2016 Lambertz Recent advances on the funtional and evolutionary morphology of the amniote respiratory apparatus (1)

Ann. N.Y. Acad. Sci. ISSN 0077-8923
A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S
Issue: Respiratory Science
Recent advances on the functional and evolutionary
morphology of the amniote respiratory apparatus
Markus Lambertz
Institut für Zoologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
Address for correspondence: Markus Lambertz, Sektion Herpetologie, Zoologisches Forschungsmuseum Alexander Koenig,
Adenauerallee 160, 53113 Bonn, Germany. m.lambertz@zfmk.de
Increased organismic complexity in metazoans was achieved via the specialization of certain parts of the body
involved in different faculties (structure–function complexes). One of the most basic metabolic demands of animals
in general is a sufficient supply of all tissues with oxygen. Specialized structures for gas exchange (and transport)
consequently evolved many times and in great variety among bilaterians. This review focuses on some of the latest
advancements that morphological research has added to our understanding of how the respiratory apparatus of
the primarily terrestrial vertebrates (amniotes) works and how it evolved. Two main components of the respiratory
apparatus, the lungs as the “exchanger” and the ventilatory apparatus as the “active pump,” are the focus of this paper.
Specific questions related to the exchanger concern the structure of the lungs of the first amniotes and the efficiency
of structurally simple snake lungs in health and disease, as well as secondary functions of the lungs in heat exchange
during the evolution of sauropod dinosaurs. With regard to the active pump, I discuss how the unique ventilatory
mechanism of turtles evolved and how understanding the avian ventilatory strategy affects animal welfare issues in
the poultry industry.
Keywords: Amniota; breathing; evolution; functional morphology; respiration; respiratory biology
Introduction
Respiration is a universal phenomenon of life that
allows organisms to utilize chemically bound energy
in an efficient way. Respiring oxygen is doubtlessly
the most common or at least best known strategy
to make this energy available. In principle, this is
true for most multicellular animals (Metazoa), but
it applies especially to the vertebrates (Craniota1 ).
The origin and early radiation of craniotes took
place in the aquatic realm, and, for this reason, one
finds numerous adaptations for water breathing in
the form of a huge structural and functional variety
of gills in the more basal taxa.2 However, especially
in limnic or brackish habitats, a very large number
of fish species are at least facultative if not obligatory
air breathers.3 The potential to use airborne oxygen
as an additional resource brings a significant selective advantage, especially in bodies of water with
low oxygen content. On the average, about 30 times
more oxygen is contained in a liter of air than in the
same volume of water. In addition to that, the much
lower viscosity of air results in less effort during the
ventilation of the oxygen-bearing medium.2
Once the faculty (structure–function complex)4
for air breathing evolved, it opened the doors to a
terrestrial lifestyle. The present review focuses on
the functional and evolutionary morphology of the
respiratory apparatus in the primarily terrestrial
vertebrate clade: Amniota. Although a number of
intriguing studies related to the evolutionary and
functional morphology of the respiratory apparatus have appeared in recent years (e.g., Refs. 5–15),
the scope of the present article is mainly restricted to
the research presented during the symposium entitled “Recent advances on the functional and evolutionary morphology of the respiratory apparatus”
at the Third International Congress of Respiratory
Science.16
Although the model shown in Figure 1 illustrates the general principles of a respiratory faculty, I limit the discussion here to amniotes. The
doi: 10.1111/nyas.13022
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Morphology of the amniote respiratory apparatus
Figure 1. The faculty of the amniote respiratory apparatus. The lungs act as the “exchanger” and the “passive pump,” in gas
exchange and ventilatory air movements, respectively. The respiratory musculature (mainly of the trunk) acts as the active pump that
generates the primary ventilatory air movements. Additional complexes involved in the respiratory apparatus are the circulatory
system and the neuronal control. Modified from Ref. 2.
respiratory apparatus is understood as a functional
unit consisting of at least four larger complexes.17
One of these complexes is the lungs as the site of
gas exchange. Nonetheless, the lungs not only serve
as the diffusion-driven “exchanger” but also have
a mechanical function: they contribute as a “passive pump” to ventilatory air movements. However,
the main motor for respiratory air movement, the
“active pump,” is represented by the interplay of
the muscular and skeletal elements of the trunk
(at least primarily for amniotes). Additionally, the
circulatory system that transports the gases within
the blood is a central component of the respiratory
apparatus in its broadest sense. This is last but not
least because blood, together with its dissolved gases,
has an effect on pH, and thus also has a regulatory
function. The primary regulatory unit, however, is
the nervous system. While the circulatory and nervous systems are not further dealt with here, the
exchanger and the active pump will be the central
aspects of this review.
The exchanger
From so complex a beginning: the ancestral
amniote gas exchanger
Lungs were doubtlessly already present before the
rise of the earliest amniotes.18 The much greater
content of oxygen in the air alone facilitated the
supply channel for the metabolic machinery of
amniotes, but other factors associated with terrestrialization (e.g., keratinized skin) required that the
lungs act as the primary site for gas exchange. On
the basis of several centuries of typology-driven
anatomical research, it was until recently the widely
purported view that the ancestral amniote lung was
comparable to that of extant amphibians: by implication a simple, almost sac-like, single-chambered
organ.19–22 All of the complexity embodied in the
diversity of amniote pulmonary morphology has
been thought to represent independently evolved
optimizations with respect to aerial gas exchange.23
One main reason for that argument is based on the
fact that most Lepidosauria (tuatara, lizards, and
snakes) indeed exhibit single-chambered lungs,24
superficially resembling those found in amphibians.
However, upon closer examination, there are significant differences between the single-chambered
lungs of amphibians and most lepidosaurs. The first
concerns a feature that becomes evident on superficial examination: the extrapulmonary airways of
amniote lungs always have a subapical entrance,25
whereas they enter amphibian lungs at their anterior
apex. A second major macroscopic difference concerns the path of the pulmonary artery. In amphibians, it forms a plexus that supplies the entire
lung, while in amniote lungs, it exhibits a strictly
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Lambertz
hierarchically branched pattern.26 This is true for
both all of the internally branched lungs of mammals, birds, crocodiles, and turtles and the singlechambered lungs of lizards and snakes. In these latter species, the pattern of the vascular supply also
mirrors the location of the larger septa that occasionally extend into the pulmonary lumen of the
single-chambered lungs. This leads to the question
of whether the so-called niches that are formed by
these septa might, in fact, be rudimentary chamber
Anlagen. A critical species for all of these considerations is the tuatara (Sphenodon punctatus), the sole
extant representative of the Rhynchocephalia. Traditionally and consistently, the lungs of the tuatara
have been described as being more similar to those
of amphibians than to any lizard.27 Reexamination,
however, revealed all of the above-mentioned typical
characteristics of amniote single-chambered lungs:
subapical bronchial entrance and several discrete
septa that extend into the pulmonary lumen, each
with individual blood supply by a branch of a strictly
hierarchically branched pulmonary artery.26 Given
that these possible indications for a branched nature
of the lungs are present in all amniotes, including
the tuatara and even in species with a highly derived,
single-chambered pulmonary morphology, such as
cobras, the hypothesis of a common branched Bauplan for amniote lungs receives further support.
In order to test this hypothesis, however, it was
necessary to actually examine the ontogeny of a typical single-chambered lung of a lizard. Geckos fulfill
all demands for such a case study: they have singlechambered lungs,24 they are phylogenetically quite
basal among extant lepidosaurs, and they are easy to
maintain and breed. The Madagascar ground gecko
Paroedura picta was chosen for this study. The early
developmental stages of its lungs could indeed be
characterized as a discrete “branching phase,” during which several chamber-like buds branch off the
central Anlage, just as it takes place in the more
“complex” amniote lungs.26 During later development, however, the branching stops and the lung
switches to an “expansion phase,” which is characterized by the growth in volume and development
of the parenchyma. The topology of the adult lung is
achieved well before hatching (Fig. 2). Although no
single study has documented the entire ontogeny of
such a single-chambered lung, partial developmental series from a variety of lepidosaurs, including the
tuatara, corroborate these findings.26
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Pulmonary complexity was apparently secondarily reduced in lepidosaurs, which immediately raises
the question, Why? Multichambered lungs, in general, are more advantageous than single-chambered
ones of comparable size: they present a larger surface area for gas exchange and they usually are
much more easy and cost effective to ventilate, due
to their higher compliance.28–30 However, the fossil record indicates that lepidosaurs underwent a
miniaturization.31 For such tiny lizards, maintaining a complexly branched lung results in severe biophysical problems. The terminal air spaces would
have become so small and the surface tension would
have become so high that it would have been
impossible to inflate these miniscule lungs without an accessory structure, such as air sacs or a
diaphragm.26 Given that neither can be assumed
to have been present, simplification was apparently
the only chance to take advantage of the ecological
opportunities that were associated with becoming
small.
In conclusion, this represents a paradigm shift
for our understanding of amniote lung evolution: it
started complex, branched, and multichambered,
and either remained that way, became yet more
complex, or became secondarily simplified.26 It may
further be worth noting that several of the early
anatomists and embryologists, such as Ivar Broman (1868–1946) and Fanny Moser (1872–1953),
had already provided crucial data for this revised
scenario.26 This once again highlights the importance of the huge amount of classical literature
dealing with anatomical and embryological topics, which, because of the fact that a lot of it has
been published in languages other than English,
frequently but unfortunately is overlooked or even
neglected in current studies.
Long and simple, yet so effective: detecting
pathologies in snake lungs
Among the lepidosaurs, numerous lineages independently evolved an elongated body that is often
associated with a reduction of the extremities.32,33
While such a snake-like habitus can be encountered
in almost all major clades of lizards, true snakes
(Serpentes) represent the most diverse taxon of the
Squamata (all extant lepidosaurs except the tuatara).
Such a dramatic change of the Bauplan must clearly
affect the entire internal anatomy of these animals.
While there are different solutions to how these
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Morphology of the amniote respiratory apparatus
Figure 2. The lungs of the Madagascar ground gecko, Paroedura picta. The upper row shows P. picta embryos at different stages
of their development, and the middle row shows the corresponding embryonic lungs. During early developmental stages, the lungs
produce several buds that branch off from the central Anlage. This is defined as the branching phase of pulmonary development.
Later in ontogeny, the branching stops and the lungs expand. This is defined as the expansion phase. The adult morphology is
already achieved well before hatching. The bottom row shows dried lungs of an adult specimen (lateral face of the left lung on the
left side and medial view of the opened right lung on the right side). Note the branching pulmonary artery that supplies the septa
bordering the dorsal and ventral niches. Modified from Refs. 26 and 43.
various snake-like animals cope with the problems
associated with an elongated body,34–36 all snakes
follow a similar path when it comes to their respiratory systems. We have just discussed that lepidosaurs
reduced their internal pulmonary complexity and
secondarily developed functional single-chambered
lungs. The same applies to snakes as well. However, the right lungs of snakes are also extremely
elongated, while the left lungs are always reduced
in size and may be entirely reduced or present only
as vestigial rudiments.37 In spite of their—with a
few exceptions—extremely simple Bauplan, when
it comes to the internal structural pattern and the
enlargement of the respiratory surface area, the huge
size of the single right lung and/or its efficiency in
gas exchange apparently allows many snake species
(e.g., elapids) to maintain highly active lifestyles.
In general, little is known about the morphological diffusion capacity of reptilian lungs,24 and,
in particular, the distribution of the gas-exchange
tissue (parenchyma) is extremely diverse among
the different clades of snakes.37 In light of the
tremendous species diversity of snakes (as well as
the huge anatomical diversity of their lungs), until
recently there was, surprisingly, only a single morphometric study on the lungs of a single colubrid
species.38 This now has been expanded by work on
the ball python (Python regius) and Burmese python
(P. molurus),39,40 both of which are representatives
of giant constrictors (Pythonidae), which also are
frequently kept as pets.
As with all pets, health issues are important,
and there is great interest in and need for effective veterinary treatment. Many snakes are known
to be very susceptible to pulmonary infections,41
but there appears to be a high tolerance for these
diseases until clinically relevant symptoms eventually become recognizable.42 This raises the question
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Figure 3. Histological sections of the pulmonary parenchyma of Python molurus. (A) A healthy individual and (B) an infected
snake at the same magnification. Note the thickened connective tissue of the trabecular septa (s) in the infected specimen. Further
note the filling of the faveolar space (f) with mucus and pus in the infected specimen. sm, trabecular smooth muscle core. Modified
from Ref. 40.
of how the animals cope with these conditions and
how they remain (at least superficially) unaffected
by such infections.
The histology of such infected pulmonary tissue
revealed that it is usually characterized by a thickening of the connective tissue of the trabecular septa
(Fig. 3). The consequence of this is an increase in
the diffusion barrier distance and therefore a reduction of the morphological diffusion capacity. In fact,
the morphological diffusion capacity for oxygen
is reduced to about one-fourth of healthy values
in infected specimens.40 Given this dramatic alteration, why does it take so long before clinically recognizable symptoms appear?
If the morphological values for the potential
of oxygen uptake are compared to physiological
recordings of actual oxygen consumption rates, it
turns out that even the infected and morphologically seriously impeded animals still can easily satisfy their demand for oxygen, at least under resting
conditions. The lungs apparently have a remarkable
overcapacity that allows them to function to a certain degree in spite of such infections.40 Possible
functional explanations for this overcapacity could
lie in the fact that, under healthy conditions, when
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the animals assume a coiled up posture or are digesting large prey, the entire respiratory parenchyma
does not have constant access to air.
However, this once again highlights that the structurally simple lungs of lepidosaurs should not be
regarded as an insurmountable obstacle or impediment: lepidosaurs are not “poor” because they have
such simple lungs. While there indeed appears to be
a limitation for reaching large body sizes for highly
active animals with simple lungs,43 pythonids show
that there is a solution to becoming quite large with
truly sac-like lungs, which, in fact, appear to have
been one key to the success of lepidosaurs as one of
the most diverse lineages of terrestrial vertebrates.
How to become a giant sauropod: modeling
heat exchange properties of the respiratory
system
After having discussed the fundamental structural
properties of amniote lung evolution and how
certain lungs work in health and disease in terms
of their primary function (gas exchange), we now
come to the function of the exchanger in temperature control. As already pointed out, an effective respiratory apparatus (considering the four
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Morphology of the amniote respiratory apparatus
Figure 4. Diagrammatic representation of the functional cascade required for the evolution of “high-performance” animals
among amniotes. Starting from the basal amniote condition that, among other traits, includes terrestrial reproduction with
internal fertilization, aspiration breathing, and multichambered lungs, a three-chambered heart with two aortas, water-resistant
skin, and economical excretory system, high-performance status evolved independently in various lineages. The final frontier or
barrier required to achieve this status appears to have been the development of homoiothermic endothermy. However, before this
could be achieved, the respiratory faculty (including its circulatory system component) and the nutritional system (including the
procurement and processing of food responsible for delivering the required metabolic energy) had to improve. Original diagram
designed by the author together with Steven F. Perry (Bonn, Germany).
above-mentioned complexes it comprises) is one of
the prerequisites for the evolution of large and active
animals with a homoiothermic/endothermic physiology (Fig. 4). However, particularly large body sizes
come at various costs for the organisms.
The largest terrestrial animals that ever evolved
were the sauropod dinosaurs, and several species
reached body masses that were hypothesized to
exceed 10 metric tons.44,45 When the metabolic rate
of these giants was estimated, it became evident that
these animals must have encountered heat dissipation problems: the concept of “gigantothermy”
was born.46 How was it possible that these animals
existed without encountering the thermal limits of
their physiological processes and as a result significant if not lethal damage?
It has long been known that sauropod dinosaurs
often exhibit a high degree of postcranial skeletal
pneumaticity, which reduced the mean density of
the body and thus can be interpreted as an adaptation that facilitated the evolution of such large body
sizes.47–50 In recent years, however, this postcranial
pneumaticity has been further interpreted as the
result of the presence of voluminous air sacs comparable to those found in birds.51,52 Sauropoda is
the sister taxon of Theropoda, which eventually gave
rise to the birds as the sole surviving representatives
of the dinosaurs. An avian-like respiratory system
has also been proposed already for the nonavian
theropods,53,54 and in recent years, a similar respiratory system for the sauropod dinosaurs has become
the preferred hypotheses as well.52,55–57
Furthermore, it has long been known that birds
are able to dissipate excess metabolically produced heat via their respiratory system.58–60 While
extant birds are available for experimental studies and direct measurements, the extinct nonavian
dinosaurs are obviously not. Methods such as the
extant phylogenetic bracket61 are valuable tools to
infer the presence of certain morphological traits,
while a functional morphological approximation62
cannot only aid in testing such hypotheses but also
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Lambertz
help in bringing back life to extinct animals. Modeling approaches are therefore not only extremely
helpful, but are also frequently the only option to
tackle evolutionarily important questions such as
the origin of the largest terrestrial vertebrates.
Computational fluid dynamics is one of such
modeling approaches that can be used to infer a
potential heat-dissipation mechanism via the respiratory system in sauropod dinosaurs. As a first
step, a relatively simple, two-dimensional model of
an extant avian analog has been created, and respiratory heat dissipation has been simulated.63 In a
further refined approach, this model has been transferred into a three-dimensional simulation.64 Both
studies revealed comparable results with realistic
values if compared to the actual experimental data
for birds. The main difference between these two
approaches was that the pressure values were more
realistic in the three-dimensional simulation. However, since the absolute pressures are irrelevant to the
pertinent question, the two-dimensional approach
remains extremely attractive because of its simplicity and the resulting much lower computing times.
At any rate, it turned out that the trachea is solely
responsible for respiratory heat exchange. Work in
progress currently aims at transferring the obtained
results and models to a putative sauropod respiratory system with its gigantic dimensions. This
approach has the potential, especially in combination with additional estimates for radiational heat
loss over the skin, to answer the question about how
sauropods were able to reach such exceptional body
sizes. The respiratory apparatus could indeed have
played more than one central role in this evolutionary cascade: via the provision of sufficient oxygen for the huge metabolic demand, but simultaneously also via the dissipation of the resulting excess
metabolic heat through evaporative cooling in the
trachea.
The active pump
Breathing in a straitjacket: the unique
chelonian ventilatory dilemma
In terms of their ventilatory apparatus, turtles are
doubtlessly the most astonishing group of vertebrates that ever evolved. The basic motor for ventilation in amniotes was (and frequently still is)
the ribs. Although numerous auxiliary breathing
mechanisms that at least compliment costal ventilation evolved in all major amniote lineages, none
entirely eliminated the ribs as part of their respira106
tory apparatus—none but turtles, in which the ribs
are integrated in their most iconic morphological
feature: the shell. The ribs broaden during development and fuse with each other (as well as with several
other bones) and thereby form a large portion of the
carapace:65,66 the dorsal part of the shell. On a functional level, this has severe consequences, because
the ribs become completely immobile and cannot
be recruited to generate the volumetric changes that
are required for ventilatory air movements. So how
do turtles breathe?
This question, in fact, is a very old one that can
be dated back at least to one of the founding fathers
of experimental biology: Marcello Malpighi.67,68 In
a letter that was published in part by the Royal
Society of London in 1671,69 Malpighi draws the
comparison to frogs and how they breathe. Extant
amphibians employ a buccal pump mechanism,
which, in principle, can be described as the process of swallowing air.70–72 Indeed, at first glance,
this seems to make perfect sense for turtles. Observing resting turtles reveals that they spend a large
amount of time performing oscillatory movements
of their buccal floor. Given that the ribs cannot be
recruited for these purposes and that it is known
that air swallowing exists, why not assume that
turtles do the same? In fact, the idea that turtles also perform buccal pumping to ventilate their
lungs persisted well into the 20th century.73 However, during the 1790s, Robert Townson performed
several basic functional morphological and physiological studies in Göttingen.67,74 He subsequently
published a privately printed book, which, in addition to English translations of his original Latin dissertations, also contained a previously unpublished
study on ventilation in turtles.75 There, he questioned the air-swallowing hypothesis and proposed
a new one: turtles use antagonistic muscles of their
ventral body wall to generate ventilatory air flow.
Although it required more than a century and a half
and sophisticated electromyographical analyses68,76
to test Townson’s hypothesis, it turned out to be correct. Inspiratory air flow mainly is generated by the
cup-shaped M. obliquus abdominis, which is situated
in the posterior flanks of all turtles (Fig. 5). When
this muscle contracts, it flattens and decreases pressure within the shell and thus also within the lungs,
and air flows in. Expiration is mainly achieved by
the M. transversus, which directly wraps around the
pleuroperitoneal cavity (Fig. 5). Upon contraction,
this muscle pushes the viscera against the lungs,
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Morphology of the amniote respiratory apparatus
Figure 5. Reproduction of the very first illustrations of the main respiratory musculature in turtles; from Ref. 75. In his seminal
study, Robert Townson (1762–1827)106 was the first to hypothesize that antagonistic muscles of the ventral body wall are the motor
of ventilation in turtles. The original captions are provided here in full, with occasional clarifications added in brackets. Plate I
represents a tortoise (Testudo orbicularis (Emys orbicularis)) on its back. * The sternum (plastron) turned back. + (Note that there
is no direct representation for the symbol used between Q and i on the right-hand side of Plate I.) The peritoneum covering the
left lobe of the lungs. (A) The muscle of inspiration (M. transversus abdominis) nearly in its natural situation, still connected to the
testa (carapace), but separated from the sternum (plastron). (B) The place of its insertion in the testa (carapace). (C) Where it was
connected to the sternum (plastron). (a) The same muscle still connected to the testa (carapace) and sternum (plastron), but turned
back. (b) When (sic, most likely meant where) it is inserted in the testa (carapace). (c) Where it is inserted in the sternum (plastron).
(D.d) The cellular membrane (connective tissue) by which it is united to the muscle of expiration (M. obliquus abdominis). (E.e)
The muscle of expiration (M. obliquus abdominis). (F.f) Where it arises from the peritoneum. (G.g) The dotted line shows where the
peritoneum ceases to be connected to the bladder (cloacal bursa). (H.h) The outline of the bladder (cloacal bursa) when inflated.
(I) The middle bladder not covered by the peritoneum. (i) The outline of it where covered by the peritoneum. (K) The right lobe
(simply the right lung) of the lungs. (L) One of the bronchia (right extrapulmonary bronchus). (M) The aspera arteria (trachea).
(N) The neck. (O) The neck curved as when brought under the testa (carapace). (P) Two of the muscles that draw the neck under
the testa. (Q) The inside of the testa (carapace) where the fore legs have been cut away. (R) The os hyoides (os hyoideum). (S)
Its horns. (T) The inferior maxilla (lower jaw). (V) The superior maxilla (upper jaw). (W) The os pubis. Plate II. Represents the
testa (carapace), or upper shell of the tortoise (Testudo orbicularis (Emys orbicularis)) with the muscles of respiration. (A) The
muscle of expiration (M. transversus abdominis). (B) Its insertion in the testa (carapace) near the spina dorsi (vertebral column).
(C) Termination of the muscular fibers where they were connected to the peritoneum. (D) The same muscle turned back. (E) The
muscle of inspiration (M. obliquus abdominis). (F) Its insertion in the margin of the testa (carapace). (G) Where it was inserted in
the margin of the sternum (plastron).
and air flows out. While the general homology and
synonymy of the respiratory muscles in turtles is
of most likely interest to the specialist only (see
Ref. 77 for a detailed discussion), it might be worth
noting that the “M. diaphragmaticus,” as Bojanus
in his classical anatomical study78 called it, actu-
ally represents a thoracic portion of the transverse
muscle. In order to avoid any further confusion,
either with the mammalian or crocodilian muscles
with the corresponding name, “M. diaphragmaticus” in turtles should be replaced by M. transversus
thoracis.77
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Theoretically, this unique ventilatory mechanism
must have originated before the evolution of the
shell. The crucial questions, however, are. When did
it take place and can we actually track it in the fossil
record?
Recent years have brought spectacular new
insights into the early evolution and origin of
turtles.66,79–85 The current best candidate for the
oldest known representative of the chelonian lineage is Eunotosaurus africanus, from the Permian of
South Africa.85,86 On the basis of the bone histology
of a single rib of this species, it was assumed that this
stem-group representative that still exhibits individual ribs that are not fused to form a complete shell
already lacked the intercostal musculature, which is
also lacking in modern turtles.66 This would have
had severe implications for its mode of breathing,
as the intercostal muscles are the main motor of
rib movements. A more complete sampling corroborated this assumption of lacking intercostals
and furthermore led to a refined hypothesis about
the morphology of the ventilatory apparatus of
E. africanus. Potential osteological correlates for
muscle attachments were discovered only on the
third, sixth, and seventh ribs, while ribs four and
five lacked such indications.77 These putative attachment sites were restricted to the caudal edges of ribs
3, 6, and 7, making them unlikely to represent intercostal muscles. This distribution of muscle attachments, however, corresponds well with the origin of
the main expirator in extant turtles, the M. transversus, which is bipartite in nature and composed of
a thoracic (M. t. thoracis) and abdominal (M. t.
abdominis) portion. It was consequently concluded
that E. africanus, although it still possessed individual ribs and no shell, already showed the bipartite
nature of its transverse muscle; this part of the chelonian ventilatory apparatus was already present in
the currently earliest known stem representative. It
was therefore further concluded that the evolutionary origin of the turtle Bauplan was achieved by a
division of function. Initially, the ribs and associated trunk musculature had dual functions in respiration and locomotion. The ribs broadened over
time and provided mechanical support and aided in
torsional control, which freed several of the muscle
groups from their original function77 (Fig. 6).
However, the most crucial question remains:
when and how did the main inspiratory muscle
(the M. obliquus abdominis) evolve to its caudally
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displaced and cup-shaped form? There are unfortunately no unambiguous osteological correlates for
this muscle, meaning that its presence and location must be indirectly inferred. Lyson et al.77
hypothesized, based on an extant analog,76 that a
gravity-induced passive mode of inspiration could
at least have supplemented ventilatory air movements. Through various interorgan connections, the
liver was assumed to pull on the lungs (compare the
schematic cross section in Fig. 6), decreasing intrapulmonary pressure and allowing air to flow in.
The origin of the chelonian M. obliquus abdominis will most likely remain a conundrum. It is interesting, however, to note that among the shell-less
stem representatives of turtles, the plastron, which
is the ventral part of the shell, begins to fuse earlier
than the carapace. E. africanus still possessed a set
of paired and unfused gastralia,77 but the currently
known next younger representative (Pappochelys
rosinae) also has broadened yet unfused ribs, yet
the gastralia are partly fused, which is interpreted
as the first evidence of a plastron-like formation.84
In keeping with the scenario proposed by Lyson
et al.,77 this evolutionary sequence is highly plausible, as increased rigidity of the ventral portion of
the body wall facilitates the inspiratory function of
the M. obliquus abdominis, which in extant turtles
inserts on the caudal edge of the plastron.
The broiler chicken: a basic functional
morphological question at the forefront
of animal welfare issues
The avian respiratory system presents a unique ventilatory strategy among extant amniotes (but see the
discussion about nonavian dinosaurs above). While
the exchanger is kept at a more or less constant volume during the entire breathing cycle, highly pliable air sacs cause the ventilatory air movements.87
These air sacs are ventilated by a pump mechanism of the sternum, which is elevated and lowered dorsoventrally.88–92 The sternum consequently
has to be regarded as a central element in the
avian ventilatory apparatus, and there appears to
have been a constraint on maintaining this structure throughout the evolution of the modern birds
(Neornithes).93
Although it remains debatable when and how
active flight evolved in early birds,94–97 it is characteristic for the vast majority of the extant species.
The avian M. pectoralis, which originates at the
C 2016 New York Academy of Sciences.
Ann. N.Y. Acad. Sci. 1365 (2016) 100–113 Lambertz
Morphology of the amniote respiratory apparatus
Figure 6. Proposed scenario for the evolution of the unique chelonian ventilatory mechanism. During the phylogeny of stem
turtles, an increase in trunk rigidity occurred (left). A division of function between the ribs (torsional control) and the hypaxial
muscles (ventilation) is assumed to have already occurred at the very base of the stem lineage of turtles (right). The intracoelomic
organization (lower middle) is assumed to have facilitated this via the potential for gravity-induced (g) passive inspiration. Modified
from Refs. 77 and 84.
sternum, generates the downbeat of the wing and
is usually the largest single muscle in flying birds.
This also makes it very attractive for the meat industry. Indeed, the production of broiler chickens, for
instance, has been geared toward the selection for
strains that show large pectoral muscle mass and has
resulted in an increase over the last decades in order
to maximize profits. This results in a mechanical
conflict: an increase in pectoral muscle mass must
have an impact on the animal’s performance. Additional load influences not only locomotor costs, but
also those associated with ventilation.98–101
The ultimate desire for fast production of broilers
today results in quite abnormal animals in which
the pectoral muscle mass grows much faster than
the rest of the of animal. Neither the lungs nor several other organs can keep up with this artificially
accelerated development.102 In addition, the ossification of the skeleton of broilers is far from complete
at their slaughter age. For instance, the uncinate
processes, osseous projections of the posterior side
of the vertebral ribs in birds that are integral for
avian ventilatory performance,103–105 retain a cartilaginous connection to the rib.102
These analyses indicate that the relative heterochronic and allometric development of broilers
makes them very susceptible for pathological conditions and results in an unintended yet significant
impact on animal welfare of these chickens.102 These
analyses furthermore not only highlight that broiler
chickens represent a powerful model to examine
basic functional morphological questions but also
that breathing mechanics has a great relevance for
applied science in modern society.
C 2016 New York Academy of Sciences.
Ann. N.Y. Acad. Sci. 1365 (2016) 100–113 109
Morphology of the amniote respiratory apparatus
Lambertz
Conclusions
The latest advancements in our understanding
of the functional and evolutionary morphology
of the amniote respiratory apparatus summarized
here elucidate a general conclusion: even after
several centuries of morphological research, there
still remains a need for studies on such presumably ancient questions. Many issues have yet to be
resolved, and even almost dogmatically accepted
views can turn out to be incorrect or at least questionable upon closer examination. The integration
of various approaches, such as the close collaboration of neontologists and paleontologists, or of fundamental and applied researchers, or the application
of modeling approaches that sometimes originate in
distant disciplines, appears to be the most promising
path in order to achieve far-reaching conclusions.
Solid morphological data remain a cornerstone of
the development of critical evolutionary hypotheses
that subsequently can be tested using more modern approaches, such as developmental genetics.
Some of the recent advances that are summarized
here appear to be simply basic research, but upon
closer examination, they can have great relevance for
applied questions as well, including animal welfare
issues.
Traditional morphological research and therefore also the proper education in this field, which,
in turn, requires maintaining attractive faculty
positions for scientists with a respective background, remain important in modern universities
and society. Although the golden age of morphology doubtlessly already took place during the 19th
century, morphological research has not lost any of
its contemporariness and value today.
Acknowledgments
The present article derives from a symposium held
on July 8, 2014, in Bad Honnef, Germany, during the
course of the Third International Congress of Respiratory Science (ICRS). Financial support for the
ICRS-3 was granted by the Deutsche Forschungsgemeinschaft to Steven F. Perry (Pe 267/16-1). Further partial financial support for the particular symposium from which this paper was derived was
granted to the author by the Deutsche Zoologische
Gesellschaft. I wish to express my sincere thanks to
all speakers of the symposium, whose diverse talks
gave fascinating insights into various aspects of the
110
latest morphological research. These were (alphabetically): Jonathan R. Codd (Faculty of Life Sciences, University of Manchester, Manchester, UK),
Tyler R. Lyson (Denver Museum of Nature & Science, Denver, CO), J. Matthias Starck (Department
of Biology II, Ludwig-Maximilians-Universität
München, Germany), Steven F. Perry (Institut für Zoologie, Rheinische Friedrich-WilhelmsUniversität Bonn, Bonn, Germany), Peter G. Tickle
(Faculty of Life Sciences, University of Manchester, Manchester, UK), Christian Wirkner (Allgemeine & Spezielle Zoologie, Institut für Biowissenschaften, Universität Rostock, Germany), and
Ulrich Witzel (Fakultät Maschinenbau, Arbeitsgruppe Biomechanik, Ruhr-Universität Bochum,
Bochum, Germany). I would furthermore like to
cordially thank Steven F. Perry for his constructive
criticism on earlier versions of the manuscript.
Conflicts of interest
The author declares no conflicts of interest.
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