondary branches divide further into tertiary bronchi or segmental bronchi,
which form the bronchioles (arbor alveolaris), ending in the alveolar sacs (Figure 8).
As mentioned before, the right main bronchus is slightly longer than the left one
(Figure 9), which means that it has more cartilaginous rings, between 16 and 18 until the
exit of the first branch of the right cranial bronchus, and another 7 or 8 more rings before the
triple branching described previously (Table 2). The left main bronchus has between 19 and
22 cartilaginous rings up to the region where it divides into the two left secondary bronchi
(Table 2). From this point, the diameter and width of the bronchi decrease accordingly
until the alveolar sacs (Table 2). The cross-sectional area of each bronchus is approximately
half of the tracheal area. Thus, the total cross-sectional area of the two primary bronchi is
practically equal to the cross-sectional area of the trachea.
Animals 2023, 13, x FOR PEER REVIEW 9 of 16
bronchus ventilates the left cranial lobe, while the left caudal bronchus ventilates the left
caudal lobe. Each of these secondary branches divide further into tertiary bronchi or seg-
mental bronchi, which form the bronchioles (arbor alveolaris), ending in the alveolar sacs
(Figure 8).
As mentioned before, the right main bronchus is slightly longer than the left one (Fig-
ure 9), which means that it has more cartilaginous rings, between 16 and 18 until the exit
of the first branch of the right cranial bronchus, and another 7 or 8 more rings before the
triple branching described previously (Table 2). The left main bronchus has between 19
and 22 cartilaginous rings up to the region where it divides into the two left secondary
bronchi (Table 2). From this point, the diameter and width of the bronchi decrease accord-
ingly until the alveolar sacs (Table 2). The cross-sectional area of each bronchus is approx-
imately half of the tracheal area. Thus, the total cross-sectional area of the two primary
bronchi is practically equal to the cross-sectional area of the trachea.
Figure 9. Ventral view of the lung: (a) right lung; (b) left lung; (1) trachea; (2) right main bronchus;
(3) right cranial lobar bronchus; (4) right mid lobar bronchus; (5) right caudal lobar bronchus; (6)
accessory lobar bronchus; (7) left main bronchus; (8) left cranial lobar bronchus; (9) left caudal lobar
bronchus.
Table 2. The morphometric data of the bronchi from the 11 individuals of Arctocephalus australis
investigated in the present study. A: adult; J: juvenile.
ID Age
Group Sex Length (cm) Width
(cm)
Lumen
Bronchus
Diameter (cm)
Bronchus
Circumference
(cm)
N° Cartilaginous
Rings
Right Left Right Left
M9719 J F 6.4 + 4.7 9.2 1.1 0.9 3.5–3.2 17 + 8 20
M7419 J M 6.8 + 5 9.5 1.1 1 3.7–3.5 18 + 8 22
M7019 J M 7 + 5 9.8 1.1 1 3.7–3.5 18 + 7 21
M8419 J F 7 + 5 10 1.1 1 3.7–3.5 16 + 7 19
M8319 J M 7.4 + 5.1 10.2 1.1 1 3.7–3.5 18 + 7 21
M10019 J F 8.4 + 5.2 10.6 1.1 1 3.8–3.6 17 + 8 20
M7919 J M 9 + 5.2 11 1.2 1.1 3.8–3.6 18 + 8 21
M8219 J F 9.3 + 5.4 11.8 1.2 1.1 3.9–3.7 16 + 7 20
Figure 9.
Ventral view of the lung: (
a
) right lung; (
b
) left lung; (1) trachea; (2) right main bronchus;
(3) right cranial lobar bronchus; (4) right mid lobar bronchus; (5) right caudal lobar bronchus;
(6) accessory lobar bronchus; (7) left main bronchus; (8) left cranial lobar bronchus; (9) left caudal
lobar bronchus.
Animals 2023,13, 199 9 of 15
Table 2.
The morphometric data of the bronchi from the 11 individuals of Arctocephalus australis
investigated in the present study. A: adult; J: juvenile.
ID Age
Group Sex Length (cm) Width
(cm)
Lumen
Bronchus
Diameter (cm)
Bronchus
Circumference
(cm)
N◦Cartilaginous
Rings
Right Left Right Left
M9719 J F 6.4 + 4.7 9.2 1.1 0.9 3.5–3.2 17 + 8 20
M7419 J M 6.8 + 5 9.5 1.1 1 3.7–3.5 18 + 8 22
M7019 J M 7 + 5 9.8 1.1 1 3.7–3.5 18 + 7 21
M8419 J F 7 + 5 10 1.1 1 3.7–3.5 16 + 7 19
M8319 J M 7.4 + 5.1 10.2 1.1 1 3.7–3.5 18 + 7 21
M10019 J F 8.4 + 5.2 10.6 1.1 1 3.8–3.6 17 + 8 20
M7919 J M 9 + 5.2 11 1.2 1.1 3.8–3.6 18 + 8 21
M8219 J F 9.3 + 5.4 11.8 1.2 1.1 3.9–3.7 16 + 7 20
M10419 J M 9.8 + 5.4 12.4 1.3 1.2 3.9–3.7 17 + 7 20
M7319 A F 13 + 6 15.9 1.4 1.3 4.1–3.9 17 + 8 21
M9919 A F 14 + 6.4 17.6 1.6 1.5 4.3–4 18 + 8 22
Mean J - 7.9 + 5 10.5 1.1 1 3.7 16–18 + 7/8 20–22
Mean A - 14 + 6.2 16.7 1.5 1.4 4.2 16–18 + 7/8 20–22
Width, lumen bronchus diameter, and bronchus circumference are equal in both bronchi, right and left.
3.7. Lungs
There are two lungs, one right and one left (Figure 10), that occupy the largest part of
the thoracic cavity (Figure 11). In the case of the South American fur seal, they approach
the level of the 9th rib. Each lung is covered by the pulmonary pleura and invaginated in
the ipsilateral pleural sac, to which it is attached by the pulmonary ligament. Inside this
pleural sac, the lung can move freely.
Animals 2023, 13, x FOR PEER REVIEW 10 of 16
M10419 J M 9.8 + 5.4 12.4 1.3 1.2 3.9–3.7 17 + 7 20
M7319 A F 13 + 6 15.9 1.4 1.3 4.1–3.9 17 + 8 21
M9919 A F 14 + 6.4 17.6 1.6 1.5 4.3–4 18 + 8 22
Mean J - 7.9 + 5 10.5 1.1 1 3.7 16–18 + 7/8 20–22
Mean A - 14 + 6.2 16.7 1.5 1.4 4.2 16–18 + 7/8 20–22
Width, lumen bronchus diameter, and bronchus circumference are equal in both bronchi, right and
left.
3.7. Lungs
There are two lungs, one right and one left (Figure 10), that occupy the largest part
of the thoracic cavity (Figure 11). In the case of the South American fur seal, they approach
the level of the 9th rib. Each lung is covered by the pulmonary pleura and invaginated in
the ipsilateral pleural sac, to which it is attached by the pulmonary ligament. Inside this
pleural sac, the lung can move freely.
Figure 10. Ventral view of the lungs, washed with water and filled with compressed air: (1) right
lung; (2) left lung.
Figure 11. Ventral view of the thoracic cavity of Arctocephalus australis: (1) left lung; (2) right lung;
(3) heart; (4) diaphragm.
The lungs of the Arctocephalus australis are divided into lobes by deep interlobar fis-
sures. In other words, these lungs show a well-defined lobulation, the patter of which is
as follows (Figure 12):
Figure 10.
Ventral view of the lungs, washed with water and filled with compressed air: (1) right
lung; (2) left lung.
The lungs of the Arctocephalus australis are divided into lobes by deep interlobar
fissures. In other words, these lungs show a well-defined lobulation, the patter of which is
as follows (Figure 12):
•
Right lung: It has four differentiated lobes, the first being the cranial lobe. Next, and
separated from the cranial lobe by a deep interlobar fissure, is the middle lobe, with an
elongated and pyramidal shape. Caudally to the middle lobe is the caudal lobe, with
an expanded fan-like shape. The Arctocephalus australis has a fourth lobe in the right
lung, the accessory lobe. It is located between both lungs, specifically in the caudal
Animals 2023,13, 199 10 of 15
mediastinum (Figure 12). Ventrally, this accessory lobe has a groove for the passage of
the caudal vena cava and the right phrenic nerve (Figure 13).
•
Left lung: The left lung shows one pair of lobes. The first is the cranial lobe, which has
an irregular surface. It is divided into two parts by a short fissure. The caudal lobe is
large and has scarce subdivisions. Interestingly, its shape is very similar to that of the
caudal right lobe (Figure 12).
Animals 2023, 13, x FOR PEER REVIEW 10 of 16
M10419 J M 9.8 + 5.4 12.4 1.3 1.2 3.9–3.7 17 + 7 20
M7319 A F 13 + 6 15.9 1.4 1.3 4.1–3.9 17 + 8 21
M9919 A F 14 + 6.4 17.6 1.6 1.5 4.3–4 18 + 8 22
Mean J - 7.9 + 5 10.5 1.1 1 3.7 16–18 + 7/8 20–22
Mean A - 14 + 6.2 16.7 1.5 1.4 4.2 16–18 + 7/8 20–22
Width, lumen bronchus diameter, and bronchus circumference are equal in both bronchi, right and
left.
3.7. Lungs
There are two lungs, one right and one left (Figure 10), that occupy the largest part
of the thoracic cavity (Figure 11). In the case of the South American fur seal, they approach
the level of the 9th rib. Each lung is covered by the pulmonary pleura and invaginated in
the ipsilateral pleural sac, to which it is attached by the pulmonary ligament. Inside this
pleural sac, the lung can move freely.
Figure 10. Ventral view of the lungs, washed with water and filled with compressed air: (1) right
lung; (2) left lung.
Figure 11. Ventral view of the thoracic cavity of Arctocephalus australis: (1) left lung; (2) right lung;
(3) heart; (4) diaphragm.
The lungs of the Arctocephalus australis are divided into lobes by deep interlobar fis-
sures. In other words, these lungs show a well-defined lobulation, the patter of which is
as follows (Figure 12):
Figure 11.
Ventral view of the thoracic cavity of Arctocephalus australis: (1) left lung; (2) right lung;
(3) heart; (4) diaphragm.
Animals 2023, 13, x FOR PEER REVIEW 11 of 16
• Right lung: It has four differentiated lobes, the first being the cranial lobe. Next, and
separated from the cranial lobe by a deep interlobar fissure, is the middle lobe, with
an elongated and pyramidal shape. Caudally to the middle lobe is the caudal lobe,
with an expanded fan-like shape. The Arctocephalus australis has a fourth lobe in the
right lung, the accessory lobe. It is located between both lungs, specifically in the
caudal mediastinum (Figure 12). Ventrally, this accessory lobe has a groove for the
passage of the caudal vena cava and the right phrenic nerve (Figure 13).
• Left lung: The left lung shows one pair of lobes. The first is the cranial lobe, which
has an irregular surface. It is divided into two parts by a short fissure. The caudal
lobe is large and has scarce subdivisions. Interestingly, its shape is very similar to
that of the caudal right lobe (Figure 12).
Figure 12. Lungs of Arctocephalus australis: (a) dorsal view; (b) ventral view; (1) right cranial lobe;
(2) right middle lobe; (3) right caudal lobe; (4) right accessory lobe; (5) left cranial lobe; (6) left caudal
lobe.
Figure 12.
Lungs of Arctocephalus australis: (
a
) dorsal view; (
b
) ventral view; (1) right cranial lobe;
(2) right middle lobe; (3) right caudal lobe; (4) right accessory lobe; (5) left cranial lobe; (6) left
caudal lobe.
Animals 2023,13, 199 11 of 15
Animals 2023, 13, x FOR PEER REVIEW 12 of 16
Figure 13. Detail of the groove formed by the accessory lobe for the passage of the caudal vena cava
and the right phrenic nerve.
The different parts of both lungs can be described as follows:
1. Base, or diaphragmatic surface of the lung: It is concave as it overlaps the convex
thoracic surface of the diaphragm. It is limited by the basal border.
2. Apex: It is free, sharpened, and laterally flattened. It fills the space of the pleural
dome.
3. Two surfaces: (A) The costal surface: Lateral, larger, smooth, and convex. It is in con-
tact with the inner surface of the lateral thoracic wall. (B) The medial surface: It is
smaller than the costal and is related to the mediastinum and the mediastinal struc-
tures. It presents a deep depression formed by the heart and its pericardium, the car-
diac impression. The cardiac impression is deeper in the left lung (Figure 14).
Figure 14. Detail of the cardiac impression in the left lung.
4. Three distinct borders (ventral, dorsal, and basal): (A) Ventral border: It is sharp and
irregular. It occupies the costomediastinic sinus and presents the cardiac notch. The
ventral border of the left lung is slightly greater than the one of the right lung (Table
3). (B) Basal border: The basal border separates the base (or diaphragmatic surface)
from the costal and medial surfaces. As in the case of the ventral border, the basal
Figure 13.
Detail of the groove formed by the accessory lobe for the passage of the caudal vena cava
and the right phrenic nerve.
The different parts of both lungs can be described as follows:
1.
Base, or diaphragmatic surface of the lung: It is concave as it overlaps the convex
thoracic surface of the diaphragm. It is limited by the basal border.
2. Apex: It is free, sharpened, and laterally flattened. It fills the space of the pleural dome.
3.
Two surfaces: (A) The costal surface: Lateral, larger, smooth, and convex. It is in
contact with the inner surface of the lateral thoracic wall. (B) The medial surface:
It is smaller than the costal and is related to the mediastinum and the mediastinal
structures. It presents a deep depression formed by the heart and its pericardium, the
cardiac impression. The cardiac impression is deeper in the left lung (Figure 14).
4.
Three distinct borders (ventral, dorsal, and basal): (A) Ventral border: It is sharp and
irregular. It occupies the costomediastinic sinus and presents the cardiac notch. The
ventral border of the left lung is slightly greater than the one of the right lung (Table 3).
(B) Basal border: The basal border separates the base (or diaphragmatic surface) from
the costal and medial surfaces. As in the case of the ventral border, the basal border of
the left lung has a greater extension than in the right lung (Table 3). (C) Dorsal border:
It is thick and rounded. It forms the dorsal boundary between the costal surface and
the medial surface. Contrary to what happens in the ventral and basal borders, the
dorsal border of the right lung is the one with a greater length (Table 3).
Table 3.
Morphometric data of the lungs from the 11 individuals of Arctocephalus australis investigated
in the present study. A: adult; J: juvenile.
ID Age
Group Sex
Length (cm) Maximum Width
Dorsal Border Ventral Border Basal Border (cm)
Right Left Right Left Right Left Right Left
M9719 J F 20.1 19.3 12.8 13.9 10.7 13.6 12.6 11.3
M7419 J M 20.5 20 13 14.3 11 14 12.9 11.8
M7019 J M 21.6 21 13.4 15 11.3 15.3 13.2 12.1
M8419 J F 22.6 21.3 13.7 15.5 11.6 15.5 14 12.8
M8319 J M 23.3 22 14.2 16.3 11.9 15.7 14.3 13
M10019 J F 24 22.9 14.7 16.5 12.1 16.3 14.5 13.4
M7919 J M 25.8 24.2 15 16.7 12.6 16.7 15.1 13.8
M8219 J F 27.7 26 16.8 18.2 13.7 17.7 16.4 15.2
M10419 J M 28 26.2 17.2 19 14.1 18 18 16.7
M7319 A F 33 30.5 23.5 25.7 19.6 24.5 24 22.6
M9919 A F 35 32.7 24.5 26.3 20.1 25 24.7 23
Mean J - 23.7 22.5 14.5 16.1 12.1 15.8 14.5 13.3
Mean A - 34 31.6 24 26 19.8 24.7 24.3 22.8
Animals 2023,13, 199 12 of 15
Animals 2023, 13, x FOR PEER REVIEW 12 of 16
Figure 13. Detail of the groove formed by the accessory lobe for the passage of the caudal vena cava
and the right phrenic nerve.
The different parts of both lungs can be described as follows:
1. Base, or diaphragmatic surface of the lung: It is concave as it overlaps the convex
thoracic surface of the diaphragm. It is limited by the basal border.
2. Apex: It is free, sharpened, and laterally flattened. It fills the space of the pleural
dome.
3. Two surfaces: (A) The costal surface: Lateral, larger, smooth, and convex. It is in con-
tact with the inner surface of the lateral thoracic wall. (B) The medial surface: It is
smaller than the costal and is related to the mediastinum and the mediastinal struc-
tures. It presents a deep depression formed by the heart and its pericardium, the car-
diac impression. The cardiac impression is deeper in the left lung (Figure 14).
Figure 14. Detail of the cardiac impression in the left lung.
4. Three distinct borders (ventral, dorsal, and basal): (A) Ventral border: It is sharp and
irregular. It occupies the costomediastinic sinus and presents the cardiac notch. The
ventral border of the left lung is slightly greater than the one of the right lung (Table
3). (B) Basal border: The basal border separates the base (or diaphragmatic surface)
from the costal and medial surfaces. As in the case of the ventral border, the basal
Figure 14. Detail of the cardiac impression in the left lung.
The maximum width of both lungs is also different, and the values of the right side
are slightly lower (Table 3).
4. Discussion
Marine mammals, which live most of their lives in the ocean or in an aquatic environ-
ment, have typical characteristics of all mammals. Thus, in the case of their respiratory
system, it also consists of the same parts, starting with the nose and nares and ending with
the lungs.
It is important to remark that, in general terms, knowledge of anatomy helps to un-
derstand any physiological phenomenon. Surprisingly, and although they could provide
key insights into physiological responses to dive, in the case of the
Arctocephalus australis
,
previous reports on the anatomy of its respiratory system are scarce [
2
]. For example,
the depths to which these animals can dive and the length of time they remain sub-
merged have intrigued researchers for decades. Unlike what happens with land mam-
mals,
Arctocephalus australis
has enough oxygen to perform long dives and is able to avoid
pressure-related diseases from repetitive and deep diving. The question that arises is if
there are anatomical differences between its respiratory apparatus and that of dogs, as
a typical model of land-mammal, or if on the contrary, this species is able to live in the
water environment without special anatomical adaptations.
As mentioned before, the respiratory apparatus of the South American fur seal starts
with the nose and the nares. The nares have a greater mobility compared to other mammal
species with similar nose physiognomy. They can intentionally be totally closed or even
expand to double their size as compared to resting conditions [
5
]. Thus, the South American
fur seal has the ability to open or close the nares as if they were valves to avoid a massive
water uptake through the airways while diving. Additionally, they can increase the air
expelled per unit time when approaching the surface [
5
]. In addition, contrary to what
happens in other mammals such as the dog, the philtrum divides the nasal plane partially,
as it does not reach the upper lip [
6
]. The nasal septum is also significantly shorter than
in dogs or cats [
6
], which facilitates different pathologies affecting the upper respiratory
tracts [28]. On the contrary, the nasal cartilage is similar to that of the dog [6].
There are four groups of bone cavities connected to the nasal cavity in land mammals:
the paranasal sinuses. These sinuses act synergistically with the nasal cavity to warm and
humidify the inhaled air during breathing. Pinnipeds, other marine mammals, have lost
Animals 2023,13, 199 13 of 15
these paranasal sinuses due to the high pressures they face under water. These structures
are too fragile to resist these high pressures. Thus, in the case that these structures re-
mained in pinnipeds, they would fracture easily [
18
]. As in phocids, the soft palate of the
Arctocephalus australis is much longer than that of the dog, with a significant amount of
peripharyngeal soft tissue. This anatomical characteristic is of great clinical interest, taking
into consideration the difficulties these marine species have for intubation [
29
]. In contrast,
the larynx of the South American fur seal is practically like that of other carnivores [
6
].
Thus, the laryngeal cartilages are similar in shape and size to those of the dog.
As shown by other authors, tracheal length is directly related to the need of determined
speed air flows. When analyzing the functional implications of this fact, it is important to
compare the tracheal width to its length, since the ability to exchange large air volumes per
unit time is directly related to the absolute diameter/length ratio [
25
]. This seems to be the
reason why cetaceans have short and wide tracheas with a large pulmonary ventilations
volume (80–90%) in shorter time, which is the opposite of what happens in land-carnivores,
as these species do not have this need [
2
]. The Arctocephalus australis trachea is longer than
in cetaceans, with an early bifurcation, but it is shorter than that in dogs and cats. This
anatomical difference is probably related to its diving adaptation and its distinct ventilation
need in comparison to other marine species [30].
Mammals show variations in the bronchial branching pattern, which is of great impor-
tance when analyzing their functional implications. Thus, their bronchial tree consists of
a sequence of branches, whose number, generation, and distribution vary according to the
different mammalian species. In summary, the branching pattern is similar to that in the
dog [31,32].
As previously shown in these species, the cross-sectional area of each bronchus is
approximately half of the tracheal area. Thus, the total cross-sectional area of the two
primary bronchi is practically equal to the cross-sectional area of the trachea [
2
]. According
to our results, this is also the case for the Arctocephalus australis, which, due to the early
bifurcation of its trachea, has extremely long bronchi in comparison to other species of land
mammals [6,7].
Interestingly, the Arctocephalus australis bronchial tree shows differences compared to
other marine mammals, such as certain dolphin species. These animals have developed
a third bronchus or tracheal bronchus. This bronchus ventilates the most cranial part of the
right lung, independently of the main right bronchus entry [26,27].
The explanation could be in the South American fur seal lifestyle, as this species
alternates land and water environments. They do not need rapid ventilation, as is the case
in cetaceans, and neither live constantly on land. This could also be the reason why the
Arctocephalus australis has a short trachea and long bronchi, especially when compared to
land mammals, whose ventilation demands are different [25].
Concerning the lungs, our results showed that the lobulation pattern is very similar to
that in other species of land mammals, such as the dog or the cat [
6
,
7
]. Surprisingly, the
lungs of the South American fur seal are different from those of cetaceans, which show
unilobed lungs [
25
,
26
,
33
]. This could be related to the ability of these species to mobilize
large volumes of air at high speeds in short intervals of time; meanwhile, pinnipeds do not
have that need as they spend more time on land [33].
As it has been previously shown, the lung lobulation of land mammals, with a greater
absorption surface, is able to better bear internal impacts during terrestrial locomotion [
26
].
We think that this could be the case for the South American fur seal. However, as in other
species of marine mammals, the lung microanatomy of this species has thicker and firmer
connective tissue partitions in comparison to land mammals, which is a clear adaptation to
the aquatic environment. This greater development of the septa forms a more rigid and
resistant lung support stroma, giving the parenchyma a greater resistance to lung collapse
that could occur during diving [2].
Animals 2023,13, 199 14 of 15
In summary, the lungs of the South American fur seal show their own differential
characteristics, as they are a mixture of those of other mammal species, either marine
or terrestrial
5. Conclusions
The anatomical characteristics of the South American fur seal’s respiratory apparatus
are very similar to those observed in other land-carnivores, such as the dog.
Nevertheless, this species exhibits several differences with other land-carnivores, of
course resulting from their diving ability. Examples of this are its capacity to open or close
the nares and the early bifurcation of the trachea, which does not have a thoracic portion.
There are also interesting differences between the lungs of the South American fur
seal and other marine mammals, which is probably related to their different lifestyle and
ventilation demands.
The conclusion is that, besides these differences, being a carnivore seems to be the
critical characteristic defining the respiratory apparatus of the South American fur seal,
even though there are clear differential anatomical details to facilitate its adaptation to the
aquatic environment.
Author Contributions:
Conceptualization, I.M.-D., R.M.-O. and J.G.-S.; methodology, J.G.-S. and
R.M.-O.; data collection and validation, I.M.-D., C.T.-M., J.-P.L. and E.T.-D.; formal analysis,
I.M.-D.
,
R.M.-O. and J.G.-S.; writing—original draft preparation, I.M.-D., I.S.-Á. and P.P.-L.; writing—review
and editing, J.G.-S., R.M.-O. and I.S.-Á.; supervision, I.M.-D., R.M.-O. and J.G.-S.; project administra-
tion, J.-P.L., I.M.-D., C.T.-M. and E.T.-D.; funding acquisition, J.-P.L. All authors have read and agreed
to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement:
Ethical review and approval were waived for this study by
Fundación Mundo Marino, authorizing the use of several cadavers for an anatomical study.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Acknowledgments:
Authors thank Fundación Mundo Marino for the use of its facilities and equip-
ment to carry out this work.
Conflicts of Interest: The authors declare no conflict of interest.
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