Book - Vertebrate Zoology (1928) 9

From Embryology

Vertebrate Zoology G. R. De Beer (1928)

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Chapter IX Columba: A Chordate with Wings=


The birds are principally distinguished by the possession of feathers, and the modification of the fore limbs into wings. The hind limbs continue to serve for terrestrial locomotion, but it is important to note that although the birds have evolved the habit of standing on two legs only, the body is still carried in a horizontal position. The mouth is toothless but bordered by a horny beak, the external nostrils are on each side of the upper beak, a little way behind the tip. The eyes have upper and lower lids, and also a " third eyelid," or nictitating membrane. The ear-drum is no longer flush with the surface of the skin, but sunk at the bottom of a tube, which is the external auditory meatus. The alimentary and urinogenital systems open at the cloaca. The tail is very much shortened, and on its dorsal side is the uropygial gland. This gland, which is the only one to be found in the skin of birds, produces a secretion with which the bird preens its feathers, and makes them waterproof. There are scales on the legs, and claws at the ends of the toes (in a very few cases also on the fingers), but no dermal ossifications of any kind are present.


The feathers are arranged on the surface of the body in definite tracts, called pterylae. Feathers are formed by the epidermis (see p. 224), and are of different kinds in the various regions of the body. Those visible on the outer surface of the bird are called penna?, which include the quill or flight-feathers and the contour feathers of the adult bird. Their typical structure may now be described.

A penna consists of a stalk (quill or rachis) carrying a vane.


Fig. 54. — View of a portion of a feather to show the structure and relations of the barbs and barbules.

Two adjacent barbs (b) are represented cut off from the stalk. The barbs bear distal barbules (db) on the side away from the base of the feather, and proximal barbules (pb) on the opposite side. The hooks or hamuli (h) on the distal barbules of one barb are attached to the groove on the edge of the proximal barbules of the adjacent (distal) barb.

The vane is made up of a large number of barbs on each side of the central stalk or rachis, and each barb carries a number of barbules on either side. The barbules bear hooks and notches, by means of which the barbules of one barb are attached to the barbules of adjacent barbs. In this way a stiff, air-resisting plane is formed, which is especially well developed in the flight-feathers. The flight-feathers on the wings are called remiges, those on the tail rectrices. The remiges which are carried on the " forearm " (radius and ulna) are the " secondaries," those on the " hand " (carpals, metacarpals, and phalanges) are called the " primaries." Contour feathers cover the body and give it a smooth surface which presents little resistance to the air during flight. They are smaller than flight-feathers, and the hooks or hamuli on the barbules are not so well developed. Contour feathers usually possess an aftershaft, which is like a duplicate vane arising from the base of the rachis. As a rule it is small, but in the cassowary the aftershaft may be as long as the main shaft. The base of the quill beneath the vane is a hollow cylinder, opening below by the inferior umbilicus, and above at the base of the vane by the superior umbilicus. The superior umbilicus is between the main shaft and the aftershaft, which relations become obvious from a study of the development of the feather (see p. 224).

In addition to the pennae there are in most birds down feathers or plumulae. In these the barbules and hamuli are very degenerate so that there is no stiff vane at all. The down feathers form a dense layer which prevents the movement of the air in it, and therefore functions as a non-conductor of heat. This is important because birds are warm-blooded, and without this protection they would lose their heat rapidly by radiation from the skin to the surrounding air.

Some feathers consist only of a slender stalk with scarcely any barbs ; they resemble hairs and are known as filoplumes.

The kinds of feathers described above are characteristic of adult birds, and may collectively be called teleop tiles. In the young birds they are preceded by nestling- feathers, or neossoptiles. Filoplumes, plumutee, and pennse are preceded by preflloplumes, preplumulae, and prepennae, respectively.

Feathers are usually coloured, and since they are dead structures, their colours are due either to pigment which they contain, or to the optical properties of their texture. Feathers are moulted and replaced periodically, which in many birds enables plumages of different type and colour to succeed one another. Flight-feathers are usually moulted in pairs, symmetrically right and left, as a result of which the bird is still able to fly during the moulting period.


The skull of the pigeon, as of birds generally, is strongly ossified, so much so that the bones tend to fuse together and the sutures between them to disappear. The brain-case is much enlarged compared with lower animals. Covering the roof are : nasals, prefrontals, frontals, parietals, and squamosals (membrane-bones). The cartilage-bones of the neurocranium are : basioccipital, supraoccipital, exoccipitals, basisphenoid, laterosphenoids, orbitosphenoids, and ethmoid. The brain-case does not extend forward between the eyes, which are only separated by an interorbital septum. The bones of the auditory capsule fuse and form the periotic.

The parasphenoid of lower forms is represented by the median rostral, and the paired basitemporals, which latter are attached to the underside of the basisphenoid. There is a single occipital condyle.

It is worth noticing that the squamosal now forms part of the wall of the brain-case ; the latter is so much enlarged that the cartilage-bones are insufficient to enclose it (see Fig. 140).

The quadrate articulates with the periotic by an otic process. Stretching forwards from the quadrates are two strings of bones on each side. On the outer side are the quadrato-jugal, jugal, maxilla, and fused premaxillae, all membrane-bones forming the margin of the upper jaw. Median to these, the pterygoids run forwards from the quadrates, and articulate with the basipterygoid processes of the basisphenoid, and with the palatines, which run forwards to the maxillas. Median to them are the small prevomers, fused together in the middle line.

In the lower jaw, Meckel's cartilage is represented by the articular, and the angular, supraangular, splenial, and dentary are membrane-bones.

The hyoid skeleton is represented dorsally by the columella auris, connecting the ear-drum with the fenestra ovalis of the auditory capsule, passing behind the quadrate. Ventrally, the " hyoid " consists of basihyal, ceratohyal, basibranchial, and ceratobranchial of the ist branchial arch.

There are no teeth in the pigeon nor in any living bird.

Vertebral Column

The first two vertebras are the atlas and axis. They are followed by twelve others, forming the cervical region of the vertebral column. The articulation of the centra with one another is of a peculiar saddle-like pattern called heterocoelous, and giving the neck great flexibility. The vertebrae have neural arches, zygapophyses, extra articular facets called hypapophyses, and transverse processes. The ribs articulate with the vertebrae by two heads ; a dorsal tuberculum (fitting on to the transverse process) and a ventral capitulum (touching the centrum). None of the ribs of the cervical vetebrae reach the sternum, and the first ten, carried by vertebrae 3 to 12, are actually fused with their respective vertebrae. In this manner, each of these vertebrae has a little (vertebrarterial) canal on each side. Cervical ribs of vertebrae 13 and 14 are free.

There are five thoracic vertebrae, of which the first four are fused together, and the last is fused on to the next posterior vertebra (ist lumbar). The thoracic ribs are jointed and are attached ventrally to the sternum. All the free ribs except the last bear processes (uncinate) which overlap the next posterior rib, and help to give strength to the thoracic box.

The lumbar vertebrae are six in number, and they are fused in front with the last thoracic, and behind with the two sacral vertebrae, and the first five caudals. In this way an extensive sacrum is formed, to which the ilia of the pelvic girdle are attached, strong enough to stand the leverage on the ilia due to the horizontal position of the bird's body with the legs at the hind end.

After this come six free caudal vertebrae, and then four more all fused up together to make the pygostyle.

Pectoral Girdle and Limb

The shoulder girdle is formed of scapula and coracoid (cartilage-bones), and a clavicle (membrane-bone) which meets its fellow from the other side in the middle line to form the furcula, or " merrythought.'* The scapula extends backwards over the ribs ; the coracoid is attached to the sternum. Where the scapula, coracoid, and clavicle meet, they enclose a foramen (triosseum) between them, which acts as a pulley through which the tendon of the minor pectoral muscle passes, to be inserted on the humerus and so raise the wing.

The sternum is remarkable for its relatively enormous median keel or carina. On each side of it the pectoral muscles are inserted. Of these, the minor pectoral muscles have been mentioned above ; the major pectoral muscles pull the wing down and in so doing lift the bird in the air. The difference between " red meat " and " white meat " can be well shown in the pectoral muscles of different birds. Muscles which perform long-continued actions are rich in sarcoplasm and haemoglobin, and are therefore red. Other muscles, the action of which is not continuous, are poor in sarcoplasm, and their fibres are therefore white in colour. The falcon is a bird which spends long periods on the wing, during which its pectoral muscles are in continuous activity. It is not surprising to find therefore that these muscles are " red meat." On the other hand, the domestic fowl does not use its pectoral muscles continuously, and they are white.

The skeleton of the wing consists of humerus, radius, and ulna. The wrist and hand are somewhat modified ; there are two free proximal carpal bones, the radiale and ulnare ; but the distal carpals have fused with the three fused metacarpals to form a carpo-metacarpus. The first digit is represented by a phalanx bearing feathers which form the " bastard wing." The remaining two digits have two and one phalanges respectively, and they, together with the carpo-metacarpus, bear the primary remiges.

Pelvic Girdle and Limb

The pelvic girdle is at first sight different from that of any animal so far described. The acetabulum is perforated, and is formed from the usual three bones, ilium, ischium, and pubis. The ilium extends forwards and backwards and is attached to the long sacrum. The ischium is fused along the greater part of its length with the posterior part of the ilium, leaving an ilio-sciatic foramen through which the sciatic artery and nerve run to the hind limb. The pubis is remarkable in that it points backwards and runs along the ventral border of the ischium, from which it is separated by the obturator fissure (corresponding to the ischio-pubic foramen, and serving for the passage of the obturator nerve). Neither the pubis nor the ischium extend to the middle line ; they consequently do not meet their fellows of the opposite side, and have no symphyses. The absence of symphyses may be correlated with the fact that birds lay relatively very large hard-shelled eggs.

The femur is short and thick ; covering the front side of its lower extremity is the patella. The tibia is fused with the fibula and with the proximal tarsal bones to form the tibiotarsus. The distal tarsals are fused on to the united metarsals of the 2nd, 3rd, and 4th toes to form the tarso-metatarsus. The 1st metatarsal is small and free ; the digital formula of the phalanges is 2, 3, 4, 5, o (there being no 5th toe). The terminal phalanges bear claws. The first toe is in birds usually directed backwards, and it is opposable to the other digits. This arrangement enables a bird to stand securely on a narrow twig of a tree, with the first toe clasped round behind the twig and the remainder in front of it. The joints of the toes are bent by tendons which run back beneath the foot and up behind the tarso-metatarsus. The more the tarsal joint is bent (in squatting), the tighter these tendons are stretched, and the more strongly are the toes bent. The bird can therefore ensure a tight grip on its perch without effort, and even when asleep, simply by squatting.

It is obvious that the hind limb can bend only at the knee and between what were the proximal and distal rows of tarsals : this extreme form of the mesotarsal joint is the rule in birds.

It is to be noted that the bones of the bird's skeleton are very light, and that most of them are hollow ; some of these spaces communicate with the air-sacs which will be described in connexion with the respiratory system.

Alimentary System

The tongue is small and pointed, and behind it the two Eustachian tubes open into the mouth by a single common aperture. The glottis in the floor of the gullet leads to the lungs. The gullet swells out into the crop at the base of the neck. This is a thin- walled sac in which the food is temporarily stored. The stomach is modified in that the glands are restricted to an anterior chamber, the proventriculus. Following on this is the gizzard, which has thick hard walls, and in which the food is crushed up with the help of stones and grit. The duodenum leads out from the gizzard, and receives the three ducts from the pancreas, and the two bileducts from the liver, which does not possess a special gall- bladder. The intestine is coiled, and leads to the rectum, which bears a pair of cceca. The rectum leads to the cloaca which is peculiar in that it is subdivided into three regions. That into which the rectum opens is called the coprodaeum ; next comes the urodaeum, into which the ureter and genital ducts lead ; and lastly the proctodeum which opens to the exterior. Into the proctodeum opens the bursa Fabricii, a blind sac-like organ of unknown significance.


A knowledge of the relations of the ccelom is necessary for a proper understanding of several of the organs in birds. As in the lizard, the lungs are contained in folds of the ccelomic epithelium which connect with the liver (forming pulmo-hepatic ligaments), but in addition, these ligaments make a connexion with the side wall of the general ccelomic cavity. In so doing, they slant downwards and laterally from the roof of the ccelomic cavity, and are called the oblique septa. They separate a portion of the ccelomic cavity on their upper and outer sides, from the remainder of the perivisceral ccelomic cavity, forming the pleural cavities. Into these cavities the lungs project. The gizzard is connected with the floor of the ccelomic cavity by a post-hepatic septum, so that altogether the cavity of the ccelom is considerably obstructed and divided up. The pericardium is, of course, separated off from the rest of the ccelom by the transverse septum, but it is important to notice that in birds there is no diaphragm (see Fig. 126).

Respiratory System. — The glottis leads into a long trachea or windpipe, strengthened by cartilaginous and bony rings. This trachea divides into the two bronchi, and at the point of division a membrane extends forwards and projects into the trachea from the angle between the bronchi, forming the syrinx, by the vibrations of which birds sing.


Fig. 58.— Columba : ventral view of a dissection to show the air-sacs. a, abdominal air-sac ; at, anterior thoracic air-sac ; c, cervical air-sacs ; co, coracoid ; die, diverticulum of the interclavicular air-sac ; /, iurcula ; ^/humerus (which contains a diverticulum from ic) ; i, intestine ; ic, inter- clavicular air-sac ; pt, posterior thoracic air-sac ; r, rib ; s, sternum ; tr, trachea.

The bronchi lead to the lungs which are closely pressed up against the ribs. The cavity of the lungs is repeatedly subdivided, giving them the appearance of being filled with a very vascular and spongy material. They are no longer simple hollow sacs with large undivided cavities as in the lower forms. The lungs of the bird are peculiar in that they give off a number of pouches or air-sacs, which extend into many parts of the body. There are nine of these air-sacs, arranged in the following manner : a pair of cervical sacs at the base of the neck on each side ; an interclavicular sac in the region of the furcula ; two pairs of thoracic sacs, and a pair of abdominal sacs. The bronchi lead through the lungs, into which they give off a few air-passages, to the air-sacs. The walls of the air-sacs are not vascular and no respiratory exchange takes place in them ; they act as reservoirs, and when the body cavity is compressed by raising the sternum, the air in them is forced into the lungs and out again. The efficiency of the respiratory system of the bird is due to the fact that there are no blind ends, and the air in the spaces of the lungs is completely refreshed at each expiration. It is worth noticing that the temperature of the body of birds is remarkably high (about 42 C), and this is connected with the efficiency of the respiratory exchange. Expiration is the active process, by dropping the sternum the air-sacs expand and fill again. It may be remembered that several of the bones are hollow, and diverticula of the air-sacs extend into them, as for example those of the interclavicular sac into the humerus. Vascular System. — The heart of the bird is not unlike that of the lizard, but the ventricle is completely divided into two by an interventricular septum. The pulmonary arch is present in the bird just as it is in the lizard, and it leads from the right ventricle to the lungs. The right aortic (or systemic) arch is also present, arising from the left ventricle. The left arch which in the reptile arises from the right side of the ventricle and receives mostly venous blood, has disappeared completely in the bird. All the venous blood returns to the heart from the superior and inferior venae cava? direct into the right auricle, there being no sinus venosus. All this blood passes into the right ventricle and to the lungs, from which the arterial blood returns to the left auricle. The systemic "arch therefore receives nothing but pure arterial blood from the left ventricle, into which it has passed from the left auricle. There are therefore two completely separate circulations in the heart, and this is rendered possible by the fact that the heart is four-chambered, both auricle and ventricle being completely divided longitudinally.

The right systemic arch gives off a pair of arteries which run forwards for a short distance, known as the innominate arteries. Each divides into two, forming the carotid arteries and the subclavians. The carotids run forwards to the head ; the subclavians supply the pectoral muscles and the wings. The systemic arch runs up on the right side of the gut and reaches a position dorsal to it where it is known as the dorsal aorta. It gives off coeliac and mesenteric arteries to the alimentary canal, and sciatic arteries to the legs, and then divides to form the iliac arteries and the caudal artery which supply the hinder regions of the body.

The superior venae cavae receive the jugular veins, and these are peculiar and interesting in that the right and left veins are connected by a cross-channel at the top of the neck. In the twisting of the long and flexible neck, it may happen that the vein on one side is squeezed, and the flow of blood in it interrupted. This blood can, however, return to the heart by passing across the connexion just described, and down the jugular vein of the other side. The superior venae cavae also each receive a subclavian vein made up of a brachial vein from the wing and a pectoral vein from the pectoral muscles.

The inferior vena cava receives the hepatic veins, and is formed by the junction of a pair of iliac veins. These receive the femoral veins from the legs and the renal veins from the kidneys. The blood in the hinder regions of the body is led forwards in a caudal vein, which soon divides into three. Two of these vessels represent the renal portal veins of the lower vertebrates, but in the adult bird these veins connect direct with the iliac veins and vena cava inferior, without breaking down into capillaries in the kidneys at all. There is therefore no renal portal circulation. The third vessel into which blood may flow from the caudal vein is the coccygeo-mesenteric vein, which runs downwards and forwards in the mesentery supporting the intestine, and joins the (hepatic) portal vein. The latter runs from the intestine and duodenum to the liver, as in all vertebrates. There is one more vessel worthy of mention, and that is the epigastric vein which runs forwards from the mesentery, passes ventral to the liver, and joins the hepatic vein. This epigastric vein represents the anterior region of the anterior abdominal vein of lower forms : the hinder part of this vein is represented in the bird by the coccygeo-mesenteric vein.


Fig. 59. — Columba : ventral view of a dissection of the vascular system ; after a drawing by Mr. B. W. Tucker.

a, aorta ; ba, brachial artery ; bv, brachial vein ; c, carotid artery ; cv, caudal vein ; cmv, cceliaco-mesenteric vein ; da, dorsal aorta ; ev, epigastric vein ; fa, femoral artery ; fv, femoral vein ; h, heart ; hv, hepatic vein ; ia, iliac artery ; /, jugular vein ; k, kidney ; /, liver ; li, left innominate artery ; Ipa, left pulmonary artery ; Ives, left vena cava superior ; pa, pectoral artery ; pt, posterior mesenteric artery ; pv, pectoral vein ; rpa, right pulmonary artery ; rv, renal vein ; sa, sciatic artery ; t, testis ; vet, vena cava inferior.

The chief difference, therefore, between the venous systems of the bird and the lizard, is the direct connexion of the " renal portal veins " with the inferior vena cava in the former. It may also be noted how the great development of the pectoral muscles has brought about a modification of the vascular system, in the form of the well- developed pectoral arteries and veins. These muscles, on which the flight of the bird depends, are the most active in the body.

Urino-genital Systems

The kidneys are metanephric, not mesonephric. The kidneys lie in the roof of the coelomic cavity, and each is divided into three lobes. Each kidney is connected by a ureter with the urodseal division of the cloaca. There is no bladder.

In the male, the testes are connected with the cloaca (urodaeum) by the vasa deferentia, or Wolffian ducts. In the female, the right ovary and right oviduct as a rule disappear ; there is then only one ovary (the left) and one oviduct (also the left) or Mullerian duct in the adult bird. The reason for the suppression of one ovary and duct is presumably that if two eggs were to be laid simultaneously (one by each oviduct), their combined size would block the passage between the two sides of the pelvic girdle. The Wolffian ducts are not present in the female, and the male has no Mullerian ducts.

Nervous System

In the brain, the cerebral hemispheres are well developed, and considerably larger than in the lower forms. This increase in size is due to the enlargement of the corpus striatum, and not to the development of the cortex or superficial layer of grey matter forming the roof of the hemispheres. The cortex of the brain in birds is thin, and markedly different in this respect from that of the mammals. The cerebellum is also well developed as is the rule among animals which rely on a sense of balance, and its surface is thrown into ridges. The median portion of the cerebellum is known as the vermis, on each side of which is a conical projection known as the flocculus. The front of the cerebellum is in contact with the hinder surface of the cerebral hemispheres, and the optic lobes which form the roof of the midbrain are thrown to the side.

As in the reptiles, there are twelve pairs of cranial nerves, the spinal accessory and hypoglossal being included in the skull. The wing is supplied by the brachial plexus, composed of nerves from the hind part of the neck and the front of the thorax. The leg is supplied by a femoral nerve, and a sciatic plexus and nerve, which runs through the ilio-sciatic fissure in the pelvic girdle. The obturator nerve which pierces the obturator foramen innervates the region of the acetabulum.

Sense-organs. — With regard to the sense-organs, there is not much advance over the conditions in the reptiles. The eye is elongated from cornea to optic nerve, instead of being spherical. Projecting into the posterior chamber of the eye, which is occupied by the vitreous humour (see p. 23), is an upstanding vascular structure. This structure, known as the pecten, arises from the spot (" blind spot ") where the optic nerve and artery enter the eye ; it recalls the columella Halleri which is found with similar relations in the eye of Teleost fish. The function of the pecten is still dubious, but its vascularity suggests that it is concerned with supplying oxygen to the vitreous humour and the posterior chamber generally.

Accommodation in the eye of the bird is peculiar. The junction between the cornea and sclerotic is covered on the inside by a muscle which is striated (Cramp ton's muscle). Contraction of this muscle results in an increase of the convexity of the outer surface of the eye : cornea and conjunctiva, which accommodates the eye for near vision. The convexity of the lens is also increased by contraction of the circular muscle of the iris. At the same time, the contraction of the ciliary muscle pulls the hinder part of the eye forwards, and this reduces the tension on the suspensory ligaments, which are attached to the lens.

In the ear, the cochlear part of the saccule is better developed than in reptiles, and is beginning to show the spiral winding.

With the exception of the warm-bloodedness, and the complete subdivision of the ventricle of the heart, the characters which birds show, and which are not yet developed in the reptiles, are specialisations which do not appear in the mammals. Birds represent a further development of reptiles in one direction, while the mammals evolved in another direction from another group of primitive reptiles.

Characters of Columba which show an advance on the conditions in lower forms {and which are at the same time specialisations not found in mammals) :

Feathers ;

Modification of the pectoral limbs into wings ;

Loss of teeth ;

Formation of air-sacs (foreshadowed in the Chamaeleon) ; Formation of oblique and post-hepatic septa ; Loss of right ovary and oviduct ; Very long sacrum ; and fusion of vertebrae ; Extreme posterior position of pubis ; Loss of left systemic arch.


Parker, T. J. A Course of Instruction in Zootomy (Vertebrate). Macmillan, London, 1884.

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Mark Hill.jpg
Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
Vertebrate Zoology 1928: PART I 1. The Vertebrate Type as contrasted with the Invertebrate | 2. Amphioxus, a primitive Chordate | 3. Petromyzon, a Chordate with a skull, heart, and kidney | 4. Scyllium, a Chordate with jaws, stomach, and fins | 5. Gadus, a Chordate with bone | 6. Ceratodus, a Chordate with a lung | 7. Triton, a Chordate with 5-toed limbs | 8. Lacerta, a Chordate living entirely on land | 9. Columba, a Chordate with wings | 10. Lepus, a warm-blooded, viviparous Chordate PART II 11. The development of Amphioxus | 12. The development of Rana (the Frog) | 13. The development of Gallus (the Chick) | 14. The development of Lepus (the Rabbit) PART III 15. The Blastopore | 16. The Embryonic Membranes | 17. The Skin and its derivatives | 18. The Teeth | 19. The Coelom and Mesoderm | 20. The Skull | 21. The Vertebral Column, Ribs, and Sternum | 22. Fins and Limbs | 23. The Tail | 24. The Vascular System | 25. The Respiratory system | 26. The Alimentary system | 27. The Excretory and Reproductive systems | 28. The Head and Neck | 29. The functional divisions of the Nervous system | 30. The Brain and comparative Behaviour | 31. The Autonomic Nervous system | 32. The Sense-organs | 33. The Ductless glands | 34. Regulatory mechanisms | 35. Blood-relationships among the Chordates PART IV 36. The bearing of Physical and Climatic factors on Chordates | 37. The origin of Chordates, and their radiation as aquatic animals | 38. The evolution of the Amphibia : the first land-Chordates | 39. The evolution of the Reptiles | 40. The evolution of the Birds | 41. The evolution of the Mammalia | 42. The evolution of the Primates and Man | 43. Conclusions | Figures | Historic Embryology

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