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Comparative Respiratory System
Comparative Respiratory System
Open Access
Comparative Physiology of the Respiratory System in the Animal
Kingdom
Olga Carvalho* and Carlos Gonalves
Institute of Histology and Embryology, Medicine Faculty, University of Coimbra, Rua Larga, 3004-504 Coimbra,
Portugal
Abstract: The inconstant environment in which animals lives and the variation of their metabolic states determined the
gas exchangers system that must be able to operate efficiently across a spectrum of conditions that range from resting to
exercise and even under hypoxia. The primordial respiratory organs that evolved for water breathing were the gills,
evaginated gas exchangers, whereas for terrestrial air breathing developed a invaginated gas exchangers, the lungs.
Specialized organs evolved for animals that can extract oxygen from water and air, consider as a transitional breathing (or
bimodal). From amphibians to mammals, it is possible to verify that the dimensions of their respiratory units are being
increasingly smaller and the number per unit of lung volume increases. The evolution of the vertebrate respiratory system
achieved its most efficient state in birds, with their constant volume parabronchial lungs and their highly compliant air
sacs with low pressure ventilation that, enabling them to sustained flapping flight. In contrast, the mammalian broncho-
alveolar lungs, with their mandatory high-pressure ventilation and great volume changes, allowed the development of
adaptations that favour, for example, a highly mobile trunk for high velocity running predators or to live in a deep-sea.
Keywords: Respiratory system, lung development, morphology, alveoli.
in a single evolutionary line, the cyanobacteria, after the In all vertebrates, at a certain stage of their development,
origin of aerobic respiration [7]. arise bilaterally in craneo-caudal direction from the inner
side of the pharynx, a series of diverticula, which evaginate
The rise of atmospheric oxygen caused by photosynthetic
towards the outer surface, forming the pharyngeal pouches
activity of evolving cyanobacteria must have created a
remarkably strong selective pressure on organisms in both [16, 17]. The number of pharyngeal pouches is greater in
lower vertebrates, reaching fourteen in cyclostomes and only
domains. Adaptations to use the new, chemically superior,
four or five in birds and mammals. The pharyngeal pouches
electron receptor might have taken place, with similar
are separated by masses of mesenchyme that have the
molecular solutions creating the oxygen-reducing active
designation of pharyngeal arches, in which is located an
sites. This would mean that the aerobic respiration has a
arterial structure, called the aortic arch, which extends from
single origin and may have evolved before the oxygen was
released to the atmosphere by photosynthetic organisms and the ventral aorta to the dorsal aorta [16, 17].
that the appearance of aerobic respiration was polyphyletic During the ontogenesis of higher vertebrates, the pharyn-
[7]. geal pouches fail to open to the outside, contrarily to what
happens in fish and, temporarily, in amphibians. Thus, in
This new and more profitable method of extracting
higher vertebrates, the pharyngeal pouches just remain
energy, aerobic respiration, should have led to a domain of
aerobic organisms in the biological community, and prob- during the embryonic period, where they undergo several
changes, but very few or none of their initial characteristics
ably even leading to the extinction of some anaerobic
are presented in adults. In amniotes, as in humans, only the
organisms [8, 9].
first pair of pharyngeal pouches remains, giving origin
The evolution to multicellular organisms determined the bilaterally, the eustachian tube and middle ear [16, 17].
appearance of more sophisticated and specialized systems for
the gas exchange, in order to develop an effective system of
exchange. The existence of multicellular organisms, led to RESPIRATORY SYSTEM IN FISH
rapid and progressive morphofunctional differentiation of The fish gill adapted a structure for extraction of oxygen
groups of cells that became the precursors of tissues, organs from water that is formed by a large number of filaments
and systems currently present in more complex organisms. spaced out along the gill arches on either side of the pharynx.
In most cases, this cellular specialization does not imply the Each filament has a series of plates projecting at right angles
loss of genetic material but only changes in the genes from its upper and lower surfaces, the secondary lamellae,
expression [9, 10]. which are extremely numerous, are the site of gaseous
The respiratory systems from different groups of animals, exchange and form a fine sieve which ensures that all the
although morphologically different, have in common the water comes into close contact with the blood [2, 18].
following characteristics: they have a large capillary The gills are multifunctional organs that are responsible
network, the gas exchange surfaces are thin and moist; for the gas exchange (respiration) but also for the osmoregu-
constant renewal of oxygen-rich fluid (air or water) order to lation, acid-base regulation, and excretion of nitrogenous
provide oxygen and remove carbon dioxide; free movement waste [18, 19].
of blood within the capillary network [11, 12]. According to
Atwood, the assumptions stated above, are present either The epithelial surface of a gill arch is structurally and
external respiration is carried out by 1) cutaneous diffusion functionally zoned [2]. The filaments are covered by two
(earthworm and some amphibians), 2) by thin tubes called distinct epithelial surfaces, the lamellar and filament epithe-
tracheae (some insects); 3) by gills, the respiratory system of lia, also termed the secondary and primary epithelia respect-
fish or 4) by diffusion through the lungs, respiratory organs ively [20]. Gas exchange occurs through the secondary
present in amphibians, reptiles, birds and mammals [13]. lamellae, and the non-respiratory functions of the gills take
place in the primary epithelium [2].
The primary epithelium contains the chloride cells, which
RESPIRATORY ORGANS IN VERTEBRATES
vary in morphology and number according to the milieu
The steps of the evolution of terrestrial vertebrates are: where the fish lives. The presence of an accessory cell beside
change from anaerobic to aerobic life, accretion of unicells the chloride cell is characteristic of seawater or seawater-
into multicellular organs, formation of a closed circulatory adapted fish [20]. The secondary epithelium that covers the
system, evolution of metal-based carrier pigments that imp- free part of the secondary lamellae has an exclusive
roved oxygen up-take, formation of invaginated respiratory relationship with the arterioarterial vasculature, i.e., the pillar
organs, physical translocation from water to land, develop- cells. This epithelium consists of an outermost layer of pave-
ment of a double circulation and progression from ectother- ment cells that exhibits structural characteristics suggestive
mic-heterothermy to endothermic-homeothermy [14]. of cell coat secretion and an innermost layer of less diffe-
rentiated cells. In contrast to the primary epithelium, the
In vertebrates, the blood performs the task of transporting
secondary epithelium does not exhibit any obvious diffe-
oxygen to the cells and carbon dioxide to the external
rences between freshwater and seawater fish [20].
environment [15].
The development of the respiratory organs of vertebrates The lamellar structure helps to increase the surface area
but depends on the following complex anatomy to maintain
is closely related to the primitive pharynx, since the gills of
the flat space necessary for circulation: separation between
aquatic vertebrates and the lungs of terrestrial vertebrates
epithelial sheets (by pillar cells) and connection between the
and aquatic mammals have pharyngeal embryology origin
[16, 17].
Comparative Physiology of the Respiratory System in the Animal Kingdom The Open Biology Journal, 2011, Volume 4 37
basal lamina of epithelial sheets by groups of strands of the apical membrane of chloride cells which precludes
(collagen columns) [21]. their absolute identification [19].
To prevent ballooning and to ensure the sheet-flow They are located in the primary epithelium in close
dynamics of blood, the two layers of respiratory epithelium proximity to the blood vessels [2, 19] and are sites of active
are connected by many strands of extracellular matrix chloride secretion and high ionic permeability [28],
(ECM) materials, which are called collagen columns [21]. performing an integral role in acid-base regulation [19]. As
These columns, made of collagen fibers, are essential for in other vertebrates, fish must maintain homeostasis of intra
reinforcing the lamellae structure and the internal force of and extracellular pH and therefore use the parallel strategies
blood pressure [21]. Since collagen triggers the coagulation of buffering and excretion to defend against pH changes
cascade when exposed to blood, the collagen columns are [29]. During alkalosis conditions, the area of exposed
surrounded by the plasma membrane of pillar cells, which chloride cells is increased, which serves to enhance base
isolate them from circulation [22, 23]. equivalent excretion as the rate of Cl-/ HCO3- exchange is
increased. Conversely, during acidosis, the chloride cells
In the interface between pillar cells and collagen col-
surface area is diminished by an expansion of the adjacent
umns, exist adhesion junctions termed as column junctions
pavement cells, and this response reduces the number of
and autocelullar junctions, both of which are essential con-
stituents of the gill lamellae [24]. The column junctions is functional Cl-/HCO3- exchangers [19].
a cell-ECM adhesion and autocelullar junctions a mem- Under softwater or toxic conditions, chloride cells prolif-
brane-membrane adhesion, both involved in maintaining erate on both surfaces of the gill and might impair gas
structural integrity and hemodynamic of branchial lamellae transfer owing to a thickening of the lamellar blood-to-water
[24]. diffusion barrier [19].
The pillar cells have a spool-shape and possess a cylin- Water enters through the fish's mouth and out through the
drical cell body connecting two parallel sheets of respiratory gill, slits in a direction that is opposite to the blood flow in
epithelium [22, 23]. They also enfold 5 to 8 collagen the gill, providing a constant renewal of the oxygen supply
columns and have numerous myofilaments, parallel to the in contact with the respiratory organ [18, 30].
collagen columns, which consist of actin [21, 25] and
The exchange of oxygen and carbon dioxide takes place
myosin [21], which form the contractile apparatus of the cell. by diffusion from the surrounding water and the blood that
The pillar cells are a type of endothelial cells that flows within the capillary network of the gills, and because
delimits a network of vascular compartments within the of this countercurrent flow fish can extract 80 to 90% of
lamellae of gill fish, but since they share characteristics with dissolved oxygen in water [30].
smooth muscle cells, we can say that these cells are
During the larval development of fish, the teleosts in
specialized vascular cells with characteristics of both particular, the skin is the cutaneous surface that ensures gas
endothelial and smooth muscle cells [21].
exchange, and only in the final stage of this period begins the
The contractile apparatuses of the pillar cells possibly hematosis through the gills [31], when the muscle-skeleton
prevent collagen columns from being stretched and provide structure of the oral cavity becomes able to coordinate food
plasticity to the vascular network of the lamella against intake with the flow of water through the branchial system
changes in blood pressure [21]. Other possible function for [32].
the contractile structures of the pillar cells is that they can
change the diameter of the vascular channels, and therefore Lungfishes
contribute to the regulation of blood flow through the
lamellae [2, 21]. Changing conditions of life imposed new requirements
on the morphology and physiology of the organisms. One of
Besides the pillar cells, the gill epithelium of freshwater these changes is the evolutionary transition from aquatic to
fishes have pavement cells (also termed as respiratory cells terrestrial life, leading to adaptations in locomotion, breath-
in older literature), mucus cells, neuro-epithelial cells and ing, hearing, mechanism for food capture and other func-
chloride cells [20]. tions (Fig. 1).
The neuroepithelial cells are isolated or clustered on the The first air-breathing vertebrates were fishes, and a
internal side of the primary lamellae facing the respiratory Devonian air-breathing sarcopterygian (lobefin) occupies the
water flow [26]. They are probably involved in local and basal position in the lineage extending from the Paleozoic
central modulation of the branchial functions by interacting fishes to the most derived tetrapods [33, 34].
with the branchial nervous system and by paracrine secretion
of substances such as serotonin [27]. These cells share The evolution of tetrapods from sarcopterygian fish is
several morphofunctional features with the cells of the one of the major transformations in the history of life and
neuroepithelial bodies in the lungs of air-breathing involved numerous structural and functional innovations.
vertebrates [26, 27]. The Styloichthys changae, one fossil of sarcopterygian fish,
exhibits the character combination in a stem group close to
The chloride cells are described as large, granular, the last common ancestor of tetrapods and lungfish [35].
acidophilic and mitochondria-rich cells [28] and exhibit an
extensive tubular system emanating from the basolateral The recent discovery of a well-preserved species of fossil
membrane, an array of sub-apical vesicles, large ovoid sarcopterygian fish form in the late Devonian of Artic
nucleus and abundance of Na+, K+ -ATPase enzyme [19]. Canada, that represents an intermediate between fish with
There is a marked difference between species in the structure fins and tetrapods with limbs, provides unique insights into
38 The Open Biology Journal, 2011, Volume 4 Carvalho and Gonalves
how and in what order important tetrapod characters arose suggesting that even in this primitive lung, these proteins are
[36]. The morphological features and geological setting of still involved in surfactant homeostasis [40].
this new animal are suggestive of life in shallow-water,
To breathe air the Neoceratodus may rise to surface,
marginal and subaerial habitats [36].
exhale through the mouth, inhale and dive forward or rise to
The relevance of the extant air-breathing fishes as models the surface, breathe and reverse back into the water [39].
for events in the Paleozoic has been a recurring theme for Protopterus and Lepidosiren are bimodal breathers, that
more than one century. The lungfish is considered homo-
use both gills and lungs for respiratory gas transfer, but they
logous to the lungs of all higher vertebrates and the precursor
are obligate breathers because they die if denied access to air
of the enteleost gas bladder [34, 37].
[43, 42]. The Protopterus occupy a variety of habitats both
In our days the lungfish are represented by three genera, lentic (standing water) and lotic (running water) [43] and
the Australian lungfish, Neoceratodus forsteri, and the other possess the capacity to aestivate, reducing their metabolic
two genera: the African (Protopterus) and South American rate, which allow them to survive to extreme heat or for long
(Lepidosiren) lungfish [38]. dry periods [43-45]. In the Protopterus, the gills and skin
uptake only 10% of the total O2 uptake and these structures
The Australian Neoceratodus differ from the other
are much more effective in removing the CO2 [46].
lungfish because they breathe air for short periods and for
this reason the lung is an accessory organ which is only used The reedfish Calamoichthys calabaricus is one of the
during periods of high activity in its natural habitat [39, 40]. phylogenetically most primitive extant air-breathing fishes,
They have efficient gills and possess only a single lung, and represents an animal successfully adapted not only for
unlike both Protopterus and Lepidosiren which have paired air breathing but also for making short-term use of terrestrial
lungs and much reduced gills [41, 42]. environments. In this primitive living actinopterygian fish
the oxygen uptake is achieved by the gills, skin and a paired
The lung of N. forsteri consists of a single elongated
chamber compartmentalized by a thick cartilaginous struc- lungs and in the total volume oxygen uptake, the lungs
account for 40%, the gills 28%, and the skin 32% [47].
tural framework [40]. The epithelial lining of these support-
ing structures comprised abundant capillaries interspersed In the Lepidosiren 99.15% of the total diffusing capacity
with cells resembling alveolar type II and type I cells. These lies in the lungs, 0.85% in the skin and only an insignificant
epithelial cells which appear to be the only cell type lining 0.0013% in the gills, which shows that the gills dont have
the gas-diffusing surface [40], have long cytoplasmic plates any importance as a gas exchange organ in this species.
bearing microvilli, which form part of the gas-exchange Oxygen uptake is accomplished by the lungs and dioxide
membrane. The cells contain large numbers of osmiophilic carbon is eliminated by the skin [48].
bodies resembling mammalian lamellar bodies, and it is
The structure of the gills lamellae of Lepidosiren consists
possible that these lungfish cells may be the common
of a stratified epithelium that rests on the basal membrane
ancestral cell for the alveolar type I and II found in the
and has at least three layers of cuboidal cells with large
mammalian lung [40]. They also have a surfactant-like nuclei. Close to the epithelium there are numerous capillaries
material containing both SP-A and SP-B like proteins,
[48].
Comparative Physiology of the Respiratory System in the Animal Kingdom The Open Biology Journal, 2011, Volume 4 39
Each lung of these lungfish has a main duct and were similar to those commonly encountered in tropical
numerous chambers of different sizes, which decrease in size lowland habitats during dry seasons [51].
as they progress caudally. The honeycomb-like edicular
The sequence of evolution begun with sarcopterygian
parenchyma is disposed in these chambers and most cham-
fish, followed by the appearance of a prototetrapods (e.g.
bers contain a central lumen, which connects with the air
Elginerpeton), the emergence of aquatic tetrapods (e.g.
duct. The duct, the chambers and edicular parenchyma
Acanthostega), the appearance of eutetrapods (e.g.
consist of connective tissue septa held upright by smooth Tulerpeton) and the first truly terrestrial tetrapods (e.g.
muscular/elastic trabeculae and are supplied and drained by
Pederpes) in the lower Carboniferous [49]. Several morpho-
branches of the pulmonary artery and vein. Most interedi-
logical changes were observed during the evolution process,
cular septa have a double capillary net. The air-blood barrier
developing specialized features that allowed land locomotion
consists of three layers: a simple squamous epithelium made
and air breathing (Fig. 2) [49].
up of a single type of cell, the endothelial cells of the blood
capillaries and the combined basal lamina of the epithelial The sudden change from gill respiration to lung breathing
and endothelial cells [48]. would pose considerable physiological problems. One of the
consequences of gill loss, would be the concentration of
The skin of these fish has two layers, the epidermis and respiratory CO2 within the body, which required buffering
the dermis. The epidermis consists of a stratified epithelium by bicarbonate ion and affected processes such as acid-base
with six to ten layers of diverse cell types. Most prominent balance, O2 binding by haemoglobin, ventilation rate, res-
are superficially located cuboidal cells with a large central piratory control and also affected nitrogen excretion, ion
nucleus and the mucous cells that are dispersed among the regulation and water balance, vital processes that would need
other cell layers. The dermis is a dense connective tissue, to be assumed by others organs.
with blood vessels and small ossified scales. Numerous
blood capillaries and melanophores lie beneath the basal The advantages of tetrapod gill loss included head
membrane and between the subjacent layers [48]. mobility, development of hearing and the origin of different
ventilatory and feeding mechanisms [49, 50].
In the Protopterus and Lepidosiren the ventilation of the
gills occurs through the action of a positive pressure buccal In the primitive pure buccal pumping, found in most air-
pump anterior to the gills and an opercular suction pump breathing fishes, including lungfishes, the axial musculature
posterior to the gills. These pumps generate a nearly conti- does not contribute to expiration or inspiration. In fact, the
nuous water pressure gradient favouring a water flow in the buccal pump breathing has been proposed to constrain the
mouth, through the gills and out the opercular opening [42]. evolution of tongue morphology and head shape [52].
The ventilation of the lungs in Protopterus is achieved by the The aspiration breathing was present in some early
same musculoskeletal elements involved in aquatic ventila- tetrapods, but it only arised when the early amniotes app-
tion, the buccal force pump mechanisms [42]. eared. Aspiration breathing evolved in two steps: first, from
Early in their history, fish developed supplementary air pure buccal pump breathing to the use of axial muscles for
breathing organs in two taxonomic lines Actinopterygians expiration and buccal pump for inspiration; second, to pure
and Sarcopterygians [37]. The onset of aerial respiration in aspiration-breathing, in which axial muscles are used for
primitive fish was an important milestone in the evolution of both expiration and inspiration [52].
terrestrial vertebrates. The musculoskeletal units responsible for breathing also
The fish-tetrapod transition was one of the greatest serve other functions such as feeding or locomotion, and the
conflicting mechanical requirements of multiple functions
events in the vertebrate evolution. Tetrapods first appeared in
possibly constrain the performance and evolution of one or
the late Devonian about 360 million years ago, but appear to
both functions. The evolution of aspiration breathing may
have been primarily aquatic animals [49]. For some investi-
have allowed the musculoskeletal systems of the head and
gators the freshwater origin of tetrapods remains the most
tongue of amniotes to diversify, but the ribs and intercostal
likely scenario, but several recent findings raise the possi-
bility that the tetrapod land invasion could come from a musculature became constrained by their dual function in
aspiration breathing and high speed locomotion [37, 52].
marine habitat [50].
The loss of gills is also in connexion to the cutaneous
The evolution of tetrapods occured under environmental
respiration as a site gaseous exchange which can function in
influences and presumption that hypoxia habitat conditions
water and land.
40 The Open Biology Journal, 2011, Volume 4 Carvalho and Gonalves
So, the possible evolution of the respiratory mechanisms folds [37]. The highly varying extent in lung exchange is due
maybe begun with an ancestral fish adapted for oxygen to differences in the amount of gas exchange performed by
uptake and CO2 elimination in aquatic medium, but under via lungs in concert with cutaneous and buccal cavity
conditions of low oxygen, developed adaptations that exchange [37].
allowed the fish to come to the surface to obtain extra Moreover, the absence of an individualized chest well,
oxygen from the air, but the gills still functioned for CO 2
with no ribs or diaphragm, the amphibians pulmonary venti-
elimination.
lation is mainly accomplished at the expense of swallowing
At this stage of evolution, the skin would function mainly air, carried out by rising of the oral cavity floor [58].
for CO2 elimination and, as the lung became more efficient
The remarkable heterogeneity of the morphology of the
and more involved, not only in uptake of oxygen but also in amphibian gas exchangers matches that of the diversity of
elimination of carbon dioxide, the skin became less impor-
the environments in which the animals live, the lifestyle they
tant and probably covered with hardened scales to reduce
pursue, and their pattern of interrupted development. The
water loss and the animal could now remain away from
skin is the main pathway for gas transfer in aquatic species
water for longer periods [53]. It seems possible to accept that
while in terrestrial ones, it has been relegated or rendered
the cutaneous respiration was important for the earliest land
redundant [14].
vertebrates [53].
In the salamanders (Plethodontidae), some of which live
in cold well-aerated waters, gas exchange occurs across the
RESPIRATORY ORGANS IN AMPHIBIANS skin and buccal cavity [59]. Skin breathing is important in all
Based on paleontological criteria, the first amphibians extant amphibians but is the only means of gas exchange in
have arisen by evolution of fish Crossoptergeos ripidistios, those salamanders (terrestrial and aquatic) which possess
extinct in the late Devonian period [11]. neither lungs nor gills. Gas exchange takes place in the dense
subepithelial capillary network, the inflow to which is in part
Modern amphibians occupy a central position in under- from the arterial system and in part from a branch of the
standing the fundamental changes that have occurred in the pulmonary arch carrying venous blood. The oxygenated
evolution of air breathing. Dual subsistence in water and cutaneous blood flows into the venous system. This is in
land has required development of certain respiratory adapta- contrast to the arrangement of pulmonary outflow in tetra-
tions. pods and lungfish which allows (complete or partial) separa-
The transition from aquatic to land environment exposed tion of oxygenated from venous blood [60].
the gas exchange organ to a much richer oxygen ambience, The caecilians (Apoda) possess long, tubular lungs, but
which allowed a drastic reduction in the ventilation require- in some species the left lung is remarkably reduced or totally
ments, but at the same time created problems for the disposal missing [61]. The lungs of caecilians are internally sub-
of carbon dioxide, because at 20C the water solubility of divided, forming air cells that are supported by diametrically
this gas is 28 times greater than that of oxygen [54]. placed trabeculae.
To prevent a severe respiratory acidosis, the Terran In the newts (Urodela), animals that are mostly aquatic,
animal began to use the skin as an important respiratory the lungs are poorly vascularised with the internal surface
organ, designed especially for the removal of carbon dioxide, being smooth. Lungs of most amphibians such as Amphiuma
which required a substantially reduction of the barrier tridactum and the cane toad, Bufo marinus, have an
represented by the scales that covered the surface of their abundance of smooth muscle tissue [62], a feature that may
aquatic ancestors. At the same time there must have occurred explain the high compliance of the lungs [63]. In Amphiuma,
an increased bicarbonate concentration in plasma, in order to during expiration, the lung virtually collapses, producing an
compensate the increase of carbon dioxide [55]. almost 100% turn-over of inspired air [62]. Amphiuma is
These animals are mainly characterized for presenting an aquatic but has very well developed lungs.
aquatic larval form, the tadpole stage, where hematosis takes The lungs of terrestrial species are highly elaborate pre-
place through the gills. Next they suffered a metamorphosis senting a series of stratified septa that divided the lung into
that allowed them to reach adulthood in terrestrial habitat small air cells and the lungs of Anura and Apoda are more
and in which the breathing air was carried out by the lungs, complex than those of Urodela [14].
skin and mouth [56]. The amount of cutaneous and buccal
gas exchange and its percentage in the total gas exchange,
varied from species to species and also during seasons [37, RESPIRATORY ORGANS IN REPTILES
55, 57]. It is assumed that reptiles made their appearance on Earth
Amphibians have the simplest lungs, rudimentary lungs about 310 million years ago, and their adaptation was so
that are adequate for ectothermic and low aerobic meta- perfect that they dominated the planet for over a hundred
bolism animals [14]. million years. The innumerous fossils that have been dis-
covered allow us to group them in a numerous orders
The paired lungs of recent amphibians are unicameral
lying in the dorsal pleuroperitoneal cavity. In the various capable for living in different habitats, such as land, air or
aquatic environment.
amphibian species the lungs differ greatly in size, their
topographic extension and the dimension of exchange Reptilians are the first vertebrates adequately adapted for
surface by the development of interconnected folds with terrestrial habitation and utilization of lungs as a sole
highly varying number of subdivisions and height of their pathway for acquisition of oxygen [14]. The skin that was no
Comparative Physiology of the Respiratory System in the Animal Kingdom The Open Biology Journal, 2011, Volume 4 41
longer necessary for gas exchange, became an armor to identified within the conducting portion of the lung of turtles
protect against dehydration [55], being waterproof, dry, [64, 68, 69] and crocodiles [70].
covered with keratinized epidermal scales or developing
The epithelial cells lining the respiratory surface of
dermal bone plates [56].
reptilian lungs are differentiated into type I and type II cells
Compared with their gigantic prehistoric ancestors, cur- and it is possible to observe multilamellar bodies [14, 64, 71]
rent reptiles are small and insignificant and can be grouped similar to those present in mammals [72, 73]. These suggest
in four orders: chelonians, such as turtles and tortoises; that also in reptiles occurs the synthesis of surfactant lipo-
rincocfalos, like Sphenodon of New Zealand; crocodiles protein material responsible for the stability of their
(crocodiles and caimans) and squamata order (lizards and respiratory unit, the aedicula [64].
snakes). The role of surfactant in reptiles, which are not highly
The reptilian display great pulmonary structural hetero- susceptible to collapse from surface tension forces, is
geneity and there is no single model of reptilian lung. Based obscure, and may have other important functions such as
on complexity of internal organization, different classifica- prevention of transendothelial transudation of blood plasma
tion suggested that the turtles, monitor lizard, crocodiles and across the blood-gas barrier, immune suppression and
snakes have a profusely subdivided (multicameral) lung, the attraction of macrophages [2].
chameleons and iguanids have a simpler (paucicameral) lung
Reptilian lungs have preponderance of smooth muscle
and the teju lizard (Tupinambis nigropunctatus) have a
tissue and this tissue has been associated with intrapul-
saccular, smooth-walled, transparent (unicameral) lung [14].
monary connective movement of air [14].
Division of the lumen of the lung into a number of
chambers, by septation, enlarges the exchange area, fact that
is observed in turtles, lizards and crocodiles [37]. RESPIRATORY SYSTEM IN BIRDS
The lungs are localized in the pleuroperitoneal cavity and Birds respiratory system, the lung air sac system, is the
there is no diaphragm separating the thoracic from the most complex and efficient gas exchanger that has evolved
abdominal cavity. Presence of ribs and intercostal muscles in in air-breathing vertebrates. The compact and virtually cons-
reptiles, allow the development of more effective pulmonary tant-volume avian lung has been totally uncoupled from the
ventilation than that of the amphibians which do not have compliant, avascular air sacs.
these anatomical structures. The main properties that impart high respiratory effi-
Generally, the pattern of organization of the respiratory ciency on the lungair sac system of birds are a cross-current
system of reptiles is identical to mammals, with the lungs design and inbuilt multicapillary serial arterialisation system;
coated externally by a serosa [64]. The conducting portions auxiliary counter-current system; large tidal volume; large
are supported by complete cartilaginous rings, which con- cardiac output; continuous and unidirectional parabronchial
tinue through the extra and intrapulmonary bronchi. The ventilation; short pulmonary circulatory time; superior mor-
branching of the bronchial intrapulmonary tree in reptiles is phometric parameters [14]; a particularly large respiratory
similar to mammals, however they have specific designa- surface area and a remarkably thin blood-gas (tissue) barrier
tions [65], which appear sequentially bronchus, tubular [74].
chambers, niches and aedicules. Their respiratory system allows them to breathe at alti-
The intrapulmonary bronchi of the reptiles that give tudes that can reach nine thousand meters without acclima-
immediate access to respiratory areas correspond to the tization, fact that is impossible for humans and other mam-
mammalian respiratory bronchioles, the tubular chambers, mals, in which the barometric pressure of high altitudes can
according to their position and morphofunctional structure, at least induce a comatose state [75-77].
are equivalent to the alveolar channels in mammals, and the To maintain physiological function at high altitude, under
niche are similar to alveolar sacs. By its position in the reduced environmental oxygen availability, the capacity to
respiratory system and anatomical constitution the aedicules transport O2 must increase. The exposure to hypoxia causes
are equivalent to the alveoli of mammals, however they have an immediate increase in breathing due to stimulation of
an oblong structure compared with the spherical form of arterial chemoreceptors and changes in metabolic state. The
mammals alveoli. ability to adjust peripheral heat dissipation to facilitate the
The intrapulmonary bronchi of turtles that live essentially depression of body temperature during hypoxia, which
in aquatic environment have a reinforcement that extends to reduced the metabolic demand, allows birds to fly high and
or near the respiratory areas [64], characteristic that is for long periods, and is a result of an evolutionary adaptation
similar to the aquatic mammals that have the ability to dive [78]. The bar-headed goose, a typical high altitude bird,
to great depths, such as seals, dolphins and whales [66]. This depresses metabolism less than low-altitude birds during
reinforcement, along with the presence of a smooth muscle, hypoxia and breathes substantially more than birds that fly at
appear to be adaptations that allow these animals to support low altitudes. The bar-headed goose has a haemoglobin with
the high pressures to which they are subjected during the higher O2 affinity and may be capable of generating higher
immersion to great depths. inspiratory airflows [79].
The epithelium of the trachea and bronchi is pseudo- The respiratory system of birds is separated into lung (the
stratified columnar ciliated, with non ciliated secretory cells gas exchanging part) and a series of airs sacs (non res-
and basal cells, all in direct contact with the basal membrane piratory) with anastomosing air capillaries and pneumatized
[67]. Isolated or groups of neuroendocrine cells were also bones, [30, 37, 80] that allow unidirectional flow of air,
42 The Open Biology Journal, 2011, Volume 4 Carvalho and Gonalves
compared to the blind sac and tidal flow in mammalian lungs are based on a continuous basal membrane, forming the
[2, 77, 81]. simple squamous epithelium [89]. From the deepest area of
each atria arise 2 to 4 infundibula that continue with the air
Lack of diaphragm displaced the lungs to the coelomic
capillaries with 3 to 10 m diameter [37, 90, 91]. They are
cavity where they are closely attached to the ribs [2]. Inter-
calated between the sacs, the lungs are largely continuously lined by squamous cells, that are similar to the cells of the
atria, but they are not based on the basal membrane [87]. The
ventilated back-to-front by a concerted action of the cranial
infundibula and air capillaries of adjacent atria form
and caudal groups of air sacs [2, 37].
anastomosis to one another [37, 77].
There are fundamental differences in the breathing
The blood capillaries are surrounded by extremely small
mechanics of different birds, driven in part by the morpho-
logical differences of the rib cage and sternum associated air capillaries and other capillaries, which give an
appearance of a dense network. The blood capillaries are
with skeletal adaptations to locomotion [82]. The uncinate
embedded in a rigid structure with numerous cross-braces
processes are bony projections that extend from the vertebral
that provide mechanical support of the small vessels at
ribs, providing attachment sites for respiratory muscles.
numerous points [92]. This feature contributes to mechanical
The elongation of ribs, rib cage and sternum associated strength of blood capillaries and allows them to have a
with diving species, as well as longer uncinates, maybe remarkably thin blood-gas barrier (BGB) that is uniformly
important upon resurfacing when inspiration occurs against arranged all around the circumference of the blood capillary
the pressure of water against the body [82]. The reduction in [92].
the sternum and the shortest uncinate length found in the
The diameters of the air capillaries are comparable to
walking species, suggests that they may play a reduced role
those of blood capillaries and as a consequence of the very
during breathing in these species [82].
small diameter, the surface tension of these air capillaries is
The circular lumen of the trachea has a cartilaginous or so high, despite their very well-differentiated surfactant, that
partially ossified support ring, whose number varies accord- they can only remain patent as rigid structures in a volume-
ing to species [76] and is lined by a cilindric pseudociliated constant lung [37]. The surfactant of these rigid air
epithelium with goblet cells [83]. The trachea bifurcates into capillaries lowers the high air capillary surface tension to
two primary bronchi, with an epithelial lining similar to the such an extent that the remaining surface tension cannot suck
trachea but with incomplete cartilaginous rings, which fluid from the blood into the air capillary, thus preventing
disappear or are reduced when they reach the bronchial lung edema and maintaining gas exchange [37].
parenchyma [83].
Together with the extensive network of blood capillaries,
The pair of lungs of the birds are relatively small, non- the air capillaries form the gas exchange surface of the birds
compliant [37], localized in the dorsal thorax region and with lungs.
little moving during breathing, as air is driven unidirec-
Unlike those observed in lung alveoli of mammals, the
tionally though the lung, via the system of air sacs [84].
air capillaries are not terminal fund sacs formations, and
The connection between the primary bronchus and the therefore allow an unidirectional air flow through the lungs
secondary and tertiary bronchi is labyrinthic, markedly of birds [30, 77, 80, 87].
opposed to the monopodic branch of mammal. The primary
bronchus gives rise to four craneo-medium secondary bron- The lung air sacs are pair formations, and their total
number for the two lungs varies between 6 and 14 depending
chus and to seven caudal-dorsal secondary bronchus [11,
on the species, are generally referred to as cranial group and
76]. In the secondary bronchus the mucosa is lined by a
caudal group, and all cranial bags communicate with all
simple cuboidal or columnar epithelium, without goblet cells
secondary bronchi, fact that does not occur with caudal bags
[83]. Tertiary bronchus or parabronchus are arranged in a
[37, 76, 91]. The oxygen concentration is higher inside the
series of parallel lines, whose ends are open to the secondary
bronchus. All the way through the parabronchus have caudal bags whereas the concentration of carbon dioxide
reaches higher values inside the cranial bags. This qualitative
recurrent anastomoses between them [77]. The number of
difference is explained by the particular pattern of
parabronchus varies from species to species, but is higher in
unidirectional airflow that occurs in the lungs of birds [80].
the birds that fly better [85], has been estimated in Gallus
domesticus between 300 and 500 parabronchus [77, 86]. The inhaled air moves into the respiratory system, when-
Parabronchus have an average diameter of 500 m [85], and ever the chest cavity expands by the action of inspiratory
are lined by a simple squamous epithelium [87], just like the muscles, and during expiration the air is expelled by action
mammals alveolar channels. Along the inner surface of of the expiratory muscles. Although the birds do not have
parabronchus, small vesicular structures with hexagonal diaphragm, the entry and exit of air in to the respiratory
shape emerge, with 100 to 200 m in diameter [37, 77, 87]. system is a process similar to the observed in mammals.
These structures called atria are separated from each other by
During inhalation, air flows through the mesobronchus in
septa mainly consisting of smooth muscle cells located in the to the posterior air sacs, and at the same time, the air enters
freeboard [76, 87], and collagen and elastic fibers, located at
the anterior air sacs via the dorsal secondary bronchus and
the base [87]. The atria epithelium has two types of cells,
parabronchus. During exhalation, the air leaves the posterior
one of which are the granular cells [87] that are confined to
air sacs and passes through the parabronchus, and to a lesser
the atria, have a cytoplasm that contains multilamellar bodies
extent, through the mesobronchus, to the trachea. At the
and are considered analogous to the cells of type II
same time in the anterior air sacs, the air moves through the
pneumocytes of the mammals lungs [88]. The other are the secondary ventral bronchus towards the trachea. There is
squamous cells, which line the inner surface of the atria and
Comparative Physiology of the Respiratory System in the Animal Kingdom The Open Biology Journal, 2011, Volume 4 43
thus, during the two phases of the respiratory cycle, a lower capacity of the air sacs, large surface for gas exchange
continuous unidirectional flow through the parabronchus and a very thin air-blood barrier, explain the unique charac-
[80, 91]. teristics of the respiratory system of birds, allowing them to
extract oxygen from the highly rarefied air atmosphere.
The flow inside the air capillaries and inside the blood
capillaries occurs in opposite directions, i.e., in the blood
capillaries the flow goes from the most peripheral areas of RESPIRATORY SYSTEM IN MAMMALS
the parabronchus into its axis, while in the air capillaries
move away from the axis of parabronchus. It is established a Some 300 million years ago, the ancestors of modern
counter-current system of gas exchange between air reptiles finally emerged completely from water and made a
capillaries and blood capillaries [77, 80, 83]. commitment to air breathing. From them, developed the two
great classes of vertebrates with high maximal oxygen
Briefly we can say that the anatomical and physiological consumption: the mammals and the birds. A remarkable
features that have just been summarily exposed, such as a feature of these two groups is that although the cardiovas-
continuous and unidirectional ventilation of parabronchus, cular, renal, gastrointestinal, endocrine and nervous systems
B
Fig. (3). Comparation between the birds (A) and mammals (B) respiratory systems.
44 The Open Biology Journal, 2011, Volume 4 Carvalho and Gonalves
show many similarities, the lungs are radically different [93]. In mammals the capillaries are located in the alveolar
The distinct morphology of avian and mammalian lungs walls which are widely separated from each other. Thus the
reflects not only an increased demand for gas exchange, but BGB has to withstand the full transmural pressure [92]. The
is historically correlated with the divergent modes of capillary is typically polarized with one side having very thin
locomotion that facilitate higher rates of ventilations [94]. BGB whereas on the other side the barrier is thicker [92] and
contains strands of type collagen which provides support for
It is thought that mammals made their appearance on
the alveolar wall and maintains the integrity of the alveoli
Earth during the Jurassic Period, the age of reptiles, when the
[97]. In contrast to an uniform thin BGB in the birds, in
process of divergence of the continents begun [11, 56].
mammals half of the surface area of the capillaries provides
Mammals evolved homoiothermy independently from inefficient gas exchange due to its increased thickness (Fig.
birds, but in a very similar way. For the mandatory increased 3).
metabolism, they required a correspondingly increased gas
exchange surface, which became available by the develop-
ment of the broncho-alveolar lung. REFERENCES
The nearest ancestors of mammals appear to have been [1] Peret J. Controversies on the origin of life. Int Microbiol 2005; 8:
23-31.
same group of reptiles and the lung of the mammals derived [2] Maina JN. Comparative respiratory morphology: themes and
from a multicameral reptilian lung with three rows of lung principles in the design and construction of the gas exchangers.
chambers. The branched conducting bronchial system Anat Rec (New Anat) 2000; 261: 25-44.
originated by stepwise further subdivision of these lung [3] Forterre P. Looking for the most primitive organism(s) on Earth
today: the state of the art. Planet Space Sci 1995; 43: 167-77.
chambers, terminating in the branched respiratory bronchioli [4] Eigen H, Lindemann BF, Tietze M, et al. How old is the genetic
and ductus, covered with alveoli [37]. code? Statistical geometry of the tRNA provides an answer.
Science 1989; 244: 673-79.
Of all tetrapods breathing systems, the mammals respi- [5] Gribaldo S, Brochier-Armanet C. The origin and evolution of
ratory system has been the most extensively studied, often Archae: a state of the art. Philos Trans R Soc B 2006; 361: 1007-
with the aim to acquire knowledge with medical relevance. 22.
[6] Owen T, Cess RD, Ramanathan V. Enhanced CO2 greenhouse to
In mammals there is no dissociation between locomotion compensate for reduced solar luminosity on early Earth. Nature
and respiratory movements and both are closely coupled 1979; 277: 640-1.
especially during exercise. [7] Castresana J, Saraste M. Evolution of energetic metabolism: the
respiration-early hypothesis. Trends Biochem Sci 1995; 20: 443-8.
The strong musculature of the diaphragm does not only [8] Schopf JW. The evolution of the earliest cells. Sci Am 1978; 239:
act as a forceful inspiratory muscle together with the inter- 85-103.
costals musculature, but is also responsible for maintaining a [9] Alberts B, Bray D, Lewis J, et al. Molecular biology of the cell,
Garland Publishing Inc., New York 1994; pp. 218-34.
pressure gradient between the pleural and the peritoneal [10] Grunwald DJ. A fin-de sicle achievement: Charting new wares in
activity during strong exercise [95]. During respiration at vertebrate biology. Science 1996; 274: pp. 1634-5.
rest, expiration is performed by elastic retractile forces of the [11] Weichert CK, Presch W. Elements of chordate anatomy, McGraw-
extended rib cage and by the retraction forces of the lung Hill Book Company, New York 1986; pp. 209-45.
[12] Maina JN. Fundamental structure aspects and features in the
itself out of the surface tension of the alveoli together with bioengineering of the gas exchangers: comparatives perspectives.
their extended elastic fibre systems. During exercise, Adv Anat Embryo Cell Biol 2002; 163: 1-108.
expiratory movement of the intercostals musculature is [13] Atwood WH. In: Bahar LS, Johnston B, Eds Colliers
strongly supported by the muscles of the abdominal wall, encyclopedia, Maxwell Macmillan International Publishing Group,
which is also the case for all sound productions, speech and New York, Oxford, Singapore, Sydney 1992; pp. 137-66.
[14] Maina JN. Structure, function and evolution of the gas exchangers:
singing [93]. comparative perspectives. J Anat 2002; 201: 281-304.
In mammals the lungs do not empty completely during [15] Gray H. In: Bannister LH, Berry MM, Collins P, Dyson M, et al.,
Eds. Grays anatomy, Churchill Livingstone 1995; pp. 1627-82.
the expiration, and the result is that convective flow alone [16] Moore KL, Persaud TVN. Before we are born. Essentials of
cannot take the inspired gas to the periphery of the lung embryology and birth defects, W.B- Saunders Company 1998; pp.
where some of the gas-exchanging alveoli are located. 241-54.
Instead the last part of the distance is accomplished by a [17] Schoenwolf GC, Bleyl SB, Brauer PR, et al. In: Larsens Human
Embryology, Churchill Livingstone 2009; pp. 319-36.
relatively large peripheral airways to allow mixing of the [18] Evans DH, Piermarini PM, Choe KP. The multifunctional fish gill:
inspired air with that already in the lung, and the resulting dominant site of gas exchange, osmoregulation, acid-base
large alveoli cause additional problems [92]. regulation, and excretion of nitrogenous waste. Physiol Rev 2005;
85: 97-177.
In the mammalian lung, the airway and vascular systems [19] Perry SF. The chloride cell: structure and function in the gills of
form a complex multigenerational dichotomous branching freshwater fishes. Ann Rev Physiol 1997; 59: 325-47.
tree-like arrangement [96]. Transported by bulk-flow (con- [20] Laurent P, Dunel S. Morphology of gill epithelia in fish. Am J
vention) in the initial (large) parts of the bronchial system Physiol 1980; 238: R147-159.
[21] Kudo H, Kato A, Hirose S. Fluorescence visualization of branchial
and mainly by diffusion in the terminal (fine) sections of the collagen columns embraced by pillar cells. J Histochem Cytochem
airway system, the inspired air ultimately reaches the alveoli 2007; 55: 57-62.
where it is exposed to capillary blood across a thin, extensive [22] Olson KR. Vascular anatomy of the fish gill. J Exp Zool 2002; 293:
tissue barrier [14]. 214-31.
[23] Wilson JM, Laurent P. Fish gill morphology: inside out. J Exp Zool
The alveolar surface is mainly lined by type I and type II 2002; 293: 192-213.
cells. Type II cells secrete surfactant. [24] Kato A, Nakamura K, Kudo H, et al. Characterization of the
column and autocellular junctions that define the vasculature of gill
lamellae. J Histochem Cytochem 2007; 55: 941-53.
Comparative Physiology of the Respiratory System in the Animal Kingdom The Open Biology Journal, 2011, Volume 4 45
[25] Mistry AC, Kato A, Tran YH, et al. FHL5, a novel actin-binding [52] Brainerd EL, Owerkowicz T. Functional morphology and evolution
protein, is highly expressed in eel gill pillar cells and responds to of aspiration breathing in tretapods. Respir Physiol Neurobiol
wall tension. Am J Physiol 2004; 287: R1141-54. 2006; 154: 73-88.
[26] Dunel-Erb S, Bailly Y, Laurent P. Neuroepithelial cells in fish gill [53] Hughes GM. Species variation in gas exchange. Proc R Soc Med
primary lamellae. J Appl Physiol 1982; 53: 1342-53. 1966; 59: 494-500.
[27] Bailly Y, Dunel-Erb S, Laurent P. The neuroepithelial cells of the [54] Dejours P. From comparative physiology of respiration to several
fish gill filament: indolamine-immunocytochemistry and problems of environmental adaptations and to evolution. J Physiol
innervation. Anat Rec 1992; 233: 143-61. 1989; 410: 1-19.
[28] Foskett JK, Scheffey C. The chloride cell: definitive identification [55] Howell BJ. Acid-base balance in transition from water breathing to
as the salt-secretory cell I teleosts. Science 1982; 215: 164-6. air breathing. Fed Proc 1970; 29: 1130-4.
[29] Claiborne JB, Edwards SL, Morrison-Shetlar AI. Acid-base [56] Vron G. Organisation et classification du rgne animal, Eds.
regulation in fishes: cellular and molecular mechanisms. J Exp Nathan, Paris 1995.
Zool 2002; 293: 302-19. [57] Lenfant C, Johansen K, Hanson D. Bimodal gas exchange and
[30] Nielsen KS. How Birds Breathe. Sci Am 1971; 225: 72-9. ventilation-perfusion relationship in lower vertebrates. Fed Proc
[31] Herbing IH, Miyake T, Hall BK, Boutilier RG. Ontogeny of 1970; 29: 1124-9.
feeding and respiration in larval atlantic cod Gadus morhua [58] Carrier DR, Wake MH. Mechanism of lung ventilation in the
(Teleostei, Gadiformes): I. Morphology. J Morphol 1996; 227: 15- Caecilian Dremophis mexicanus. J Morphol 1995; 226: 289-95.
35. [59] Gatz RK, Crawford EC, Piiper J. Respiratory properties of the
[32] Herbing IH, Miyake T, Hall BK, Boutilier RG. Ontogeny of blood of lungless and gill-less salamander, Desmognathus fuscus.
feeding and respiration in larval atlantic cod Gadus morhua Respir Physiol 1974; 20: 33-41.
(Teleostei, Gadiformes): II. Function. J Morphol 1996; 227: 37-50. [60] Piiper J. Respiratory gas exchange at lungs, gills and tissues:
[33] Liem KF. The biology of lungfishes: an epilogue. J Morphol 1986; mechanisms and adjustsments. J Exp Biol 1982; 100: 5-22.
1: 299-303. [61] Maina JN, Maloiy GMO. A scanning and transmission electron
[34] Clack JA. Earliest known tetrapod braincase and the evolution of microscopic study of the lung of a caecilian Boulengerula taitanus.
the stapes and fenestra ovalis. Nature 1994; 369: 392-4. J Zool (Lond) 1988; 215: 739-51.
[35] Zhu M, Yu X. A primitive fish close to the common ancestor of [62] Stark-Vancs V, Bell PB, Hutchson VH. Morphological and
tetrapods and lungfish. Nature 2002; 418: 767-70. pharmacological basis for pulmonary ventilation in Amphiuma
[36] Daeschler EB, Shubin NH, Jenkins FA Jr. A Devonian tetrapod- tridactylum: an ultrastructural study. Cell Tissue Res 1984; 238: 1-
like fish and the evolution of the tetrapod body plan. Nature 2006; 12.
440: 757-63. [63] Hughes GM, Vergara GA. Static pressure-volume curves for the
[37] Duncker H. Vertebrate lungs: structure, topography and mechanics. lung of the frog (Rana pipiens). J Exp Biol 1978; 76: 140-65.
A comparative perspective of the progressive integration of [64] Fleetwood JN, Munnell JF. Morphology of the airways and lung
respiratory system, locomotor apparatus and ontogenic parenchyma in hatchlings of the loggerhead sea turtle, Caretta
development. Respir Physiol Neurobiol 2004; 144: 111-24. caretta. J Morphol 1996; 227: 289-304.
[38] Bemis WE, Burgreen WW. The biology and evolution of [65] Perry SF. Reptilian lungs: functional anatomy and evolution. Adv
lungfishes. J Morphol 1986; 1: 3-4. Anat Embryol Cell Biol 1983; 79: 1-81.
[39] Kemp A. The biology of the Australian lungfish, Neoceratodus [66] Kooyman GL. Respiratory adaptations in marine animals. Am Zool
forsteri (Krefft 1870). J Morphol 1986; 1: 181-98. 1973; 13: 457-68.
[40] Power JHT, Doyle IR, Davidson K, Nicholas TE. Ultrastructural [67] Castells MT, Ballesta J, Pastor LM, et al. Histochemical
and protein analyses of surfactant in the Australian lungfish characterization of glyconjugates in the epithelium of the
Neoceratodus forsteri: evidence for conservation of composition extrapulmonary airways of several vertebrates. Histol J 1990; 22:
for 300 million years. J Exp Biol 1999; 202: 2543-50. 24-35.
[41] Shelton G. The regulation of breathing. Fish Physiol 1970; 4: 293- [68] Pastor LM, Ballesta J, Hernandez F, et al. Microscopic study of the
359. tracheal epithelium of Testudo graeca e Pseudemys scripta
[42] Burggren WW, Johansen K. Circulation and respiration in elegants. J Anat 1987; 153: 171-83.
lungfishes (Dipnoi). J Morphol 1986; 1: 217-36. [69] Pastor LM, Ballesta J, Castels MT, et al. A light and electron
[43] Greenwood PH. The natural history of African lungfishes. J microscopic study of the epithelium of the extrapulmonary airways
Morphol 1986; 1: 163-79. of Mauremys caspica and Lacerta lepida (Reptilia). J Submicrosc
[44] Fishman AP, Pack AI, Delaney RG, Galante RJ. Estivation in Cytol Pathol 1988; 20: 25-36.
Protopterus. J Morphol 1986; 1: 237-48. [70] Perry SF. Functional morphology of the lungs of the Nile crocodile,
[45] Perry SF, Euverman R, Wang T, et al. Control of breathing in Crocodylus niloticus: non-respiratory parameters. J Exp Biol 1988;
African lungfish (Protopterus dolloi): a comparison of aquatic and 134: 99-117.
cocooned (terrestrialized) animals. Respir Physiol Neurobiol 2008; [71] Solomon SE, Purton M. The respiratory epithelium of the lung in
160: 8-17. the green turtle (Chelonia mydas L.). J Anat 1984; 139: 353-70.
[46] Lenfant C, Johansen, K. Respiration in the African lungfish [72] Kikkawa Y, Motoyama EK, Cook CD. The ultrastructure of the
Protopterus aethiopicus. I. respiratory properties of blood and lungs of lambs: the relation of osmiophilic inclusions and alveolar
normal patterns of breathing and gas exchange. J Exp Biol 1968; lining layer to fetal maturation and experimentally produced
49: 437-52. respiratory distress. Am J Pathol 1965; 47: 877-903.
[47] Sacca R, Burggren W. Oxygen uptake in air and water in the air- [73] Askin FB, Kuhn C. The cellular origin of pulmonary surfactant.
breathing redfish Calamoichthys calabaricus: role of the skin, gills Lab Invest 1971; 25: 260-8.
and lungs. J Exp Biol 1982; 97: 179-86. [74] Maina JN. What it takes to fly: the structural and functional
[48] de Moraes MFPG, Holler S, da Costa OTF, et al. Morphometric respiratory refinements in birds and bats. J Exp Biol 2000; 203:
comparison of the respiratory organs in the South American 3045-64.
lungfish Lepidosiren paradoxa (Dipnoi). Physiol Biochem Zool [75] Tucker VA. Respiratory physiology of house sparrows in relation
2005; 78: 546-59. to high altitude flight. J Exp Biol 1968; 48: 55-66.
[49] Long JA, Gordon MS. The greatest step in vertebrate history: a [76] Lasiewski RC. Respiratory function in birds. Avian Biol 1972; II
paleobiological review of the fish-tetrapod transition. Physiol 287-342.
Biochem Zool 2004; 77: 700-19. [77] Maina JN. Scanning electron microscope study of the spatial
[50] Graham JB, Lee HJ. Breathing air in air: in what ways might extant organization of the air and blood conducting components of the
amphibious fish biology relate to prevailing concepts about early avian lung (Gallus Gallus variant domesticus). Anat Rec 1988; 222:
tetrapods, the evolution of vertebrate air breathing, and the 145-53.
vertebrate land transition? Physiol Biochem Zool 2004; 77: 720-31. [78] Scott GR, Cadena V, Tattersall GJ, Milsom WK. Body temperature
[51] Randall DJ, Burgreen WW, Farrel AP, Haswell D. The evolution of depression and peripheral heat loss accompany the metabolic and
air breathing in vertebrates. Cambridge University Press 1981; pp. ventilatory responses to hypoxia in low and high altitude birds. J
133-50. Exp Biol 2008; 211: 1326-35.
46 The Open Biology Journal, 2011, Volume 4 Carvalho and Gonalves
[79] Scott GR, Milsom WK. Control of breathing and adaptation to high [88] Lorz C, Lopez J. Incidence of air pollution in the pulmonary
altitude in bar-headed goose. Am J Physiol 2007; 293: R379-91. surfactant system of the pigeon (Columba livia). Anat Rec 1997;
[80] Scheid P. Respiration and control of breathing. Avian Biol 1982; 249: 206-12.
VI: 405-53. [89] Scheuermann DW, Klika E, De Groodt-Lasseel MHA, et al. An
[81] Maina JN. Developmental dynamics of the bronchial (airway) and electron microscopic study of the parabronchial epithelium in the
air sac system of the avian respiratory system from day 3 to day 26 mature lung of four bird species. Anat Rec 1997; 249: 213-25.
of life: a scanning electron microscope study of the domestic fowl, [90] Duncker HR. Structure of the avian respiratory tract. Respir
Gallus gallus variant domesticus. Anat Embryol 2003; 207: 119-34. Physiol 1974; 22: 1-19.
[82] Tickle PG, Ennos AR, Lennox LE, et al. Functional significance of [91] Randall DJ. In: Animal physiology, R. Eckert, W.H. Freeman and
the uncinate processes in birds. J Exp Biol 2007; 210: 3955-61. Company, New York 1988; pp. 474-519.
[83] Banks WJ. In: Applied veterinary histology, Williams and Wilkins, [92] West JB, Watson RR, Fu W. The honeycomb-like structure of the
Baltimore, Hong Kong, London, Sydney 1986; pp. 447-66. bird lung allows a uniquely thin blood-gas barrier. Respir Physiol
[84] Thompson MB. Comparison of the respiratory transition at birth or Neurobiol 2006; 152: 115-8.
hatching in viviparous and oviparous amniote vertebrates. Comp [93] West JB, Watson RR, Fu W. The human lung: did evolution get it
Biochem Physiol 2007; 148: 755-60. wrong? Eur Respir J 2007; 29: 11-7.
[85] Akester AR. The comparative anatomy of the respiratory pathways [94] Hicks JW, Farmer CG. Gas exchange potential in reptilian lungs:
in the domestic fowl (Gallus domesticus) pigeon (Columbia lvia) implications for the dinosaur-avian connection. Respir Physiol
and domestic duck (Anas platyrhyncha). J Anat 1960; 94: 487-505. 1999; 117: 73-83.
[86] King AS, Cowie AF. The functional anatomy of the bronchial [95] Duncker HR. The emergence of macroscopic complexity. An
muscle of the bird. J Anat 1969; 105: 323-36. outline of the history of the respiratory apparatus of vertebrates
[87] Klika E, Scheurermann DW, De Groodt-Lasseel MHA, et al. from diffusion to language production. Zoology 2001; 103: 240-59.
Pulmonary macrophages in birds, Barn Owul, (Tyto tyto alba) [96] Maina JN, van Gils P. Morphometric characterization of the airway
Domestic Fowl (Gallus, gallus f. domestica) Quail (Coturnix and vascular systems of the lung of the domestic pig, Sus scrofa:
coturnix) and Pigeons (Columbia livia). Anat Rec 1996; 246: 87- Comparison of the airway, arterial and venous systems. Comp
97. Biochem Physiol 2001; 130: 781-98.
[97] Weibel ER. Morphological basis of alveolar-capillary gas
exchange. Physiol Rev 1973; 75: 1097-109.
Received: November 26, 2010 Revised: January 10, 2011 Accepted: January 10, 2011