Paper - The functional history of the coelom and the diaphragm (1913)

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Jones FW. The functional history of the coelom and the diaphragm. (1913) J Anat Physiol. 47(3):282-318. PMID 17232958 .

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This historic 1913 paper by Jones describes the the coelom and the diaphragm.

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Modern Notes: diaphragm | coelomic cavity | rib

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The Functional History of the Coelom and the Diaphragm

By Frederic Wood Jones

It is possible, in investigating the function and the true meaning of any structure, or organ, of the animal body, to gain some information that may help in its proper understanding, by studying the conditions that are present in animals too simple in their organisation to possess the particular system that we wish to investigate. It is possible, by determining the exact point in the animal scale at which the particular structure appears and by studying the change in habit and function in those animals in which its first rudiment is shown, to glean, in some measure, an idea as to the purpose of the newly developed element. If a new function is developed at one point in the animal scale, and at the same time a new organ develops, it is a strong ground for argument that some relation exists between the organ and the function. Again, if, with an utter change of the general structure of the animal plan, some other, but lesser change in the bodily organs appears for the first time, it is a strong argument that the new conditions of the animal body and the functions of the new organ are in some way intimately associated. This appears a simple proposition, and it is one the simplicity of which was apparent as a working guide to John Hunter; but it is one that is not always used to its full advantage in modern anatomy.

In an attempt to unravel the true meaning of the diaphragm, it is not enough to study its condition in animals in which it is well developed, or even to examine those rudiments by which it shows its first presence in the animal series; but it is necessary to see clearly the conditions in those animals in which it is entirely undeveloped, and, further, to note the other changes in the animal body that are coincident with its first appearance. It is therefore logical, in such an inquiry, to examine first the structure and economy of those animals that possess one single simple body cavity—the ecelom—undivided by any partition into secondary chambers. This brings us to the study of some simple Ceelomate type (see fig. 1); and before the study of such a type can be in any way satisfactory, some sort of idea must be gained of the true meaning and function of the simple coelom itself. Following the lines of our first proposition, it becomes necessary to see what conditions are found in animals too low in the animal scale to possess a coelom, and what changes in general structure and function accompany its first appearance. It is therefore necessary to glance at the general conditions that prevail in animals which do not possess a coelom—the great class of the Coelenterata.

Fig. 1. — A simple Celomate type

Fig. 2. — A simple Celenterate type seen in a diagrammatic median seen in a diagrammatic median longitudinal section. longitudinal section.

It is by no means essential to discuss all the anatomical characters of a typical Coelenterate, and a diagram of a representative member is sufficient to indicate the general features of the group (see fig. 2), but some outstanding characteristics of the class must be noted. Regarded as an experiment of Nature in animal construction, it may be said that the Coelenterate type did not lead far, and it would appear that the limit in the size to which the coelenterate body may grow is the cause of the nonsuccess of the group in the struggle for supremacy. A solitary Coelenterate is, typically, a small animal, and though some of the most bulky masses of animal growth are composed of Coelenterate animals, it is by, an aggregation of myriads of bodies in a colony that this size is reached, and not by the growth of the individual animal. The attainment of at any rate some considerable size is an essential for success in the onward march of animal perfection, and this appears to be only possible among the Coelenterates by the herding together, in one composite mass, of an enormous number of individuals, all integral parts of one great corporate body.. But though in this way the possibility of growth is attained, it is only brought.about by the sacrifice of the other great essential of success in animal progress—the power to move from place to place. These great composite bodies are deprived of the power of locomotion, for but little specialisation into organs to subserve the many functions of an individual appears to be possible in complex colonial masses. It now becomes a question why, although the Coelenterates are so very limited in the size of their individual growth, the Coelomates are able to grow as individuals, and have no need to resort to the production of colonial forms in order to extend their growth and development. It would appear that it is because there is in the Coelenterates no definite vascular system that individual growth is limited. A body cannot grow large unless in its economy some provision is made for the nourishing of its distant parts. This is the function—and the primary function—of a vascular system. A central organ is needed to pump nourishment to outlying parts, and when this condition is attained, the animal body can spread out in various directions, and become specialised into different parts for the performing of different functions. With a vascular system individual growth may proceed, without the resort to colony production, and without the consequent loss of the power of movement of the individual. Seeing that no definite vascular system is provided in the Coelenterata, and that in the Coelomata it very soon appears, it becomes reasonable to inquire if any connexion between the presence of a coelom and the development of a vascular system is to be found. Now, it may be said at once that the development of the coelom does not appear to be in any way connected with the vascular system. Whatever the colom may afterwards become, it is “essentially and primarily (as first. clearly formulated by Hatschek) the perigonidial cavity, or gonoccel” (Ray Lankester). The coelom, therefore, is in its origin a thing having no relation to the vascular system, and is merely a space developed round the gonads, or primitive sexual glands. But this matters not at all to the present inquiry, for it is only necessary to determine if its development—due to whatever primary cause—has any influence upon the production of a vascular system, and here it would seem that some connexion may be found. In the lowest Coelomates, in which the coelom is but imperfectly developed, there is, so far as is at present known, no definite vascular system ; and it is not until some degree of perfection in the development of the coelom is arrived at that the system of a central contractile organ and peripheral tubular ramifications to supply distant parts is established.

In the lowest Coelomates, the Turbellarians, where the coelom is not fully developed, there is probably no vascular system.

In Nemertea there is a body cavity in the young stages, and a vascular system.

In the Annelida, where the body cavity becomes definitely established, the first well-developed vascular system becomes permanent in the animal series. It is at this point, where a well-developed cooelom becomes an established thing, that a well-recognised contractile organ becomes developed.

It would, therefore, appear to be not unreasonable to attempt to establish some connexion between the increasing perfection of the development of the coelom and the establishment of a definite system of vessels ramifying from a central contractile organ—an essential vascular system.

In what way may the presence of a coelom make it possible for the growing complexity of animal organisation to elaborate a system of tubes and a contractile vessel? The answer would appear to be found in the fact that, in order to maintain any circulation of the nutrient fluids through the tubes, the alternate contraction and expansion of the central organ is necessary, and to-permit of this alternate contraction and expansion the presence of a surrounding space is an essential. An effectual alteration in size of the contractile organ cannot be maintained when it is surrounded by solid tissues: it is necessary to have a space in which the organ may contract and expand, and the coelom provides such a space. The central space of a Coelenterate body—the archenteron—is not a cavity suitable for the enclosing of a contractile vessel, for, since it is not a closed space, in which pressure may be regulated, the contractions of the central organ would have to be carried out in opposition to very varying pressures (see fig. 2). A Coelenterate animal living in the water is subjected to a variety of external pressures, and these pressures it has no power to regulate or guard against in its central cavity; but with the advent of a closed space within the body, and contractile fibres within the substance of the body wall, an internal pressure may be regulated, and a contractile organ may work in a uniform pressure. The coelom, therefore—developed first as a perigonidial cavity—becomes, when perfected, a space which, supported by the body wall and under the control of the body musculature, permits of an even pressure being maintained within the body cavity in which a rhythmically contractile organ may work and establish a circulation.

This primitive circulation is a system the purpose of which is to carry nutritive products to distant parts of a not very highly specialised animal body. It is in its first inception a lymph-vascular system, that carries only the products of digestion in its stream, and so permits cells and organs distant from the alimentary system to be nourished. So far, no sort of respiratory function is added to its rédle; and it is only later on in animal development that it becomes a hemo-lymph vascular system, and carries oxygen in its stream (see fig. 3).

We have now arrived at another important landmark in the inquiry into the purposes of the coelom, for with the advent of a hemo-lymph circulation, the beginning of a respiratory system is indicated. Besides the products of digestion, it is necessary, as the body becomes more complex, that distant cells and organs should receive a supply of oxygen, and this oxygen is carried to them in a variety of ways; but the only method that concerns us here is the distribution of oxygen by the vascular system.

Fig. 3. — A simple Coelomate type showing a contractile vascular system within the celom.

In some of the lower Coelomates the oxygen is taken up at the general body surface, and is carried in the blood stream from the more superficial parts of the body to the deeper parts. This method of conveying oxygen to the blood stream is one that is obviously limited to lowly animals, for, with the specialisation of the body, the external surface cannot be utilised as a respiratory area. The next step is, therefore, that, instead of the blood stream going to the surface to pick up its oxygen, the oxygen is brought to the deeper parts of the body and conveyed to the blood stream. This is the dawn of an intra-coelomic respiratory system; and it, again, is an outcome of the perfecting of the development of the coelom. We have seen that the ecelom, as a space*within the body, allows of the regulation of an internal pressure, and so permits the primitive heart to contract and expand. If a simple Coelomate be imagined (see fig. 3) to be subjected to pressure from without, it is easy to see that, by expanding its body wall against the pressure, it may reduce the pressure within the coelom to the normal. This is the stage at which a vascular system becomes possible. But it is also easy to conceive a further stage of perfection in the control of the pressure within the ecelom in which an animal may create at will, at intervals, an actual negative pressure within its body cavity. This is the stage at which an intra-coelomic respiratory system may become developed.

An intra-coelomic respiratory system, therefore, only comes into the animal economy after the development of a vascular system, and appears in the animal series only after the coelom and body wall are so far perfected that the creation of negative pressures within the body cavity is possible. The development of an intra-coelomic respiratory system marks one of the most important epochs in animal evolution, for, with various modifications, it is found in all animals beyond this stage in development. The first beginnings of such a system may be described briefly as limited areas of the external surface of the body “sucked” in towards its central cavity (see fig. 4). In Nemertea the first appearance of the intra-coelomic respiratory system is as ingrowths from the surface of the body intruding upon its central cavity as “side organs” or “ciliated furrows.” In Arthropods the system becomes further developed by the production of the elaborate “tracheal systems,” which are tubes by which air can be sucked from the surface far into the tissues of the body. In all their complications such systems are essentially communications between the superticial layers of the body and the deeper layers by means of which air can be drawn into the central parts of the body when a negative pressure is created within the coelom. In principle the lung system of the air-breathing vertebrates is essentially the same, but in this case a specialised part of the alimentary tract is set apart for the development of reservoirs into which the outer air may be drawn (see fig. 5).

Fig. 4. — A simple Celomate type in which a Fie. 5.—A Coelomate (vertebrate) type in portion of the outer surface of the body which a portion of the pharynx has as been ‘‘sucked” into the coelom as a been ‘‘sucked” into the celom as a respiratory system (L). respiratory system (L)

The lung systems of the air-breathing vertebrates are merely extensions of the process of “sucking” in to the deeper parts of the body, portions of the more superficial layers in which air may be inspired and held in contact with the ramifications of the vascular system, to permit of the pieking up of oxygen by the oxygen carriers of the blood. The possession of lungs in some form is the common possession of a vast assemblage of animal types, and the method by which the air is drawn into the lungs and expelled again is a physiological problem that is solved in a variety of ways in different types.

Reptiles, amphibians, birds, and mammals all have this in common, that they possess lungs; but the only point of resemblance that they share in the method of filling and emptying them is that all do it by creating an alteration of the pressure within their body cavity by means of the action of the muscles of their body walls,

The great majority of reptiles fill their lungs and empty them again by alternately raising and depressing their ribs, and so altering the capacity of the coelom. This movement takes place slowly in some of the Ophidia, and the rhythmic heaving movements of portions of the body are easy to see. In active Lacertilians the movements are of the same nature, but frequently are far more rapid. In the Chelonians the respiratory movement is slow (3 to the minute (Bert) ), and, in consequence of the encasing of the body in a hard outer covering, it is limited to those portions of the body wall both in front and behind where, owing to the exit of the limbs, the carapace fails to meet the plastron.

Some doubt as to the precise action at these two parts of the body exists, but it would appear that at one spot or the other the action of the muscles of the body wall must be inspiratory.

Special reference should perhaps be made to the method of respiration in the tortoise, since this animal has so often been investigated for the purpose of determining the actual rudiments of the mammalian diaphragm. I cannot help thinking that the selection of so specialised a creature as a subject in which to discover anything connected with primitive respiratory mechanism is unfortunate.

Although the actual anatomical condition does not appear to be complex, still it must not be forgotten that the tortoise has adopted a method of respiration that is somewhat different from that displayed by any other vertebrate type. A tortoise in a state of activity actually breathes by alternately pushing its shoulder girdle backwards and pulling it forwards by means of the muscles of its fore limb, while in more passive breathing the same, but much slighter, movements are effected by the muscles acting on the shoulder girdle from within the carapace.

Among the amphibians, the swallowing of air by the action of the buccal muscles is obvious, and it appears to take place in both the tailed and the tailless forms, and in all amphibians the proper muscles of the cooelom are expiratory in their action.

The method of respiration in birds has been several times investigated, and Hunter made the first considerable contribution to the subject in 1774 ( Works, vol. iv. p. 176), unaware of the previous work of Harvey in 1653. From these, and from the many subsequent investigations of the subject, there appears to be no doubt that it is mostly by the movements of the muscles of the abdominal wall that respiration is carried on.

Now, all these lung-breathing creatures fill their lungs with air, and empty them again by movements of the muscles of their body wall; there is in them no partition between chest and abdomen as a developed diaphragm, and what rudiments of such a structure as are present in them, act, not as the mammalian diaphragm, as a muscle of inspiration, but as a muscle the action of which on the lungs, if indeed it has one, is that of expiration.

Since all these creatures breathe by means of lungs, and yet perform all the respiratory movements without the aid of a structure like the mammalian diaphragm, it would not appear unreasonable to question the supposition that the diaphragm of the mammals is developed for the especial purpose of breathing with lungs.

In 1822 Sir Charles Bell published his classic upon the nervous mechanism of human respiration, and in this work he sharply distinguished between an external respiratory system of muscles and nerves and an internal system. The diaphragm and its nerves constituted the internal respiratory system: the muscles of the face, the neck, the chest, and the back, and their accompanying nerves, constituted the external respiratory system. Bell thoroughly appreciated the great importance of his external respiratory system, and he added a note to his paper, when in 1836 he republished it, to express his regret that his ideas had not been appreciated or extended ; it may even be said that to-day, in naming one nerve only of all his external respiratory group as “the external respiratory nerve of Bell,” full appreciation is not being given to his work.

Looked at from the point of view of Bell’s work, it may be said that it is the internal respiratory system that becomes developed in man and some of the higher Mammalia, and that in the lower lung-breathing orders the processes of respiration are entirely carried on by the external respiratory system. It therefore becomes necessary to determine the true relationships of these two systems, and to see how far this new internal respiratory system is introduced for the purposes of respiration when so many lungbreathing vertebrates carry on all their respiratory processes without it.

It also becomes natural to inquire, since lungs are not a new possession in the mammals, what change of general structure peculiar to the Mammalia might have necessitated the introduction of this new feature.

The Muscles of the Body Wall

It is to the fish that we must turn for the most simple expression of the musculature of the body wall—the musculature that composes the wall of the coelomic cavity. The typical three-layered condition which is familiar in the higher forms is brought about by adaptations of a very simple underlying condition which finds its earliest evolution in the simple coelom wall of fishes.

The lower vertebrates, and in all probability the immediate ancestors of the lowest vertebrates, were animals which lived in the water. Two functional factors dominated the disposition of their body-wall muscles; for it was necessary for them to perform swimming movements, and also to be able to maintain a pressure within their coelomic cavity to resist the external pressure of the water in which they lived.

In a typical fish the lateral body musculature forms the most conspicuous part of the animal, and it clothes the whole body from the head to the tail. The muscular mass is divided into a dorsal part above the lateral line, and a ventral part below it. The dorsal fibres run in the long axis of the body from head to tail, and form a uniform, longitudinally directed, muscular mass; but the ventral fibres below the lateral line run obliquely around the sides of the coelom and become longitudinal only at the mid-ventral line.

In the dogfish the ventral sheet is a single layer, and its fibres are directed obliquely downwards and forwards (cephalad) ; it corresponds to the internal oblique layer of the Mammalia as well as that part of the rectus abdominis which is derived from its ventral longitudinal fibres in the middle line. In Protopterus another layer is added. This layer is external to the oblique layer of the dogfish, and its fibres are directed downwards and backwards (caudad). This new oblique set of fibres represents the external oblique layer of the Mammalia and so much of the rectus abdominis as is derived from its longitudinal ventral fibres. It is not until the Amphibia are reached that a third layer is added to the musculature of the abdominal wall. This new layer is the transversus sheet, and it is developed deep to the two oblique layers of Protopterus in intimate relation to the lining membrane of the coelomic cavity. The fibres of this layer pass for the most part transversely round the body cavity, only their dorsal and ventral fibres tending to become oblique. In the mid-dorsal line and in the mid-ventral line the fibres of the transversus layer run in the anteroposterior axis of the body, forming behind the sub-vertebral rectus of Humphry, and in front the deepest portion of the rectus abdominis.

The transversus layer may be looked upon as the muscle for the compression of the coelom. It is introduced into the anima] type coincident with the need for increased internal pressure for the functions of expiration from lungs, more perfect circulation, and increased general activity. The fishes have no need for a muscle for the compression of the coelomic cavity in order to expel air from distended lungs; and it appears that there is at any rate a functional association between the development of this layer and the acquisition of the power of air-breathing.

The story of the body-wall muscles, looked at from a broad functional standpoint, is therefore fairly clear. One layer, an ultimate intermediate layer, is developed in connexion with the coelom wall, mainly for the purpose of making this wall more or less resistant; and in this layer the ribs are developed. One layer is developed outside this rib-bearing layer for the purpose of producing movements of the body, or of the limbs. One layer is developed inside the rib-bearing layer in order to compress the coelom. The last layer is only introduced into the animal series hand in hand with the development of air-breathing lungs, in order to raise the intra-coelomic pressure and to squeeze air out of the lungs after it has been previously “ pumped” in.

As a higher specialisation of the muscles of the external layer is the function they exert of expanding the coelom wall by dragging upon the intermediate rib-bearing layer and so causing a decrease of pressure within the ceelom. This higher specialisation steps in first in the Reptilia, and afterwards becomes the stereotyped method of inspiration—a method of filling the lungs by suction instead of by pumping down or swallowing air.

Ribs And Their Physiological Import

We have seen that the coelom, when once it is developed in any degree of perfection, is essentially a space in which, at. an even pressure, the functions of the contractile vascular system can be carried on. We have also seen that the function of the inner muscular layer of the body wall is essentially developed in connexion with the coelom of the air-breathing vertebrates, and serves to compress the coelom and assist in expelling its contents.

The muscles of the middle layer have, however, a different function, and within their thickness the ribs become laid down.

For what purpose are the ribs developed? It is obvious that they are not introduced into the animal structure, as is at times assumed, for the purpose of making the body wall capable of expansion, and so acting as agents of inspiration, for in fishes and in tailed amphibians the ribs are present apart from any respiratory action.

The ribs of fishes cannot be present in order that the diameters of the coelom may be enlarged for the purpose of filling the lungs. The obvious suggestion for the reason of their presence would appear to be that they are developed within the walls of the coelom to prevent the coelom being crushed in by external pressure, and in fact serve the same purpose as the “ribs” of a boat.

Fig. 6. — Diagram to show the different arrangement of piscine (left side of figure) and mammalian (right side of figure) ribs and spinal nerves.

The habits of fish make it peculiarly necessary that the walls of their coelom should have some protection against the pressure from without of the water in which they live, and ribs are developed in part in order to withstand this pressure. Not only are fish subjected to the pressure of the water against their sides, but they have to resist in their body cavity the pressure that they themselves create by the movements of their lateral muscles for the production of the swimming motions of their tails. When the tail is a functional means of propulsion of an animal, it is necessary that its movements be brought about by means of the lateral muscles derived from the outer layer.of the body muscle sheets; to give these muscles origin, and to withstand the pressure of their contraction, the ribs become developed in the thickness of the middle muscular layer. In thus seeking the functional cause of the development of ribs in the fishes, I am not overlooking the fact, demonstrated by August Miiller in 18538, that the “ribs” of Teleostean fish are not morphologically the same structures as the ribs of the mammals (see fig. 6). The fact does not weigh against the present view, but rather strengthens it—that in different classes of vertebrates structures, not morphologically identical, should be developed for the same functional purpose. In the reptiles, we have among the Ophidia the greater part of all the movements of the animal carried on by contractions of the lateral muscles, and here the development of ribs reaches its maximum. Among the Lacertilians the development of limbs renders the action of the lateral muscles and of the tail less important, and in them the ribs tend to become reduced; but among the crecodiles the tail still functions actively, and the ribs are numerous, and extend over the whole of the coelom wall.

The difference in functional value of the tails of lizards and those of some other members of the Reptilia is at once obvious from a study of the animals in a natural state of activity. The tails of many lizards seem to be almost a hindrance to the owner, and various means are adopted for carrying the tail in any particularly hurried action. So far is this the case that Bates (The Natwralist on the Amazons) has said, “The tails of lizards seem to be almost useless appendages to the animals.” Again, the readinéss with which most species will part with their tails tells of the comparative functionless state of this organ.

Among the amphibians a state of great interest is arrived at, for the tailed Amphibia are well provided with ribs, while in the group of the Anura the ribs have become greatly reduced and almost absent. Not only so, but, as Goette has shown, the middle layer of body muscles, in which ribs are laid down, is developed in the tailed tadpole of Bombinator igneus, but is wanting in the tailless adult.

Among the Aves the lateral muscles that act upon the tail are of little importance, and the ribs are reduced, but here other functional factors come into play.

Among the Mammalia, it would at first sight be expected that the development of ribs would reach the maximum in members of the Cetacea, for in them the hind limbs and pelvis are reduced to the merest rudiments, and propulsion through the water is effected by the movements of the hinder end of the body. As a matter of fact, it is among the Cetacea that the most reduced rib series is seen in the whole of the Mammalia, for in Hyperoodon no more than nine ribs go to make up the entire thoracic wall. Here we have an apparent contradiction ; but I think that it is by no means a real contradiction, and that the explanation lies in the very special nature of the swimming movements of the Cetacea.

The tails of fishes, amphibians, and reptiles are moved from side to side ; they are flattened from side to side, and are acted on by lateral muscles (see fig. 7). The “tails” of the Cetacea are moved up and down, are flattened from above downwards, and are moved by dorsal and ventral muscles (see fig. 8). Itis at once obvious that the ventral flexion of the hinder end of the Cetacean body, which gives the powerful “flip” with which the animal propels itself through the water, must prohibit the development of ribs upon that part of the spinal column which undergoes the flexion. It may be mentioned that the enormous bulk of the rectus abdominis, which acts as the flexor of the Cetacean “tail,” was noted by

Fig. 7. — Dorsal view of a fish to show the action of the lateral muscles in producing the lateral movements of the tail in swimming (necessity for complete rib series).

Fig. 8. — Lateral view of a Cetacean to show the action of the dorsal and ventral muscles in producing the up-and-down movements of the tail in swimming (necessity for abbreviated rib series).

John Hunter. Among the Pinnipedia — in which the swimming movements are mostly carried out by the very specialised hind limbs—the rib series is a long one, the seals having fifteen, and the walruses fourteen, rib-bearing vertebree.

I therefore regard ribs — from whatever morphological factor they are developed—as being present for the purpose of protecting the coelomic cavity from pressure, caused by the contraction of the lateral fibres of the outer layer of muscles acting on a functional tail.

It is impossible to regard ribs as being developed to assist the processes of respiration, and I do not think it is any more possible to look upon them as being introduced into animal structure, “in connexion with the mechanism of circulation ” (Keith).

But although ribs are evolved to withstand pressure, and to guard the ecelom from being crushed in, they soon developed another réle. Acted upon by the muscles of the outer layer, they can be made to produce a negative pressure in the coelom, and so become inspiratory in function—in the same way as inspiration had been previously brought about in the invertebrates. In reptiles, birds, and mammals they have taken on this new function, and become essentially the mechanism by which air is drawn from without into the cavity of the lungs. In fishes, where there are no lungs, and in Amphibia, where the lungs are filled by a different method, the ribs act only in their original rédle of pressure-resisting structures.

The story of the invertebrates is repeated, and structures that at first merely resisted an external positive pressure subsequently come to create an internal negative pressure.

Among the snakes the movements of the ribs are the greatest of all the factors in altering the pressure within the coelom, and the expanding and contracting of the body is easy to see in the slow respiratory movements of these creatures. In the pronograde mammals, again, the muscles acting on the ribs are the chief inspiratory agents; and in man, when the breathing is of the so-called “thoracic” type, it is the movements of the ribs that fill the lungs with air. The passive ribs of the fishes and tailed amphibians have therefore become in the mammals the actively moving structures that bring about the negative intra-thoracic pressure, and so fill the lungs with air. The “hoops” laid down in the sides of the animal for the purpose of resisting pressure (caused by muscular contractions or outside influences) have, in fact, developed into the “external respiratory system,” and this “external respiratory system” is the all-important functional respiratory apparatus in most lung-breathing animals.

The Development of Limbs and the Reduction of the Rib Series

Those animals that use their tails as active organs of locomotion have, as a rule, a large number of ribs. The number of ribs tends to diminish with the developing perfection of the limbs. A tadpole is propelled through the water entirely by the movements of its tail, and it starts to develop a rib-bearing body layer; a frog’s activity depends entirely upon its welldeveloped limbs, and it has the merest rudiment of ribs. No doubt, other factors come into play, and the bald assertion may not be pushed too far ; yet there is sufficient evidence to be found in a broad survey of the animal kingdom to warrant the statement that with increasing functional perfection of lateral limbs the number of the ribs tends to diminish.

I have given the reason that may perhaps be the underlying one in the association of tail movements with a large number of ribs—ze. that the ribs may render the body wall firm, and enable it to resist the pressure caused by the contractions of the lateral tail muscles to which they give origin. I am well aware that another factor also enters into this association, and I have called attention to it briefly in a former paper (Journal, vol. xliv. p. 377); but since the whole process is so intimately bound up with this question of coelomic pressure and respiratory movements, it must be repeated in a few words. When ribs are reduced consequent on the development of limbs, they are lost first from those segments opposite which the limbs develop. The ribless cervical region and the ribless lumbar region are developed only in association with the outgrowth of functional limbs.

Fig. 9. — Diagram, after a reconstruction of a human embryo of 6.9 mm, by Streeter, to show the nerve roots running to the limb plexuses.

I have ventured to suggest that the concentration of the nerves from several segments, as a plexus, upon one point is the primary cause of this condition ; for the gathering together of the epiblast of several primary segments prohibits the development of the mesoblast between these segments.

The mammalian nerves arise within the circle of the ribs, and, in order to reach the limbs, pass out between the ribs (see fig. 6). In the embryo this is done without disturbance, since epiblastic nerves and intervening mesoblast pass parallel to each other from the relatively short dorsal column to the relatively broad limb bud (see fig. 9). It is only when disproportion of growth between the column and the limbs upsets this parallel arrangement that the intervening mesoblast becomes abbreviated and rib elements, which have started to develop, become aborted.

The possession of a neck and a waist, therefore, may be said to be introduced into the animal form as a structural necessity consequent on the acquirement of limbs.

But it will be at once objected that the Teleostean fish, which have both pectoral and pelvic limbs functional, have no neck and no waist—no “ribless” cervical or lumbar regions.

I take it as a support for these ideas that the coexistence of piscine limbs with a full series of ribs is the outcome of the different morphological plane upon which the piscine “ribs” are developed. The ribs of fish articulate with the centra of the vertebre, and not with their neural arches, and therefore the nerves do not have to pass between the ribs, or their mesoblastic basis, to reach the limbs. Nerves may be gathered into plexuses regardless of the underlying ribs in Teleostean fish, although the altered relation of the ribs in the orders higher than this does not permit of such an arrangement (see fig. 6).

It must also be remembered that the lateral limbs of the fish are altogether subservient to the tail as a functional means of propulsion. We may therefore assume that there is a connexion between the functionactivity of lateral limbs and the abbreviation of the rib series, that ribless areas—the neck and waist—are developed in association with functional limbs ; and that this functional end appears to be brought about by the formation of the limb plexuses.

It must be remembered that this process has far-reaching results, since, of that portion of the coelom included between the fore and hind limbs, one part will now be begirt with ribs and the other be ribless.

The Origin of the Diaphragm

The gradation is by simple steps, and the process is easy to understand by which an animal type comes into existence having the following features: (1) it has an external muscular layer which may expand its coelom wall and decrease its intra-coelomic pressure; (2) it has an intermediate layer in which protecting ribs are developed for shielding the coelom from external pressure; and (3) it has an internal muscular layer by which the coelom may be squeezed and the intra-coelomic pressure raised.

Animals of this type inspire and expire air; their respiratory organs are within their general coelomic cavity; they produce young by laying eggs, and pass their urinary products with their feces as comparatively small solid masses; they all possess an undivided coelom and an undivided cloaca.

We have now to deal with a new animal type—the one in which the coelomic cavity becomes subdivided into separate compartments by the development of a muscular partition, the diaphragm.

This type is, of course, that of Mammalia, and, in order to follow the story of the subdivision of the coelom, it is necessary to determine (1) from what is the septum derived, and (2) what features are possessed by the lung-breathing Mammalia which differ from those of the lung-breathing Sauropsida, and which might render such a septum necessary.

The development of the diaphragm is ontogenetically not by any means so clear as its phylogenic history would suggest, and but little of the actual stages of embryonic development, as usually described, helps much in the solution of the problem.

It is among the tailless Amphibia that the origin of the mammalian diaphragm has been sought for the most part by those who have investigated its evolution. The observations made by Beddard and, later, by Keith upon the condition found in Xenopus and Pipa form the basis of most recent accounts of the first stages of the septum that in the mammals comes to separate the thoracic and abdominal cavities.

In 1895 Beddard described certain fibres of the transversus sheet that in these forms became detached from the body wall to obtain attachment to the root of the lungs and the pericardium. From these fibres he derived the mammalian diaphragm.

In 1906 Keith added fibres from the deep layer of the rectus in these amphibians, and these he homologised as the costo-sternal fibres of the diaphragm of man.

The actual recognition of this amphibian “diaphragm” was, however, due to the researches of Humphry, who published his observations on the muscles of the Cryptobranch in the sixth volume of the Journal of Anatomy and Physiology. In this paper (republished in Observations in Myology, 1872), he says: “There can, I think, be little doubt that the crura of the diaphragm in mammals are formed by the lumbar parts of the subvertebral rectus bending downwards on the sides of the aorta and encircling it, and that the lateral parts of the diaphragm are in a like manner formed by an inflection of the lateral parts—the depressores costarum and transversalis parts—of the same sheet.”

The sheet that is alluded to in this description is the whole transverse layer, the “subvertebral rectus” being the posterior fibres of the sheet running in the long axis of the body, and the “ transversalis part,” the fibres running at right angles to the long axis of the body, and which are applied to the sides of the coelomic cavity. The depressores costarum are the fibres running to the ribs that are, as Humphry recognised, like the fibres of the triangularis sterni, also derived from the transversus layer.

The amphibian “diaphragm” is therefore a derivative of the most anterior portion of the transversus sheet, and this diaphragm is the anterior limit of the coelomic cavity (see fig. 10). The amphibian “diaphragm” on contraction exerts a pressure upon all the body viscera; the lungs and the whole alimentary tract are situated below this diaphragm, and are all subjected to its pressure.

Fig. 10. — The diaphragm of the frog. The anterior abdominal wall has been reflected upwards and the abdominal viscera removed: the lungs and cesophagus are seen cut. The convergence of the fibres of the transversus layer is seen at the cephalic end of the coelom : the lungs being caudad to the cephalic extension of the transversus sheet (diaphragm),

The mammalian diaphragm also appears to belong to the same sheet of muscles, the crura being derived from the posterior longitudinal fibres (“subvertebral rectus”), the costo-sternal slips from the anterior longitudinal fibres (“deep layer of the rectus”), and the remaining costal fibres from the transverse part (transversus proper) (see fig: 11).

It would therefore appear as though the amphibian transversus “diaphragm” had migrated backwards in the Mammalia, causing a subdivision of an originally single pleuro-peritoneal cavity.

There is, of course, every indication that this is the actual process involved.

Fig. 11. — The costo-sternal fibres of the diaphragm of a human fetus of five months, showing the arrangement of the transversus sheet (B), entering into the diaphragm (C), and the triangularis sterni (A).

In the first place, the innervation of the mammalian diaphragm indicates that the sheet is derived from a cervical segment; and in the second, the caudal migration of the diaphragm is a process which is well recognised in embryology. The well-known diagram of Mall (reproduced at fig. 12) depicts the vertebral level of the diaphragm in a series of embryos of different ages, and makes clear this caudal migration in the early stages of the development of the human embryo.

In an embryo of 2:1 mm. the rudiments of the diaphragm are situated in the anterior end of the coelom opposite the upper cervical segments, and it is not till the embryo has reached a length of 15 mm. that the muscular sheet has migrated caudad so far as the lower dorsal region.

Two very interesting reconstructions of human embryos exhibited by Professor Peter Thompson (Brit. Med. Assoc., 1912) show two stages of the migration of the diaphragm with great clearness, and also help to make plain some very confused points in the nomenclature of the various structures which take a part in separating the thoracic from the abdominal coelom.

Fig. 12.—Diagram to show the vertebral level of the diaphragm in embryos of different ages (lengths in millimetres) after Mall.

The conditions shown are, briefly, as follows :—

The younger embryo of 25 mm. was of the third week, and the liver outgrowth had invaded the septum transversum which was opposite the fourth cervical segment, and no so-called “pulmonary ridges” (Mall) were present. The older embryo was of the first month, and the diaphragm was separated by some distance from the origin of the phrenic nerves in the fourth cervical segment. Two ridges, “the pulmonary ridges,” connected the diaphragm to this segment, and these two ridges were caused by the phrenic nerves. Since these “pulmonary ridges” (subdivided into pleuropericardial and pleuro-peritoneal membranes) have had a certain importance ascribed to them as factors in closing the coelomic compartments, it is as well to realise that they are merely the stretched-out fourth cervical (phrenic) nerves in the matrix of the septum transversum into which they originally grew when that structure was at their vertebral level.

It is also to be noted that in the embryo of one month, although the diaphragm was so far perfected as to be free from the liver outgrowth, and already sunk far caudalwards from its original segment, it still occupied a position cephalad to the lung buds which were, at the end of the first month, still abdominal organs exactly as in the Amphibia and Reptilia.

The lower dorsal region becomes the permanent site of the septum transversum in all the mammals, for the diaphragm is always situated as far caudad along the animal body as the ribs extend. Upon the dorsal aspect of the body and upon its sides the diaphragm may therefore extend for a variable distance, since the rib series of the mammals varies from nine to twenty-four pairs.

Upon the ventral aspect its caudad migration is normally limited to the posterior extremity of the sternum; but it was noted long ago by John Hunter that in Delphinus the diaphragm transgresses the limits of the abbreviated sternum and “is attached some way down on the inside of the abdomen.” Nevertheless, despite this trespass of the sternal fibres, the diaphragm of the Cetacea is remarkably oblique, its cephalic surface being directed towards the dorsum of the animal.

==The Separation of the Diaphragm from the Cervical Region.

Although for the sake of simplicity I have pictured the diaphragm as migrating caudad from the neck region, I do not imagine that this is necessarily the correct interpretation of the process. It is quite certain that the fourth cervical segment and the rudiments of the diaphragmatic musculature are originally in apposition, and that the nerve elements from that segment extend into the diaphragm. It is equally certain that in the adult these two structures become widely separated; but it is probably nearer the truth to say that the fourth cervical segment grows away, cephalad, from the diaphragm than that the diaphragm migrates backwards.

The head region has extended further forwards from the site of the diaphragm by an enlargement of the dorsal region—a process which I take to be evidence of the evolution of the pleural cavities for the reception of the extra-coelomic lungs.

This stretching out of the thoracic region is manifest in many wellknown anatomical facts. Thus the supra-diaphragmatic heart and the infra-diaphragmatic liver retain their primitive relationships to each other and to the abdominal region, as represented by the yolk sac and umbilicus. The comparative growth is again manifested, not only in the nerve supply of the diaphragm, but also in that of the heart and abdominal viscera. This aspect of the question cannot be discussed here, but it is teeming with suggestive anatomical conditions.

One relation that perhaps has a more than usual interest is the constant apposition of the cartilaginous xiphisternum to the pericardium, to which it is bound by the inferior sterno-pericardial ligaments. It would seem that this portion of the sternum is on a different morphological (as it is on a different anatomical) plane from the rest of the sternum, for it bears an intimate relation to the heart and pericardium throughout all their changes in position. In searching for the true morphology of the sternum, I should imagine that the pre-sternum and meso-sternum have to be reckoned as distinct from this precardiac portion.

The Primitive Functions of the Diaphragm

The line of argument that we have followed has led us to believe that ribs, at any rate, were not introduced into the animal series for the purposes of respiration with air-breathing lungs; since ribs appear in the vertebrate series before lungs are developed, and lung-breathing is carried out in many animals in the entire absence of ribs. The same train of thought applies to the diaphragm. A muscular post-pulmonary diaphragm does not exist in a host of animals in which lung-breathing is carried on as a normal life process. It is therefore difficult to believe that in the Mammalia this muscle was introduced solely for respiratory purposes.

Amongst the lung-breathing vertebrates we have seen that the Amphibia mostly swallow air by forcing it into their lungs by the compression of their buccal musculature. Most members of the Reptilia draw air into their lungs by the expansion of any portion of the walls of their body cavity ; while the highly specialised Chelonia make respiratory movements with their free limbs and their mobile head and neck.

Among the Aves respiratory movements are mostly abdominal, for the air is passed backwards and forwards across the pulmonary tissue by the filling and emptying of the abdominal air sacs. Such abdominal movements are especially obvious in a chicken suffering from “gapes,” for in such cases the forced efforts of respiration are well seen, and it is evident that the essential respiratory portion of the coelom is the yielding abdominal wall.

Now, all these animals, although their breathing movements are carried out without any regard to the presence or absence of a “diaphragm,” nevertheless possess some rudiments of that structure which is ultimately destined to become the basis of the mammalian diaphragm.

The essential representative of the mammalian diaphragm is present in all vertebrates, although its influence upon the filling or emptying of the lungs is very varied. In some types it empties the lungs, in some it fills them, and in some (Chelonians) it may perform both functions.

This muscular sheet, therefore, does not perform a constant réle in regard to the respiratory movements among the different vertebrate classes, and the question naturally arises, Is there any function which this muscular layer does constantly subserve? It seems obvious that this function is the elemental one of compressing the coelom: and perhaps this muscle is most correctly regarded as a simple instrument for raising the general intracelomic pressure. In some animals the lungs are within the general coeelomic cavity, and are therefore subject to the pressure effects of this muscular sheet, and in some the lungs are in a separate compartment and so are not compressed by the contractions of the muscle. In all the Mammalia the lungs are removed from the compression influence of the diaphragm sheet, and only the abdominal viscera proper are subject to its pressure, while in most other vertebrate classes, the lungs, in common with the other viscera, are equally influenced by the movements of the diaphragm. The problem as to the evolution and perfection of the mammalian diaphragm would therefore seem to be centred in this change of animal economy.

The primary reason for this removal of the lungs from the general coelom, and from the compressing influence of the diaphragm, would seem to be the increasing need for a high intra-coelomic pressure which is manifest in the evolution of the Mammalia. I think that it is not beyond probability that the association of the mammalian condition of the coelom with the mammalian condition of the cloaca may be a functional one, and may prove to be the solution of the problem.

Among the Amphibia, Reptilia, and Aves it is probable that the intracoelomic pressure is never very great, since the simple condition of the posterior visceral outlets permits an easy extrusion of the visceral contents. The evolution of the musculature of the pelvic floor which guards the posterior visceral outlets supports this supposition ; for there is a steadily developing perfection of the visceral sphincters manifested in the ascending vertebrate scale. Like so many other questions in connexion with the evolution of the coelom, this history of the development of the visceral sphincters becomes bound up with the many adaptations brought about in the animal body with a change from an aquatic to a terrestrial mode of life. For it is at once apparent that some raising of coelomic pressure is necessary in order to expire the air from lungs, when once gill-breathing is finally abandoned. Air-breathing is the first stimulus for the creation of a heightened internal pressure, and it leads to the first stage in the evolution of the musculature of the visceral outlets; increased general bodily activity adds to the heightened pressure: but the mammalian subdivision of the simple cloaca is probably the greatest factor of all.

Among all the non-mammalian vertebrates the urinary, genital, and alimentary products are extruded through the simple cloaca; and this simple cloaca is guarded by a common sphincter muscle derived from the caudo-pelvic musculature. Alimentary débris is, as a rule, not bulky in proportion to the size of the animal. Only the Chelonians among the reptiles, and the more rigidly vegetarian groups among the birds pass at all large feecal masses. Urinary excreta, again, are ejected, in the great majority of cases, as small solid masses of uric acid appended to the feces. The genital products are passed along the oviducts and into the cloaca in most instances as eggs, which bear a varying, but never overwhelming, proportion to the size of the parent individual.

An enormous change, however, comes over the animal economy with the evolution of the Eutherian mammals, and I think it is quite certain that every factor in this change is one that makes an increasing demand upon a high intra-coelomic pressure.

Firstly, the cloaca, which served as a common orifice for all the visceral outlets, becomes subdivided, and urinary, alimentary, and genital products are now extruded through separate openings; and moreover, whilst the old visceral sphincter (levator ani) still retains its control, new sphincters are added to guard each separate orifice. The faeces become more bulky, the liquid urine is extruded through a muscular urinary passage, and, above all, the habit of egg-laying is abandoned and living young are produced.

The production of living young is doubtless an important factor, for, though some of the Sauropsida are also viviparous, and some of the most primitive mammals are oviparous, it is probable that these exceptions do not disturb the general connexion between the creation of a high intraecelomic pressure and the production of living offspring. Ornithorhynchus and Echidna extrude eggs from separate oviducts into a single cloacal chamber, in this respect falling into line with the Sauropsida. In the different members of the Marsupialia the evolution of viviparous habits is beautifully seen, and has been made clear by the study of the reproductive habits of Perameles by Professor J. P. Hill, Hand in hand with this evolution the perfection of the diaphragm increases.

I regard the diaphragm, therefore, as an organ for producing that heightened intra-coelomic pressure which is necessary for the expulsion of the abdominal contents in the Mammalia. The life activities of these animals demand that their coelomic pressure should be high, and the compressor layer of the coelom wall (transversus layer) has become proportionately strengthened for the creation of this pressure. But hand in hand with this development there comes about a changed position of the diaphragm in the body; and I am in agreement with those who account for this change by supposing that the lungs have in a manner herniated out from the general coelomic cavity ; and this herniation, I should suppose, was caused as a direct consequence of the increased coelomic pressure. The process by which the lungs are extruded from the coelomic cavity has been likened to the descensus of the testicle, and I imagine that the simile is a true one.

The Primitive Action of the Diaphragm and the Abdominal Muscles

The transversus layer acts as a simple compressor of the coelom in the frog. The diaphragm acts primarily in the mammals in the same way upon that portion of the celom which is still subjected to its pressure effects. In the Mammalia its action is best likened to that of the plunger of a piston, for its central part descends upon the abdominal cavity and tends to drive its contents onwards.

Now, it is obvious that when the diaphragm descends, its force may be expended in two ways, for it may merely protrude a flaccid abdominal wall ; or, this wall being held rigid, it may increase the internal pressure and help to expel the abdominal contents.

Concerning the action of the abdominal muscles of man there is a wearying unanimity in the majority of text-books of anatomy: “Their chief action is to retract the abdominal walls, and, by compressing the contents of the abdomen, they are powerful agents in vomiting, defecation, micturition, parturition, and laboured expiration” (Cunningham): this may be taken as the typical teaching of modern English text-books.

And yet I do not think that this account gives the real meaning of the action of the abdominal muscles of man; for in all expulsive abdominal efforts they appear to act far more as resisters than as creators of intracoeelomic pressure. It is true that the abdominal muscles can contract and so retract the abdominal walls — young children and many Oriental mountebanks can do this to a surprising degree; and this action is also seen in the “scaphoid belly” of acute abdominal disease.

Nevertheless, it is true that in ordinary abdominal expulsive efforts the abdominal wall is not so retracted; and to imagine that the abdominal contents are expelled by retraction of the abdominal walls appears to me to be an entirely wrong interpretation of the true facts.

Intra-abdominal tension is raised in expulsive efforts, not by the contraction of the abdominal muscles, but by the descent of the diaphragm ; and the abdominal muscles merely contract in order to keep the abdominal wall rigid to withstand the pressure created by the diaphragm.

It is well known to every clinician that when the abdominal muscles do not perform this function there is a difficulty in all expulsive abdominal efforts, not because the abdominal muscles fail to compress the abdominal contents, but because they yield before the expulsive efforts of the ‘diaphragm, and so render its contractions unavailing. The question is, in reality, a very simple one and has only to be put to the test of practice, for it is easy to contract the abdominal muscles as far as voluntary efforts permit, and note that no expulsive tendency is produced; while, on the other hand, it is equally easy to contract the diaphragm and note that the abdominal muscles at once respond by making the abdominal wall unyielding, and a very definite expulsive effort is the result.

The role of the abdominal muscles in this act I regard as being very similar to that of the intercostal muscles (both external and internal). Many réles have been assigned to these layers, and opposed functions have been imagined for the separate sheets of the intercostal muscles. And yet the question seems best solved, as modern French anatomists solve it, by saying: “Leur réle comme inspirateur ou expirateur est tout a fait secondaire, s'il existe. Ils interviennent par leur tonicité, leur élasticité et leur contraction, pour résister; pendant l’inspiration, a la pression atmosphérique; pendant |’expiration, 4 la pression intrapleurale. Quand ils sont paralysés, l’espace intercostal se déprime ou bombe, suivant le moment de la respiration” (Saulieu et Raillere). I think that there is no better statement than this for conveying the correct idea as to the functions of these muscles; and I regard their réle as one entirely similar to that of the abdominal muscles in their function as muscles of the coelom wall. The ribs, the intercostal muscles, and the abdominal muscles (more especially the obliquus internus) function as resisters of pressure either within or without the coelom. With the diaphragm the case is quite otherwise, for the very simplest experiments in one’s own person will make clear the pressure influence which it is able to exert; and a much more convincing evidence of its real function may always be observed during the third stage of labour. Many of the simple devices of obstetricians and midwives for assisting the third stage of labour are directed to giving free play to the action of the diaphragm, and to permitting a fixation of the abdominal muscles. It is in the management of the third stage of labour that the true réles of these two sets of muscles are always tacitly acknowleged. Post-mortem evidence may. also be obtained of the action of the diaphragm in the expulsion of the foetus. I have seen in many cases multiple hematomata of the diaphragm in women who have died either in childbirth or after confinement. Even in a woman of 37 who aborted at 43 months, as the consequence of an operation, the diaphragm was markedly thicker than that of a virgin of 19 examined on the same occasion ; and, in addition, the diaphragm of this woman showed ‘a series of large hemorrhages in the muscular portion, each hemorrhage being due to the rupture of muscular fibres.

From the evidence at my command (which I readily acknowledge is altogether insufficient to warrant dogmatic statements), I should think it highly probable that some hypertrophy of the diaphragm takes place during the later months of pregnancy, and of the severe expulsive efforts of the muscle at the completion of pregnancy there can be no doubt.

I therefore regard the diaphragm of mammals as the muscle for producing intra-abdominal pressure, and the muscles of the abdominal wall (especially the obliquus internus) as the resisters of this pressure ; these are the functions that the midwife recognises in the human female when, during the third stage of labour, she directs her patient to try to blow the bottom out of a soda-water bottle, and at the same time puts on a binder to assist the muscles of the abdominal wall if they be flaccid.


The primary function of the diaphragm, and of that muscular layer from which it is derived, is, as we have seen, the compression of the coelom. In Reptilia and Amphibia it compresses the lungs, since they are within the general coelom, and so it acts as an expiratory muscle.

We have also seen that there is a change in the method of inspiration in the transition from Amphibia to Reptilia, for while the Amphibia, as a rule, swallow or pump air into their lungs, the Reptilia suck in air by the creation of a negative pressure within the coelom. This is a most important change in animal economy, for while the pumping method tends to drive air into the lungs it also tends to drive blood out; whereas the sucking method tends to fill the lungs with both air and blood. There is, therefore, a far more efficient respiratory mechanism in the Reptilia than is found in Amphibia; and this more efficient mechanism is brought about by the action of derivatives of the outermost of the body muscle layers— or by the “external respiratory system” of Charles Bell. In the Mammalia, however, a further perfection of the respiratory apparatus is developed, for the lungs, having once left the general coelomic cavity, come to lie within a space (the pleural cavities) which is under the most perfect control of the external respiratory system, and which is cut off from the fluctuating increases of pressure brought about in the abdominal coelom.

When the “external respiratory system” of the Mammalia is brought into play only the lungs and the great vascular channels are subjected to the negative pressure created; whereas in the Reptilia all the body organs, including the whole of the alimentary tract, share in, and help to dissipate, this negative pressure.

The Mammalia therefore possess, in the action of the “ external respiratory system ” alone, a more efficient respiratory mechanism than do the Reptilia. In the Mammalia, however, or at any rate in a great number of them, there is also another inspiratory factor added ; and this new factor—the diaphragm or “internal respiratory system” of Charles Bell—makes the mammalian process of respiration an enormous advance on anything displayed by the Amphibia or by the Reptilia.

At each descent of the diaphragm in the Mammalia the intra-abdominal pressure is raised; but at the same time, of course, the intra-thoracic pressure is lowered ; and so the diaphragm becomes a muscle of inspiration as well as one of abdominal compression.

The réle of the diaphragm as an inspiratory muscle is a highly important one, but it must be remembered that it is an entirely secondary one, and the actual importance of the diaphragm as a respiratory muscle varies among the Mammalia. The Carnivora, as a whole, are usually credited with a greater dependence on the more primitive external respiratory system than are the Herbivora, in which it is generally held that the diaphragm plays a more important réle. Be this as it may, still, despite a great lack of actual experimental knowledge, it is an ascertained fact that even the horse is able to carry on all its ordinary respiratory movements in the complete absence of the action of the diaphragm. Both phrenic nerves have been divided in.the horse, and “the animal, after the first temporary increase in the frequency of the breathing had disappeared, could be driven in a light vehicle without any marked dyspnea” (Manual of Physiology, Stewart, 4th ed., p. 212). Although the respiratory symptoms are soon recovered from in a horse with divided phrenics, a symptom that becomes of increasing severity is the collection of feces in the rectum—and this is a very interesting point. It is highly probable that what has been proved by experiment to be true in the horse is equally true of practically all of the pronograde mammals; and it is also highly probable that the rib-breathing Carnivora can more easily dispense with the respiratory action of the diaphragm than can the diaphragm-breathing Herbivora.

And yet in man the case is very different, for section of the phrenics, or trauma involving these nerves, is fatal. A man can live with his external respiratory system completely in abeyance (Hilton), but he cannot live with his internal respiratory system inactive (Bell).

It would therefore seem that man has a greater dependence on the diaphragm as a respiratory muscle than have the pronograde mammals. The work of Charles Bell is of particular interest in this respect. Hilton has recorded a case in which a man lived an active life although the ribs were completely immovable: a case showing that the action of the human diaphragm was so important as a respiratory factor that it alone sufficed to carry on all the respiratory needs of the body. But Charles -Bell has described in most graphic language the condition of a man (Case CXLIV.) in whom, owing to a fracture of the cervical vertebra, the diaphragm was put out of action. This man lived for half an hour. “Every time he drew his breath it was attended with an effort to raise his shoulders, and a contraction of the muscles of the throat: every time he breathed, his head appeared to sink beneath his shoulders. On putting the hand on the pit of his stomach no motion of the viscera of the abdomen could be perceived.”

Another interesting case in this connexion is one described by William Thorburn and James Gardner (Brain, 1903, p. 120), in which a tumour of the axis vertebra involved certain cervical nerves. In this man “it is probable that the left phrenic nerve alone was completely paralysed,” and that “the diaphragm continued to act slightly ”; but its action must have been considerably impaired and its “movement could not be detected.”

Under these circumstances respiration was carried on by the muscles of the external respiratory system: it was noted that the sterno-mastoids and trapezii acted vigorously in respiration, which was maintained at the rate of 28 to the minute, and that “at each breath the chest was drawn upwards like a solid, unexpanding mass.” This case presents a remarkable likeness to the previous one, save that the right phrenic nerve in this man probably remained in part functional.

The Reason for the Paramount Importance of the Respiratory (or secondary) Function of the Diaphragm in Man and some other Mammals

We have seen that the external respiratory system will suffice for carrying on all the respiratory functions in some pronograde mammals, as the horse and the rabbit; and we have reason to suppose that probably all pronogrades could survive section of the phrenic nerves. We have also seen that in man, even when the external respiratory system fails to act altogether, death does not ensue; while total paralysis of the internal respiratory system produces death from respiratory failure. The unavoidable conclusion is therefore that the primitive (pronograde) mammal is dependent upon the external respiratory system; while man has become dependent upon the internal respiratory system.

It therefore becomes necessary to seek the reason for the paramount importance of the human diaphragm as a respiratory muscle—an importance which has led anatomists, physiologists, and clinicians to regard this muscle as the essential respiratory mechanism of the Mammalia. I think that

Fic. 13.—Diagram of a pronograde mammal to show the action of the muscles passing from the fixed fore limb and shoulder girdle to the movable ribs.

there can be no doubt that it is the loss of fixation of the shoulder girdle and fore limb in man that has brought about this change. I regard the loss of fixation of the fore limb as the cause of the waning importance of the external respiratory system and the consequent waxing of importance of the internal respiratory system. The majority of the muscles of the external respiratory system pass from the fore limb and shoulder girdle to the ribs, and, in the pronograde mammals in which the fore limb is a fixed point, act from the fore limb and shoulder girdle upon the ribs.

A horse elevates its ribs, and so has an efficient external respiratory system by pulling its ribs towards its fixed fore limb and shoulder girdle (see fig. 13). In man, however, with the loss of the fixation of the fore limb, the muscles that pass between the ribs and the shoulder girdle and fore limb act upon the movable fore limb from the ribs as a fixed point (see fig. 14). In the language of descriptive anatomy, the origin of the muscles in the pronograde becomes their insertion in the orthograde. As an example of this the serratus anterior will suffice. In man, this muscle,

Fig. 14. — Diagram of an orthograde mammal (man) to show the action of two muscles passing from the more fixed ribs to the movable fore limb and shoulder girdle.

when acting, produces a round arm lunge, an action foreign to the pronogrades, in which the contraction of the muscle produces an elevation of the ribs towards the fixed scapula: the serratus anterior of man pulls the shoulder girdle ventralwards round the ribs, while in the pronogrades it pulls the ribs dorsalwards to the fixed shoulder girdle.

The muscles which were the chief agents of the external respiratory system of the pronogrades have therefore become mere factors in producing movements of the arms in orthograde man. These facts are, of course, well known to every clinical observer; for it is one of the commonplaces of clinical, or even lay, experience that in times of any respiratory distress there is an attempt to so revert to the pronograde condition as to effect a fixation of the fore limb and shoulder girdle. In asthma, emphysema, and a variety of other pathological conditions in which there is a difficulty in respiration, the patient will grasp the back of a chair or the edge of the table in order to fix the fore limb, and so give full play to the external respiratory muscles in the pronograde position. A runner at the end of a race will grasp his thighs with his hands for the same reason.

There is therefore an attempt manifested in all cases of obstructed

Fic. 15.—Diagram of an aquatic mammal to show the action of the muscles passing from the more fixed ribs to the movable fore limb and shoulder girdle.

respiration to assume the pronograde position, and so, by the fixation of the fore limb and shoulder girdle, to call the external respiratory system to the aid of the internal respiratory system. Indeed, one cannot help thinking that, from the accounts of the manner of death of persons dying from total diaphragmatic paralysis, life in such cases could be at any rate prolonged by an effectual fixation of the fore limb and shoulder girdle as a point of origin for the muscles acting upon the ribs.

Now, it will be at once apparent that although man is a familiar instance of the loss of fixation of the fore limb and shoulder girdle—and an instance in which the pathological conditions have been well studied,— there are other members of the mammalian series in which such fixation of the fore limb is equally lost. The members of the Cetacea at once come to mind, for in them the fore limb has become reduced to a mere paddle which, owing to the aquatic habits of the animals, has lost altogether its pronograde fixity as a point of origin for thoracic muscles (see fig. 15).

It is of the greatest interest in this connexion that it was noted by John Hunter that in these animals the diaphragm reached its maximum of development, and the reason he assigned for its great muscularity was that the air had to be inspired against the resistance of the surrounding water pressure. The facts were again noted by Owen, who stated that “the diaphragm is most muscular, longest, and most oblique in Cetacea, in which the central tendon is almost obsolete.”

Of the anatomical fact there is no doubt—the Cetacea have an unusually highly developed and highly muscular diaphragm ; but that John Hunter’s is the only, or the correct, explanation of the fact is open to question. Since all these aquatic animals must inspire their air at the surface of the water, the water pressure surrounding their bodies cannot be very great; it is therefore unlikely that the great muscular strength of the diaphragm is developed solely for this reason. It seems to me to be highly probable that it is the loss of fixation of the fore limbs, which has deprived the external respiratory system of its efficacy, that has resulted in the great development of the internal respiratory system in the Cetacea.

I therefore regard the high development of the diaphragm in the Cetacea and other aquatic mammals as being due, not to the pressure of the surrounding water, but to the loss of fixation of the fore limbs and shoulder girdle, and as being strictly analogous to the same high development in man. I know of no direct evidence upon the point, but I should regard it as almost certain that section of the phrenic nerves would be inevitably fatal in a Cetacean.

Other comparisons may be instituted, and to this end I examined, when in Manchester, the condition of the diaphragm in other mammals in which there is, at any rate, some tendency to assume an orthograde posture.

One cannot help being struck by the extraordinary human characters of the diaphragin of Macropus, and its contrast to the condition exhibited by its more strictly pronograde marsupial allies. By a comparison of the diaphragm of a foetal Macropus and a foetal Perameles it is impossible to escape the conclusion that posture, rather than zoological affinity, determines the characters of this muscle.

Again, there is a marked difference of diaphragmatic development between the Dipodide and the members of the genera of more strictly pronograde smaller rodents. The jerboas have a very highly specialised, and very human diaphragm, and I imagine that it is the alteration in posture that has caused them to develop a more human type of diaphragm than, for instance, the fairly nearly allied rats.

Kangaroos and jerboas spend a considerable portion of their time with the fore limb free of the ground (and therefore useless as a point of origin for the muscles of the external respiratory system), and for this reason I imagine there is a greater development of the internal respiratory system in these animals—a development seen in the greater perfection of the muscular diaphragm.

Again, we have, so far as I know, no direct evidence on this point; but I imagine that Perameles or Mus could survive section of the phrenic nerves far more readily than could Macropus or Dipus, in which a semiorthograde habit and a greater dependence upon the internal respiratory system have been, at any rate, partially assumed.


It will be at once apparent that if the loss of fixation of the shoulder girdle brings about such marked changes in the mechanism by which respiration is effected, then some marked modification of the reptilian method of breathing should have taken place among the birds. A bird, under most circumstances, has lost the use of the fore limb and shoulder as a fixed point, and it might be argued that they, too, should possess a diaphragm. In some measure this expectation is verified. John Hunter (Works, vol. iv. p. 177) said: “It has been asserted that birds have no diaphragm ; but this opinion must have arisen either from want of observation, or from too confined an idea of a diaphragm: for there is a moderately strong, but thin and transparent membrane covering the lower surface of the lungs, and adhering to them, that affords insertion to several thin muscles which arise from the inner surfaces of the ribs.”

This is, of course, a perfectly accurate statement of the actual condition of the avian diaphragm, and, moreover, the “thin muscles” which compose it are again derivatives of the transversus sheet.

There is therefore a strong initial resemblance between this avian diaphragm and the typical diaphragm of the mammals; and yet in this feature, as in so many others, the Aves as a class show themselves to be extraordinarily specialised from those conditions which may be considered as primitive. The birds, as a consequence of the loss of fixity of the shoulder girdle, have needed a modification of the respiratory methods which were sufficient for the pronograde reptiles, and they have gained this modification by the adaptation of some typical reptilian characteristics. The orthograde mammals, which have already, and for other reasons, evolved a transversus diaphragm, have adapted this transversus sheet to the purposes of respiration. The birds have also adapted a transversus sheet to respiratory ends, but I imagine that the routes taken, and the functional end arrived at, are very different in the two cases. In the first place, although in development the avian lungs are at one time subdiaphragmatic, the avian diaphragm is innervated by dorsal and not by cervical nerves. There is no phrenic nerve in the Aves. These facts would seem to demonstrate that though Aves and Mammalia had both used the transversus sheet—that sheet that always compresses the coelom,—they have made use of different portions of the sheet with which to subdivide their pleuro-peritoneal cavity.

Again, in lung development Mammalia and Aves have evolved along quite different lines, and the different developments have led to totally different functional results. ,

Mammals have perfected a simple type of lung, which may be defined roughly as a uniformly expansile and uniformly blood-aerating pulmonary membrane. Aves have perfected a type of lung, long foreshadowed in Reptilia, in which the blood-aerating and the expansile functions are separated and specialised.

The special features of the avian lung are brought about by the enormous development of the air sacs as mere expansile structures, while the true pulmonary tissues in which the respiratory exchanges are carried out remain as a compact and confined mass. When a bird inspires it does not to any extent expand its lungs, but it draws air through its pulmonary tissues by the expansion of its air sacs: in the same way expiration takes place by compression of the air sacs and expulsion of the air through the lungs, bronchi, and trachea. These air sacs are, for the most part, extra-thoracic structures, and the most important of them are situated within the general abdominal colom. We have, therefore, a curious elaboration of the respiratory mechanism of the reptiles ; for compression of the abdominal coelom is expiratory in effect, and expansion is inspiratory in Aves, just as it was in the lower orders. .

Changes have been brought about in birds by reason of the specialisation of the thoracic skeleton; but notwithstanding these changes, it may be said that in essential details the respiration of birds is merely an advance along typical reptilian lines. The general compression of the coelom by its compressor muscles still produces an expiratory effect ; but a greater functional perfection is secured in that the lung itself is extracoelomic, and so, in part at any rate, it is shielded from this pressure.

Expiratory efforts in the bird are made by compression of its air sacs, and not by compression of its lungs. In this way a bird can expire air with some force, but it cannot accomplish anything approaching to a mammalian cough. The laboured expiratory efforts are easily followed in young birds suffering from obstructed respiration, as in a chicken dying of “gapes”; but the mechanical disadvantage of the avian type of respiration is demonstrated by the degree of pneumonia, which would be trivial in a mammal, but which is rapidly fatal in a bird.

In Apteryx alone is there any real approach to the mammalian condition ; for this aberrant bird has no abdominal air sacs, and, in conformity with this feature, “the diaphragm presents more of its mammalian character than in any other known bird” (Owen, Comp. Anat., vol. ii. p. 91).

Some Clinical Bearings of the Human Condition of Diaphragmatic Function

It will readily be understood that the human condition of the diaphragm, the loss of fixity of the shoulder girdle, and the orthograde condition, bring in their train many specialisations which are of the utmost interest, but which scarcely come within the scope of the present paper. Yet some should be mentioned, for it has been customary to regard many conditions as pure outcomes of the upright position, without allowing a due share in their causation to the altered action of the mechanism of respiration. Many of these side issues are of distinct clinical interest, and it has seemed to me possible that a better understanding of the real nature of the diaphragm and its specialised human condition may lead to a more correct appreciation of some clinical problems. This side of the question must, however, await further discussion.

In the first place, the constant state of antagonism that exists between the piston action of the diaphragm and the resisting abdominal. muscles has to be reckoned with in all those cases, which constitute an important class, in which a yielding abdominal wall causes a difficulty in expulsion of abdominal contents, evidenced, it may be, by chronic constipation or by difficulty in the third stage of labour. The localised yielding of the abdominal wall in hernia must also be considered in connexion with diaphragmatic action; the pressure-raising muscles have already caused two normal herniz—the testicles and the lungs,—and are still potent to cause abnormal ones.

Again, the interpretation of the large class of cases in which the diaphragm has, perhaps from loss of proper antagonism, sunk to a level below its normal, and produced a resulting condition of enteroptosis, seems to depend upon a proper understanding of the true (primitive) function of the diaphragm.

Apart from these cases in which the interaction of the diaphragm and the abdominal muscles plays a primary part—cases in which the symptoms are chiefly abdominal, since the diaphragm is acting in its primitive réle— are those in which altered thoracic conditions are present. It may be said at once that in orthograde man there is an attempt to regain in part the fixity of the shoulder girdle by the tonic action of the muscles supporting the fore limb and pectoral girdle. Notable among these muscles are the trapezii by which the shoulder girdle is slung from the hinder part of the skull, and the sterno-mastoids which assist in this action.

A vast number of clinical problems hinge upon this disposition and tonic action of the muscles between the head and neck and shoulder girdle in upright man.

First come those cases in which a failure of this tonic support of the shoulder girdle is accompanied by enteroptosis—a failure of all conditions which aid the external respiratory system, resulting in a dominance and overaction of the internal respiratory system. The normal descent of the shoulder girdle and the part it plays in the late production of the symptoms of brachial neuritis have been described by T. Wingate Todd (Anat. Anzeiger, 41. Band, p. 385, 1912); and it must also be noted that in cases of enteroptosis brachial neuritis may be an accompanying symptom (case exhibited by Keith, College of Surgeons Lectwres, 1912).

Another manifestation of the loss of this human support of the shoulder girdle is seen in those cases in which corset support to the scapule has supplanted the normal trapezius action, and so produced the condition known to orthopedic surgeons as “ewe neck” (see W. Williams, Reports of Royal Southern Hospital, Liverpool, 1901, etc.).

The questions, however, as well as the morphological significance of the spinal accessory nerve and the importance of its action in relation to diaphragmatic breathing, must await further investigation and discussion.

Cite this page: Hill, M.A. (2024, May 25) Embryology Paper - The functional history of the coelom and the diaphragm (1913). Retrieved from

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