PROCEEDINGS OF THE UNITED STATES NATIONAL MUSEUM issued 8^l^v>LCl?^ h (fte SMITHSONIAN INSTITUTIONU. S. NATIONAL MUSEUMVol 104 Washington : 1955 No. 3346 MODIFICATIONS OF PATTERN IN THE AORTIC ARCH SYS-TEM OF BIRDS AND THEIR PHYLOGENETIC SIGNIFICANCEBy Fred H. Glenny ^ IntroductionMy interest in the aortic arch system in birds was stimulated bythe discovery of a functional left radix aortae in the belted king-fisher during a routine dissection of that bird in 1938. Subsequentstudies on several other species of birds produced interesting ana-tomical information, and, with continued studies, a semblance oforder in occurrence of carotid patterns became more and moreevident.After a reasonably large series of families and orders of birds hadbeen examined, it appeared that further studies might produce in-formation which could be of value in avian taxonomy. As a result,a series of systematic studies of the main arteries of the neck andthorax of birds was initiated and carried out over a period of about 12years.During the past 2 or 3 years important implications with respectto the evolution of the aortic arch system in the bhds became moreapparent, and the present treatise deals primarily with this aspect ofmy accumulated studies.The classification of birds used in this study follows the arrange-ment of Wetmore and Peters, with only a minor revision in thelistiag of the parrots in the subfamily Psittacinae. In my opinion,the Wetmore and Peters classification of the birds of the world is morein accord with the natural relationships than are the schema employedby many of the European taxonomists.Insofar as possible the names of birds as used bj^ earlier and evencontemporary writers have been checked as to sjiionymy withPeters' (1931-51) checklist. Since Peters' checklist is not complete ' The Youngstown University, Youngitown, 0hio<332543?55 1 525 526 PROCEEDINGS OF THE NATIONAL MUSEUM vur. 104for the Passeriformes, only the authority for the species listed can begiven.The British Museum catalog of birds and Sharpe's hand-list havebeen freely consulted in an effort to obtain information essential tothe establishment of the names of species and subspecies synonymouswith those in the Peters checklist.Unless otherwise noted, only smgle specimens were studied; ininstances where more were studied the number is noted after thespecies name.I wish to express sincere gratitude to the following individuals andinstitutions for their generous assistance in making available ma-terials used in the study, and for their many helpful suggestions andcriticisms in the preparation of this paper: American Museum ofNatural History; Chicago Natural History Museum; ClevelandMuseum of Natural History; Fan Memorial Institute of Biology;Meems Brothers and Ward, Inc.; Royal Ontario Museum of Zoology;Sudan Government Museum, Natural History; United States Na-tional Museum; and Ward's Natural Science Establishment, Inc.;Dr. Jolm. W. Aldrich, Dr. Dean Amadon, Dr. Doris Cochi-an, Mr. J. W.Cowland, Dr. E. Home Craigie, Dr. David E. Davis, Mr. Dwight D.Davis, Dr. Charles A. Dambach, Mr. R. N. Deaton, Dr. E. H.Dustman, Dr. Herbert Friedmami, Dr. Ira N. Gabrielson, Dr. D. L.Gamble, Mrs. M. E. Glenny, Mr. W. Earl Godfrey, Dr. Walter C.Kraatz, Mr. W. J. Leach, Mr. Ben H. Morgan, Mrs. C. P. Mountz,Dr. Harry C. Oberholser, Dr. John W. Price, Dr. Loren S. Putnam,Dr. D. P. Quiring, Mr. Tsen-Hwang Shaw, and Dr. AlexanderWetmore. Review of the literatureFrom shortly after the turn of the 19th century until its end,Em-opean anatomists and ornithologists evinced a considerable in-terest in the arterial system of birds. Among the earliest writers onthis subject were Bauer, Meckel, Nitzsch, and Hahn, followed byOwen and Barkow. With the rapid expansion of interest in com-parative morphology during the middle of the 19th century, otherworkers soon became engaged in numerous and very revealing in-vestigations to which they tried to give some semblance of order andmeaning. Prominent among this group of workers were Boas,Rathlce, Sabatier, and Garrod.During the middle of the 19th century, the theory of ontogeneticrecapitulation was developed and became of considerable importancein the fields of comparative and human anatomy and organic evolution.It was during this time that the study of anatomy received its greatestimpetus and achieved the peak of respectability in science.Garrod, of all the workers of his time, was least successful in in-terpreting his findings, with the result that the significance of his AORTIC ARCHES OF BIRDS?GLENNY 527 contributions on the carotid arteries in birds was overlooked by mostworkers. Even Forbes and Beddard failed to interpret Garrod'sstudies satisfactorily, but Boas, Rathke, and Sabatier were betterreceived by most of their contemporaries, with the result that manyof their contributions and writings have been passed on to the presenttime. With respect to their interpretations of the arrangement inbirds of the arteries and, especially, the aortic arches, they were in-correct in certain important details. Although Brenner had ques-tioned Rathke's and Sabatier's placement of the subclavian artery asearly as 1883, most textbooks in comparative anatomy still carryplates of the Rathke-Boas type of schematic diagrams.In spite of correct information presented by Gadow, Hertwig,Hochstetter, and others, only a few textbook writers have made aneffort to present the facts in preference to the presentation of a planof organization or a pattern of evolution in the aortic arch system ofthe vertebrates.A great deal of research was necessary even after the end of the 19thcentury in order to clarify the true nature of the aortic arch systemand the changes wliich these and associated vessels undergo duringembryonic development. The greatest single contribution of thiskind was made at Northwestern University under the direction ofW. A. Locy. Significant contributions on the embryonic develop-ment of arteries in birds were made during the first 6 years of the 20thcentury by Rabl, Sabin, Locy, and Twining. Thereafter, little workof importance reached the literature until 1934 when Hughes publishedhis very important studies on the development of the cephalic bloodvessels in the chick.Despite these studies, a great gap still exists insofar as the develop-ment of the coracoid or sternoclavicular, thoracic or intercostal(internal mammary), and pectoral arteries of birds are concerned,I have been unable to find a single reliable account of the exactdevelopment of these vessels. Most anatomical references allude tothe mammalian condition insofar as it is known, but actual accountsfor birds appear to be lacking.Apparently, there was little interest in the arterial system of adultbirds (for well over a quarter of a century) until I began systematicstudies of the arteries of the neck and thorax. Shortly thereafterBhadiu-i and Biswas began a similar series of studies in India, and afew other incidental papers have appeared from time to time, treat-ing largely with anomalous occurrence of vestiges of embryonicvessels.As a result of these studies, I feel that it is weU to summarize thefindings of earlier and present-day workers in such a way that futureworkers may be better able to interpret their findings. It is withthis in mind that I propose to discuss the significant changes in the 528 PROCEEDINGS OF THE NATIONAL MUSEUM vol. i04 aortic arch system and associated vessels with respect to their ulti-mate fate in birds.It must be recognized that much of the present interpretationcannot be entnely resolved without further and extensive embryo-logical studies on the nature of the origin and development of thesevessels in the various orders, families, and species of birds. Thecomplexities arising from important differences in the final arrange-ment-patterns of the arteries in the neck and thorax add considerablyto the difficulties of interpretation. As a result, much of the inter-pretation will of necessity be quite generalized. Furthermore, thisinterpretation is based largely upon the studies made on the chickembryo, and since there probably are a great many important differ-ences to be encountered in other orders of birds, the present inter-pretations may not be entirely accurate in at least some of the details.It is suggested that renewed efforts be made to carry out embryo-logical studies on the development of birds other than the chick, andthat the development of the aortic arch system be given especialattention. Among the more critical aspects of this study are themanner and time of fusion of the anterior dorsal radices aortae (dorsalcarotids), the manner in which the proximal portion of the dorsalradix, anterior to the carotid arch, atrophies, and the changes in andthe fate of the ventral radices aortae (ventral carotids).Another factor which should be taken into consideration is that ofinterpretation of the diagrammatic representations of structure,especially since there are apparent changes in the spatial relationshipsof portions of the aortic arch system in the different vertebrate groups,and these changes may be brought about as a result of other struc-tural changes or modifications. Some of these structural modifica-tions appear to produce an anterior-posterior compression or contrac-tion of the aortic arch system with corresponding changes in thedefinitive spatial relationships of the early embryonic system. Inthe amniotes, and especially in bii'ds and mammals, the ventral aortaappears to be lost, and the ventral radices aortae or ventral carotidsare greatly modified. Such a modification in the structural-spatialrelationship is rather advanced in the human embryo, with the resultthat interpretation of true homologies is sometimes very diflBcult.Too frequently schematic or diagrammatic representations are ormay be misleading as a result of faulty interpretation of both thediagrams and the actual condition as critically observed in studymaterials. Interpretation of the materials under study, however,should be facilitated by a careful study and analysis of the schematicdiagrams. When this has been done, barring the lack of importantembryological facts, there should be little difficulty in making ade-quate and correct interpretations.As an aid in the interpretation of the adult avian aortic arch deriva-tives, it is well to make comparisons with the aortic arch derivatives AORTIC ARCHES OF BIRDS?GLENNY 529in the other tetrapod vertebrates, and to attempt to show homologiessuch as do exist.Early development of the avian vascular systemIn discussing the early development of the vascular system of thechick, Patten (1929) states that the early vessels are formed frommesodermal cells that lie in the path of their development and thatthe walls of these early vessels are one cell-layer in thickness. As aresult, no clear structural differences between the precursors of botharteries and veins arise until a much later period in development.Balfour (1873) has stated that the blood vessels of the chick arise notas spaces or channels between the mesoblast cells but as a networkformed by united processes of the mesoblast cells, and that it isthi'ough these processes that the blood flows. He also stated thatfirst traces of blood vessels are to be found in the pellucid area at about30 hours of incubation.Hyman (1942) states that the blood and blood vessels arise frommesenchyme cells of the mesoderm by forming patches of cells andthat the central cells become modified into blood corpuscles, whilethe peripheral cells become oriented so as to form tubes, the earlyblood vessels. Essentially all these views represent the same concept,but expressed in slightly different ways.The vitelline veins are the earliest vessels to form in the embryoand are found to develop on the surface of the jolk sac in the splanchnichypomere and then pass to the embryo in the gut mesentery andfinally come to enter the heart at its caudal end.The ventral aorta is observed to arise at the cephalic end of theheart, with which it then becomes connected. The ventral aortathen extends anteriorly to the anterior end of the pharynx, at whichpoint it bifurcates to form the anlagen of the ventral radices aortae,which then turn laterally and dorsally and pass around the pharynx,on either side, and curve posteriorly, dorsal to the pharynx, as thedorsal radices aortae which carry the blood backwards to the vitel-line arteries which in turn pass to the yolk sac. Thus the first aorticarch which now lies within the mass of the mandibular visceral archcomes to be the first of the true aortic arches formed. Subsequentlyfive additional pairs of vessels communicating between the ventraland dorsal radices aortae come into existence for a varying length oftime, depending upon their ultimate fate in the adult bird and thefunction which they serve in the embryo or in the adult. Later, thetwo dorsal radices aortae, posterior to the pharyngeal region, come tofuse, thus forming the single median dorsal aorta (abdominal aorta)of the adult vertebrate.Jolly (1940) has pointed out that the origin and mode of formationof the large embryonic vessels is still a matter in question and cloaked 530 PROCEEDINGS OF THE NATIONAL MUSEUMin obscurity, but he supports the view that the aortic vessels form insitu and are not the result of a "budding" or outgrowth from theheart nor a product of "migration," but rather are independent inorigin and formation from the heart. Hyman (1942) asserts that atubular cavity arises on either side (in the embryo) in the splanchnic a.a.r.av X^7/^?^^ =>j[o c.ir. C.c. ^^, / Figure 108.?For explanation see facing page. AORTIC ARCHES OF BIRDS?GLENNY 531mesoderm of the hypomere, and is of the same nature as the bloodvessels, and that, as the hypomere closes below in the median ventralline, the two cavities are brought together and fuse to form the heart.With the disappearance of the ventral mesocardium the heart comes tolie free in the coelom.Patten (1939) points out that the paired ventral aortic roots ex-tend anteriorly from the bulbo-conus arteriosus (anterior heartchamber), and that the ventral aortic roots and the omphalomesentericveins constitute direct continuations of the paired endocardial primor-dia of the heart. This is not in contradiction to Jolly's view of vesselformation within the embyro.At about the 44-hour stage of incubation the heart begins regularcontraction, thus establishing the circulation of the blood.In birds and mammals the ventricle is divided into left and rightcompartments by the interventricular septum. The atrium is like-wise divided by the interatrial septum, and the sinus venosus, stillrecognizable, is incorporated into the wall of the right auricle ac-cordmg to Quiring (1933). The systemic or aortic root and the pul-monary root form by a splitting of the conus arteriosus into two maintrunks. The aortic or sj^stemic root passes from the left ventricle tothe body, while the pulmonary root passes from the right ventricleto the lungs. Thus the bird heart is comprised of two embryonicchambers, each of which is secondarily divided into two compart-ments, while the other two heart chambers of the lower vertebratesand the chick embryo are lost through incorporation and furtherstructural and functional modifications. The atrium and ventricleof the early embryonic heart alone persists as the primary heartchambers, and the valves of the conus arteriosus persist in the pul-monary and systemic roots at the point of junction of these vesselswith the ventricles.As reported by Twining (1906), Lillie (1908, 1919), Patten (J929),Hughes (1934), and others, the aortic arches make their appearance(in the chick embryo) in order and at approximately the followinglevels of development or incubation: (1) first aortic arch appears inFigure 108. ? a, Amniote aortic arch arrangement, lateral view; b, same, ventral view;c-i, ventral views of main cervical and thoracic arteries; c, in Bufo melostictus (modifiedafter Bhaduri); d, in Alligator mississippiensis (modified after Reese); e, in Sphsnodonpunctatus (USNM 19260);/, in Boa constrictor (after Hafferl); g, in birds (generalized);h, in Emys (modified after Hafferl); i, in mammals (modified after Patten). Explanationof symbols: 1-6, aortic arches; a., axillary artery; a.r., aortic root; b., basilar artery;br., brachial artery; c, coracoid artery; c.c, common carotid artery; c.d., dorsal carotidartery; c.v., ventral carotid artery; c.n.v., comes nervi vagi; d.a., dorsal (abdominal)aorta; d.b., ductus botalli; d.c, ductus caroticus; e.c, external carotid artery; i., innomi-nate artery; i.e., internal carotid artery; i.m., internal mammary artery; l.a., ligamentumaortae; l.b., ligamentum botalli; I.e., ligamentum caroticum; p., pectoral arteries; r.a.,radix aortae; s., subclavian artery; s.c, subscapular artery; t., thoracic artery; v., vertebralartery; v.a,, ventral aorta. 532 PROCEEDINGS OF THE NATIONAL MUSEUM vol. i04from 33 to 38 hours of incubation and disappears about the third orfourth day, or by the 32-somite stage; (2) second aortic arch appearsat about the end of the second day and at least by the end of 50 to55 hours of incubation, and disappears during the fourth day or byabout the 32-somite stage; (3) third aortic (carotid) arch is usuallypresent by the end of the second day or by the end of 50 hours ofincubation, and this vessel usually remains throughout the life of thebird, although it may be modified in part in the adult where it forms,at least in part, the common carotid artery; (4) fourth aortic (systemic)arch arises in the embryo during the third day of incubation and ispresent by the end of 72 hours of incubation; the right arch alone(normally) remains and serves as the functional systemic arch con-necting the systemic root with the dorsal radix aortae on the rightside; the left arch is reduced by about QYi days of incubation, andusually entirely obliterated by 7K days of incubation; (5) fifth aorticarch is a transient vessel which makes its appearance during the firsthalf of the fourth day of incubation and disappears by about the endof the fifth day; (6) sLxth aortic (pulmonary) arch makes its appearanceusually by the end of the fourth day and persists, at least in part,for the duration of the animal's life; the proximal ends of both vesselsremain but become connected with the new pulmonary artery, whichforms de novo in situ and supplies the lung; the distal portion atro-phies and the left ductus arteriosus (botalli) usually completely dis-appears, while the right remains in many birds as the ligamentumbotalli or it may fuse with the ventral face of the right radix aortaewhere it appears as a white streak (linea botalli) along the ventralface of the radix; (7) internal carotid artery appears at about the be-ginning of the third day of incubation as an anterior prolongation ofthe dorsal radLx aortae from which point it extends into the headregion, in rather close association with the brain.Early changes in aortic archesAs has already been noted, the first, second, and fifth aortic archesbecome obliterated at an early stage in the embryonic life of the bird.According to Lillie (1908), these deletions occur on the third and fourthdays of incubation in the case of the first two aortic arches, and, ashas been pointed out by Hughes (1934), the fifth arch tends to dis-appear during the fifth day of incubation.During the sixth to seventh day of incubation the fourth aorticarch of the left side loses its comiection with the truncus. At thissame time the dorsal connection between the fourth and third leftarch (ductus caroticus) becomes reduced and soon loses its attachmentwith the left fourth aortic arch. By the 7K-day stage there is no trace ofthe left systemic arch except in instances of anomalous retention suchas those cited by Biswas (1946) and Pohlman (1920). The dorsal AORTIC ARCHES OF BIRDS?GLENNY 533 radix aortae of the left side then anastomoses, medial to the ductusbotalli, to the proximal portion of the pulmonary arch. As has beendemonstrated (Glenny, 1943b, 1943d, 1944d), this secondary attach-ment precedes atrophy of the ductus botalli of the left side, andthe left radix aortae posterior to the left fourth aortic arch beginsto take over the function of the ductus botalli of that side.No accurate account of the loss of the ductus caroticus of theright side could be located. It may be assumed that this occursfirst as a disconnection at the level of the right systemic arch andperhaps may occur much later than has been suspected. Bhaduri(1939), Finn (1891), Glenny (1944a), Mathew (1944), and Subhap-radha (1944) have reported the persistence of the ductus caroticus onthe right side of several birds. Rarely, however, the otherwise func-tionally modified ductus caroticus may retain a short ligamentousconnection with the right systemic arch (Glenny, 1944a). It has beeninferred that the ductus shawi represents a functionally modifiedductus caroticus which comes to serve as the supply to thebronchi, and sends off branches to the syrinx, lung substance, and theoesophagus (Hafferl, 1933). Not altogether satisfactory studieshave been made on the exact changes which take place in the ductuscaroticus.The fact that the right dorsal radix aortae remains as the functionalvessel carrying blood to the abdominal aorta does influence the sub-sequent history of the right ductus botalli. This vessel remainsfunctional almost throughout the embryonic life of most birds, andundergoes further atrophy subsequent to hatching. While mostorders of birds retain at least a ligamentous vestige of this embryonicvessel, many families show a greater degree of atrophy of this structurethan do others. In some species where obliteration is nearly completethere is frequently evidence of its persistence as a linea botalli alongthe ventral face of the dorsal radix, with which structure it may fuse.With the atrophy of the right ductus botalli, the left radix aortaebegins to atrophy. Tbis process continues in most birds until onlya small ligamentum aortae remains as the vestige of this once promi-nent vessel. Rarely, the left radix aortae may remain as a function-ally modified vessel (Glenny, 1939) or, more frequently, with ashort lumen. In general it may be stated that almost without excep-tion extremely careful examination of the adult bird wiU reveal aminute ligamentous vestige of the left radix aortae. The difficultyencountered in determining its presence arises from the fact that theligament may become so much reduced that it is difl[icult to differ-entiate it from the surrounding fascia, and in smaller birds it is stiUmore diflScult to find.When the right ligamentum botalli is much reduced, its distalattachment to the radix aortae may be determined by the presence 534 PROCEEDINGS OF THE NATIONAL MUSEUM vol. io4 of a small ligamentous button on the ventral face of the right radix.The systemic arches in bu-ds are pau-ed structures only dmingearly embryonic stages. Biswas (1946), however, reported theanomalous occurrence of both left and right systemic arches in aspecimen of Ploceus philippinus philippinus.Normally, atrophy of the left systemic arch follows shortly afterthe disconnection of the ductus caroticus from the posterior portion ofthe dorsal radices aortae. This results in the retention of the rightsystemic arch as a functional vessel which then passes diagonallylateral and dorsad to join the remaining functional right dorsal radLxaortae which then passes diagonally toward the midline to the pointof union with its complementary vessel of the left side. The lattervessel is usually found in the adult as the ligamentum aortae. Thefunctional radix then forms a connection with the abdominal aorta.In the respect that birds present but one of the pair of systemicarches, they differ from mammals. On the other hand, the right dor-sal radix aortae in birds and the left dorsal radix aortae in mammalsare the sole functional vessels which are responsible for the distribu-tion of the blood to the abdominal viscera and posterior appendages.As is well known, the ventral or proximal portion of the embryonicsixth aortic arch remains as the functional portion of this embryonicvessel which, along with the embryonic pulmonary artery that joinsit, comes to serve as the definitive pulmonary artery of the adult.The left ductus botalli usually undergoes atrophy shortly after thecomplete atrophy of the left systemic arch, by which time the leftradix forms an anastomosis with the pulmonary arch proximal to thenormal dorsal (ductus botalli-radix aortae) connection. As a resultof this secondary connection, the left dorsal radix aortae serves thesame function as the ductus botalli (Glenny, 1943d, 1944d). This isnot the case in anomalous retention of the left systemic arch as re-ported by Biswas (1946). In this rather singular case, the distalportion of the left radix atrophied and the connection was maintainedby way of the left systemic arch, and the left ligamentum botaUiremained as the vestige of the embryonic vessel, whereas in most casesthe left ligamentum botaUi completely atrophies, or at best becomesfused with the left radix aortae either prior to or at the same time asthe radix undergoes atrophy.In instances of functional modification of the left radix aortae, theleft ligamentum botalli may or may not be completely lost; but thisis extremely difficult to ascertain since so few species or individualsmay retain a functional left radix aortae and atrophy of the ligamen-tum botaUi has usually progressed to such a stage that determinationof its presence is difficult.The distal portion of the right sixth aortic arch undergoes atrophyand becomes the ligamentum botalli or it may rarely maintain a smalllumen. In such instances where it does not appear to be present it AORTIC ARCHES OF BIRDS?GLENNY 535may fuse with the radix and be completely lost or remain as a lineabotalli, or it may be partially resorbed and remain as an incompleteligament or as a ligamentous button on the ventral surface of the radixaortae.Atrophy of the right ductus botalli and the left radix aortae occursat approximately the same time and at about the same rate. Itappears that, as in many species of birds, there may be a continuedprogressive atrophy of both of these structures for quite a time afterhatching. The rate and level of atrophy of these structures maydiffer in different species, but particularly between families and ordersof birds. It appears that, in a few orders and families of birds, atrophyof these two structures may be independent of each other. Thisassumption is based on observations on many species within a familyor order in which the ligamentum aortae may be of considerable size,while the right ligamentum botalli is almost entirely or completelylacking or remains as a linea botalli.Much confusion and misunderstanding is encountered in the litera-ture with respect to the carotid arteries. This is in part due to thelack of uniformity in terminology and to the failm'e to recognize somedefinitive vessels which are embryonic derivatives. Incompleteseries for study, along with inadequate techniques, account in partfor the failure of earlier workers to fully comprehend the significantchanges which occur during the first week or 10 days of incubation.Furthermore, many of the earlier workers probably were greatlyinfluenced in their views and interpretations by the dominant con-cept of ontogenetic recapitulation which so strongly influenced thestudies of morphologists during the 19 th century.Some authors refer to the dorsal and ventral radices aortae simplyas the dorsal and ventral carotids. This may have led to some mis-interpretation, since the internal and external carotids are sometimesreferred to as the dorsal and ventral carotids. Interpretation isdifficult because direct comparisons cannot be made between birdsand reptiles on the one hand or between birds and mammals on theother hand since the development of these vessels differs somewhat indetails in each of the three classes of amniotes.According to Twining (1906), the third aortic arch gives rise to adorsal carotid and a ventral carotid; the former is well developed andeasfly traced anteriorly, while the latter, which he regards as thebasal remnant of the first and second aortic arches, arises from thebase of the third arch. At this early stage no trace is found of a vesselconnecting the dorsal and ventral carotids, the entire blood supply tothe jaw anlagen being produced by the ventral carotids. Anastomosisof the dorsal and ventral carotids occurs during a later stage in theembryonic development.Increase in length of the dorsal and ventral carotids results fromelongation of the cervical region, and this is followed by many complex 536 PROCEEDINGS OF THE NATIONAL MUSEUM vol. io4 changes in the arrangement and orientation of the other associatedvessels.In the 5K-day chick a vessel arises de novo from the dorsal carotidat a point about halfway between the third arch and posterior borderof the eye. At a later stage this vessel comes to communicate with theventral carotid, thus forming the fork of the external carotid.Mackay (1887) maintains that the ventral carotid does not contrib-ute to the formation of the external carotid, but Twining (1906) andHughes (1934) have shown that Macka3^'s conclusions were in-correct.With elongation of the carotid arch, the ventral carotid comes toassume a somewhat more dorsal position, and in the GK-day chickembryo the secondary subclavian artery forms an anastomosis withthe third arch somewhat ventral to the ventral carotid. Consequently,Mackay's contention that the definitive subclavian and the ventralcarotid join in a common stalk is not substantiated by Twining's study.The dorsal carotid and anterior branches of the ventral carotidundergo an anastomosis between the sixth and seventh days of incuba-tion. This connection results in a dual blood supply to the upper andlower jaws. The portion of the dorsal carotid anterior to the anas-tomosing branch is referred to by Twining as the internal carotid.In the chick embryo of 7 to 8 days, the ventral carotid is reportedto lose its anterior connection. The carotid arch elongates anteriorly,and with this there is a dorsal and anterior migration of the thjrroidgland.Twining states that the vertebral is generally a branch of thecommon carotid. Glenny, in a long series of systematic studies, hasshown that the vertebrals may vary considerably in the point of origin(dorsal radix anterior to the thhd arch, the common carotid, or as abranch of the superficial cervical or ventral carotid).With the interruption of the ventral carotid at a point about midwaybetween the basal portion of the third arch and the cephalic end of theexternal carotid (Hughes, 1934; Twining, 1906) the entire bloodsupply to the head (other than that carried by the vertebrals) traversesthe dorsal carotids. The earlier communicating vessel, which con-nects the dorsal and ventral carotids, then comes to supply the vesselswhich were previously connected with the ventral carotid. BothTwining and Hughes have demonstrated that the anterior or cephalicportion of the ventral carotids function as descending oesophagealarteries. This corresponds with Glenny's (1944d) findings on theCanada goose. Thus the shunt which develops between the dorsaland ventral carotids during the sixth and seventh days of incubationin the chick embryo serves to carry the cephalic blood supply previ-ously carried by the ventral carotid.Wliile Twining considered the proximal portion of the ventralcarotid to degenerate or atrophy, Hughes, in his studies on the 9-day AORTIC ARCHES OF BIRDS?GLENNY 537 chick and subsequent stages, points out that this portion of the ventralcarotid becomes functionally modified to form the ascending oeso-phageal artery. This view is likewise shared by Glenny (1944d). Itshould be pointed out that in several orders of birds this functionallymodified vessel may be short and greatly reduced, with the result thatduring its development it may be readily overlooked and even inthe adult bird may be detected only after the most careful examinationor upon injection with colored materials. Bhaduri and Biswas(1945, 1947, 1954) have shown that it may be continuous, and retainits natm^al connection. I have observed the superficial cervical arteryto be continuous and uninterrupted for the entire length of the neckin several orders of birds. This is probably the basic or ancestralarrangement, whereas the discontinuity of these ventral carotids isprobably a modification rather than the usual condition.At about the eighth to ninth day of incubation the innominate arterymay be recognized as originating from the basal portion of the thirdaortic arch.Therefore, it may be seen that (1) the innominate arteries arederived from the basal portion of the third arch; (2) the vessel fromthe point of junction with the subclavian to the region of the thyroidgland represents, for the most part, the dorsal portion of the thirdarch; and (3) the vessel lying beyond this point up to the base of thehead represents the dorsal radix aortae, anterior to the third arch.The origm and development of the cephalic branches of both theinternal and external carotid arteries are extremely well treated byBauer (1825), Hughes (1934), Ottley (1879), Twming (1906), andothers in both general and specific studies on the vascular system ofbirds. Hughes has pointed out that there are several importantdifferences in the connection of the cephalic branches of the externaland internal carotids between birds and mammals and, as a result,there cannot be a direct transfer of information from one group to theother. An exposition of these differences is of no great significancein this study.The ventral radices aortae (ventral carotids), as has been noted,may become functionally modified to form the ascending oesophagealartery from the posterior portion of the ventral carotids and the de-scending oesophageal artery from the anterior portion of this samevessel after disjunction. The external carotid, as a result, receivesblood by way of the dorsal carotid artery subsequent to the disjunc-tion. It is possible that extensive reduction of the proximal portionof the ventral carotid may result in a very short and much reducedascending oesophageal artery in many families of birds, while in stiUothers it is a prominent structure.Hafferl (1933) points out that the subclavian artery in birds is notthe primary blood vessel which is formed at first in the embryo butthat it arises from the ventral part of the third aortic arch, so that in 538 PROCEEDINGS OF THE NATIONAL MUSEUMthe adult animal a common trunk with the carotid artery exists as theinnominate artery.The axillary artery is derived from the distal portion of the primarysubclavian artery.Hochstetter (1890) has shown that the definitive subclavian arisesfrom the ventral ends of the carotid arches, as had previously beenannounced by Mackay (1887), but that the primary arteries to thewing-bud have their source directly from the dorsal aorta, as seg-mental vessels, and that the primary subclavian then completelydisappears. This primary vessel was regarded by Hochstetter as themammalian homologue. Sabatier (1874), Rathke (1850), and otherstended to add confusion to the matter by misplacing or improperly Figure 109.?Aortic arch system in Gallus, showing primary and secondary subclavians(ventral view, modified after Krassnig). Explanation of symbols: I, primary subclavianartery; II, secondary subclavian artery; 3, carotid arch; 4, systemic arch; 6, pulmonaryarch; c.d., dorsal carotid artery; d.a., abdominal aorta; d.c, ductus caroticus; r.a., radixaortae; s, subclavian artery; v, vertebral artery.locating the definitive subclavian, and it was not until Mackay andHochstetter published the results of their studies that any true lightwas thrown upon the problem. In 1883, Brenner challenged theviews of Eathke and Sabatier by pointing out that owing to thedifference in the relative position of the vagus nerve, superior venacava, and subclavian, the latter in birds could not correspond in adorsal mode of origin with the subclavian of mammals.Hochstetter's work demonstrated that, although the definitivevessel arises as a branch from the ventral part of the carotid arch, AORTIC ARCHES OF BIRDS?GLENNY 539there is also present a branch from the dorsal aorta to the anlage ofthe wmg, and that this latter vessel precedes the appearance of thesecondary or definitive subclavian artery. The secondary subclavianmakes its appearance on or about the sixth day of incubation, whilethe primary subclavian appears on about the fifth day according toHochstetter.Evans (1909b) has shown that the segmental subclavians commonlyoccur in the 16th to 19th intersomitic spaces. Hughes (1934) laterpointed out that the segmental subclavian of the first intersegmentalspace enlarges at the expense of the others, and soon becomes thesingle dorsal subclavian artery although considerable variability inthe primary subclavian development exists. Fleming's (1928) studiesare largely confirmatory of Hughes' observations.The two independently derived vessels (primary and secondarysubclavians) come to form a junction on about the sixth day ofincubation with the result that the limb-bud receives its blood supplyfrom two separately derived vessels until about the eighth day, atwhich time the primary subclavian atrophies and finally disappears.Confirmatory studies on the origin and development of the subclaviansin the chick were carried out by C. G. Sabin (1905). He reports thatthe primary subclavian begins to make its appearance at about 72hours of incubation, and that by the first half of the fourth day theprimary circulation is well established. He points out that the wingvessel is given off in common with the segmental artery on each sidefrom a short dorsal branch of the aorta. Development of the second-ary subclavian appears to take place from the primary subclavianforward and from the carotid arch backward. During the early partof the sixth day, Sabin reports the beginning of the formation of theultimate subclavian from the carotid arch, where it arises from theanterior surface.At the time of junction of the two subclavians the forelimb occupiesa position posterior to the heart, with the result that the secondarysubclavian has a comparatively long course to the limb. The majorblood supply to the wing is still provided by the primary vessel untilabout the seventh day of incubation, at which time the heart beginsto retrogress into the thorax, thus shortening the course of the second-ary subclavian. During the latter part of the seventh day and earlypart of the eighth day of incubation the primary subclavian atrophies,although a distal vestige may remain for a short time as a small spurextending dorsally into the base of the wing from the secondary sub-clavian.As the heart migrates posteriorly it gradually comes to lie in aposition posterior to the wing. Consequently, the definitive subclavianbecomes shortened and laterally directed. By the ninth day thecondition in the embryo is similar to that in the adult. 540 PROCEEDINQS OF THE NATIONAL MUSEUM vol. io4As Hughes has emphasized, the metamerism of the nervous, mus-cular, and vascular systems serves as an aid in following changes whichsubsequently occur during the course of embryonic development.The first and second aortic arches are metamerically associated withthe second and thu'd pro-otic segments while the third aortic arch isassociated with the first post-otic segment of the early embryo. Sincethe basal portion of the carotid arch in the adult is located at a posi-tion many segments behind the auditory capsule, it is considered thatthe aortic arches migrate posteriorly during the period of earlydevelopment.Prior to this migration, the embryo is a metamerically arrangedstructure with the segmxcntal organs of the cephalic end in an un-disturbed relationship (central nervous system with its nerve roots,somites, and aortic arches). At this time segmentally arranged inter-somitic arteries and veins are to be found; however, with a change inthis early segmental relationship and the caudad migi-ation of theaortic arches, the roots of the intersomitic blood vessels becomesevered from the aorta and these vessels then anastomose longitudi-nally with one another to form the longitudinal vertebral artery. Thenewly formed vertebral artery later acquires new connections with thedorsal aorta; thus, its formation is dependent upon the posteriormigration of the heart and the ultimate position of the aortic arches.Formation of the subclavians and vertebrals are, as a result of thecaudad migration of the heart and aortic arches, intimately relatedand it is likewise possible that the formation of the secondary ex-ternal carotid may be closely dependent upon this same modification.As noted by Hughes, the third aortic arch has migrated backwardthrough 20 segments by the first half of the seventh day of incubation.The carotid arch in its final position lies opposite the 15th cervicalganglion, and the root of the common cervical artery (Fleming, 1926)lies opposite the 18th interspace, where it joins with the persistentintersomitic artery of this interspace. As a result, the distal portionof the vertebral root is derived from the same position as the primarysubclavian artery.Anteriorly the vertebral artery becomes connected with the ex-ternal carotid by way of a deep branch of the occipital artery whichruns between the occipital arch and the atlas.In the pig, the internal mammary artery is formed by longitudinalanastomosing of the more cephalic of the thoracic intersegmentalarteries caudad to the subclavian artery, and subsequent deletions ofthe proximal parts of the other intersegmentals leave it to arise fromthe subclavian. The origin is quite similar to that of the vertebralartery anterior to the subclavian. In the bird, however, the so-calledinternal mammary (thoracic or intercostal) artery does not appear toform in the same manner as in the mammal. Insofar as I can deter- AORTIC ARCHES OF BIRDS?GLENNY 541 mine, no specific study has been made of the origin and developmentof this vessel and the other pectoral arteries.Anterior intercostal supply is derived from the ventrally locatedvessels, variously named, that arise as branches of the subclavianarteries. There are no segmentally arranged vessels arising from theright posterior radix aorta as in mammals. Posteriorly, the inter-costal muscles are supplied by segmentally arranged arteries whicharise as branches of the abdominal aorta. No connection with pos-teriorly located arteries could be established, and it is presumed thatthe so-called internal mammary is not homologous with that of mam-mals but is an intercostal artery not homologous with the inter-costals of mammals.The above observations were made possible by materials especiallyprepared for this study by Ward's Natural Science Establishment.Three-day chicks were doubly injected with colored plastic and theentire birds were then treated with corrosive solutions. As a result ofthis treatment, it was found that the left radix aortae could be in-jected for about half of its normal length.Changes in arrangement of thoracic and cervical arteriesIn birds, several significant changes may take place during thecourse of embryonic development of the individual aside from and inaddition to (1) loss of the first, second, and fifth aortic arches, (2)loss or functional modification of the ductus caroticus, (3) loss of theleft fourth aortic arch, (4) atrophy or functional modification of theleft radix aortae, (5) atrophy or loss of the ductus botalli, (6) theshunt anastomosis between the dorsal and ventral carotids (anteriorradices aortae) , and (7) the accompanying functional modification ofthe posterior end of the ventral carotid into an ascending oesophagealor superficial cervical artery and the anterior end of this same vesselinto a descending oesophageal or superficial cervical artery.The dorsal carotids usually migrate to a median ventral positionalong the long axis of the cervical vertebrae and, with thedevelopment of the ventral cervical musculature, soon become en-closed within the hypapophysial canal. These vessels then follow thecourse of this canal to a point near the site of articulation betweenthe third and fourth cervical vertebrae, where they emerge and sendoff branches comparable to those which join the internal and externalcarotid arteries.It should be noted that in most orders and families of birds the rightdorsal carotid artery comes to lie in a position dorsad to the leftdorsal carotid artery, within the hypapophysial canal. This par-ticular orientation of the carotids may be attained as a result of thegrowth of the ventral cervical muscles and their encroachment upon332543?55 2 542 PROCEEDINGS OF THE NATIONAL MUSEUM vol. i04the space occupied by the carotids within the hypapophysial canal.Further reduction in size of the hypapophysial canal, by the en-croachment of the aforementioned cervical muscles, may account,in part, for the fusion of the two carotid arteries and the resultingformation of the unicarotid arrangement.While I have noted this orientation of left and right carotids withinthe hypapophysial canal many times, Bhaduri and Biswas (1954)have made particular mention of the condition.Commonest of the modifications which occur because of the posi-tion of the dorsal radices (dorsal carotids) is that of fusion of thesevessels between the third arch and the base of the head. As a resultof this fusion of the two primary dorsal carotids, a single vessel trav-erses the length of the neck. In some orders of birds the basal por-tion of both vessels are present, while in other orders or families onlythe basal portion of one of the conjugate vessels is present. In stillother instances, a vestige of the atrophied vessel remains as evidenceof its earlier embryonic relationship in the system. When both basalportions of the conjugate vessel are present they may be equal orone side may be reduced in diameter. At the cephalic end of theconjugate carotid both left and right carotids are given off before theyfurther divide into the several internal and external branches. Thesebranches, as Hughes (1934) has pointed out, are not the same forbirds as for mammals.Reduction in the lumen of the basal portion of the dorsal carotidsmay occm- on either side, and still further alteration in this portionof the carotid may occur in the form of atrophy, with retention ofeither a complete or an incomplete ligament. Insofar as I can de-termine, this ligament has never been described in any of the literatureheretofore, and no name has as yet been assigned to it. Ottley(1879) described the presence of two white imperforate cords lyingwithin the hypapophysial canal of Bucorvus abyssinicus. These hebelieved to be the remnants of the dorsal carotids. In recent studiesI have had the opportunity of observing the same or similar structiu"eswhich are definitely the ligamentous vestiges of the dorsal carotids.Since these structures were originally noted by Ottley, it would bewell to refer to them as the ligamenti ottleyi. In forms which presentligaments on both sides (ligamenti ottleyi), the blood supply to thehead is carried by enlarged vertebral and superficial cervical arteries.When the paired dorsal radices aortae (anterior) do not enter thehypapophysial canal, the dorsal carotids may become fm-ther modifiedand may be reduced in size. In both Zanclostomus javanicus javanicusand Phaenicophaeus pyrrhocephalus the dorsal carotids were found tobe superficial vessels, much reduced, and functionally modified asoesophageal arteries in addition to the normal function of cephalicblood supply. In Rhainphococcyx curmrostris erythrognathus the leftdorsal carotid was superficial and modified to form an oesophageal AORTIC ARCHES OF BIRDS?GLENNY 543blood supply while the right vessel was reduced to a ligamentumottleyi. Both dorsal carotids have been found to be present asligamenti ottleyi in Bucorvus abyssinicus and in Rhopodyles mridirosiris.Another variation in the arrangement of the dorsal carotids resultsfrom the superficial position of one of these vessels while the com-plimentary vessel lies within the hypapophysial canal. This isobserved most commonly among the Psittaciformes, in which orderthe right carotid enters the hypapophysial canal while the left carotidis superficial and lies in close association with the vagus nerve of thatside.Some of the aberrancies noted among related species and generaemphasize the importance of geographical and ecological distributionof species, with the resultant specific and subspecific isolation asfactors in the selection of successful types which may be found topresent these anatomical variations. In addition to other factors,anatomical variations may, in conjunction with studies of geographicaldistribution, serve to show more clearly possible lineage within afamily or order of birds on the one hand and possible routes of move-ment and dispersal in the course of evolution on the other hand.The exact site of origin of the coracoid or sternoclavicular arteryvaries somewhat in different families of birds. Generally this vesselis found as a branch of the subclavian just medial to the axillaryartery, but in a few orders it arises from different points on either thesubclavian or the pectoral stem, and in some instances two, or rarelythree, pairs of these vessels are present. In order to facilitate theclassification of these vessels the following scheme is proposed:Type A: coracoid artery is medial to the axillary.Type B: coracoid artery is opposite the base of the axillary.Type C: coracoid artery is lateral to the axillary.Type D: two coracoids are present; one is medial or opposite the base of theaxillary, the other is lateral to the axillary.Type E: two coracoids are present; both are medial or opposite the base of theaxillary.Type F: two coracoids are present; both are lateral to the base of the axillary.The thoracic, intercostal, or internal mammary artery of birdslikewise is found to arise at slightly different relative positions?froma point at the base of the inferior pectoral artery to a point near thebase of the coracoid or sternoclavicular artery, and in some instancesboth of these vessels have a common root from the subclavian artery.Such differences are found to be of common occurrence within severalorders of birds. In the Galliformes and the Passeriformes thereappears to be a graded series in the sites of attachment of the thoracicartery from a lateral to a medial position. As a result of these obser-vations, numerical values can be assigned to the site of attachment ofthe intercostal or thoracic artery, and these values may come to be 544 PROCEEDrNGS OF THE NATIONAL MUSEUM vol. i04 used as an index in specific levels of evolution. The following schemeis proposed for the classification of the thoracic arteries in birds:Type 1: attachment to the pectoral stem lateral to the axillary.Type 2: attachment to the subclavian between the axillary and coracoid.Type 3: attachment to the subclavian at the base of the coracoid.Type 4: attachment to the subclavian, but with a common root for both thecoracoid and thoracic.Type 5: attachment to the subclavian medial to both the axillary and coracoid.Type 6: two separate thoracic arteries are present; the primary thoracic is thesame as type 1 above, while the secondary thoracic is the same astype 3 or type 4 above.The medial migration of the thoracic artery appears to have somephylogenetic significance as yet not understood.Arrangements of dorsal carotid arteriesInsofar as the early embryonic stages in the development of thedorsal carotids are concerned, all birds may be considered to bebicarotid, but during subsequent stages in development many partsare deleted or functionally modified in an orderly sequence of events.As a result, higher-level deletions may be regarded as significant asindices of more recent derivation or of higher levels of species evolu-tion, and with particular respect to the aortic arch system. Mostrecent evolutionary changes in the aortic arch system are related to theadult condition of the anterior dorsal radices aortae or dorsal carotidarteries.Since the bicarotid condition is more primitive than the unicarotidcondition, the former is to be considered as representing a lower levelin the evolution of the system, and any variation of the unicarotidcondition may be considered to represent an advance over the bicarotidcondition. Within each of the main groups, however, there are certainspecial arrangements or modifications which may be regarded to be ofadditional value in determining relative positions within a family ororder with respect to the evolution of the organ system.A description of each of the known and anticipated arrangementsof the dorsal carotid arteries is essential, and to clarify the classifica-tion of the carotid arrangement it is proposed that the bicarotid condi-tion be referred to as Class A and the unicarotid condition be referredto as Class B. In addition, certain numerical values are assigned tothe variations within each of these classes, and these numericalvalues may serve as indices of levels of evolution or specialization.Further, the letters d and s serve to indicate right or left side.Bicarotid arrangements 1. Bicarotidinae normales: Both dorsal carotids enter the hypapophysial canaland pass anteriorly to the head without fusing. This arrangement is foundin most orders of birds and is to be regarded as the basic arrangement. AORTIC ARCHES OF BIRDS?GLENNY 545 2. Bicarotidinae abnormales: One of the dorsal carotids enters the hypapophysialcanal, while the complimentary vessel of the opposite side remains as asuperficial vessel. This condition is of infrequent ordinal occurrence but isvery common among the parrots, in which group the right vessel enters thehypapophysial canal in most instances.3. Bicarotidinae infranormales: Both dorsal carotids are superficial and lie alongthe ventral face of the neck. This condition is of rare occurrence. Despitethe fact that it had been presumed to exist (Meckel, 1826), it was not dis-covered until 1952 when Glenny observed it in Zanclostomus and Phae-nicophaeus and a further modification of it in Ramphococcyx. These vesselswere found to send small branches to the oesophagus. /Jf # Figure 1 10.?Points of origin and types of the coracoid or sternoclavicular and thoracicor intercostal arteries (ventral views, left side only). Type of coracoid indicated bycapital letter, type of thoracic indicated by numeral (for code see pp. 543,544): a, A-1;b, B-1; c, C-1; d, D-6; e, E-1;/, F-1; g, A-2; h, A-3; t, A-4; ;, C-5. 546 PROCEEDINGS OF THE NATIONAL MUSEUM vol. i04 4. Ligamenti carotidinae normales (ligamenti ottleyi): Both anterior dorsalradices aortae (dorsal carotids) atrophy, but remain as the ligaments ofOttley and enter the hypapoph3'sial canal. This is a condition of rareoccurrence and has been observed in Bucorvus and Rhopodytes. Thiscondition represents the culmination of the bicarotid evolution exceptfor the unicarotid arrangements.Unicarotid arrangements 1. Conjuncto-carotidinae normales: A single carotid artery enters the hj^japo-physial canal, but this is supplied by a pair of vessels of equal size from thecommon carotids of both left and right sides. This arrangement is quitecommon among the Ciconiiformes.2. Conjuncto-carotidinae abnormales: The same as in 1, above, except that thebasal vessel is reduced in diameter on one side. This is the first level in themodification of the conjugate carotid arrangement and is found in theflamingos and herons.3. Ligamentum carotidinae-conjuncti: As in 2, above, or further modified exceptthat the lumen of the reduced vessel is not complete and the distal portionof the basal vessel is reduced to a ligament. This condition is found toexist at two levels of atrophy: (1) second level modification results fromatrophy at the anterior end of one of the basal vessels, but with a lumen fornearly half of its length, and (2) third level modification results from com-plete closure of the basal vessel with retention of a ligamentous vestige.This ligament may be entire or partial. The degree of resorption appears tovary in different species.4. Laevo-carotidinae or dextro-carotidinae normales: The same as in 3, above,except that there is no remaining vestige of the ligamentous connection fromthe opposite side. This is the fourth level modification of the unicarotidarrangement and is commonly found in many orders of birds.5. Laevo-carotidinae or dextro-carotidinae infranormales: The same as 4, above,except that the functional carotid is superficial and does not enter thehypapophysial canal. This has been reported in a single passerine genus,Orthonyx.6. Ligamentum unicarotidinae (ligamentum ottleyi): The culmination of theunicarotid evolution results in atrophy of the single dorsal carotid artery.This may be at either of two levels: (1) retention of the ligamentous vestige,or (2) partial or complete resorption of the ligament. In such a case, thevertebrals and superficial cervical arteries will take over the function ofsupplying the blood to the head.To simplify and codify the above classification of carotid arrange-ments, the following scheme is suggested; it may serve to indicatemore nearly those close similarities and gi-oss dissimilarities whichmay be presumed to exist and to indicate which orders of birds may beundergoing important anatomical evolution:Class AA-1 Bicarotidinae normales.A-2-d Bicarotidinae abnormales: right vessel superficial.A-2-S Bicarotidinae abnormales: left vessel superficial.A-3 Bicarotidinae infranormales.A-4 Ligamenti carotidinae normales (ligamenti ottleyi). AORTIC ARCHES OF BIRDS?GLENNY 547 Figure 111.?Arrangements of the dorsal carotid arteries and the associated cervical andthoracic arteries in Aves Bicarotidinae (ventral views). Types (for code see pp. 544-546):a, A~l; b, A-2-s; c, A-3; d, A-4. 548 PROCEEDINGS OF THE NATIONAL MUSEUM vol. io4Class BB-1 Conjuncto-carotidinae normales.B-2-d Conjuncto-carotidinae abnormales: right side reduced.B-2-S Conjuncto-carotidinae abnormales: left side reduced.B-3a-d Ligamentum carotidinae-conjuncti: partial lumen; ligament on theright side.B-3a-s Ligamentum carotidinae-conjuncti: partial lumen; ligament on theleft side.B-3b-d Ligamentum carotidinae-conjuncti: entire, on right side.B-3b-s Ligamentum carotidinae-conjuncti: entire, on left side.B-4-d Dextro-carotidinae normales: right carotid alone enters the hypapo-physial canal.B-4-S Laevo-carotidinae normales: left carotid alone enters the hypapo-physial canal.B-5-d Dextro-carotidinae infranormales: right carotid is superficial (left islacking).B-5-S Laevo-carotidinae infranormales: left carotid is superficial (right islacking) . B-6a-d Ligamentum unicarotidinae (ligamentum ottleyi): entire, right side.B-6a-s Ligamentum unicarotidinae (ligamentum ottleyi): entire, left side.B-6b-d Ligamentum unicarotidinae: incomplete or lacking, right side.B-6b-s Ligamentum unicarotidinae: incomplete or lacking, left side.By means of this codified classification, all birds can be placed inone of two major groups with respect to the adult carotid arrangement,and these in turn may then be further subdivided to show their ap-parent value with respect to levels of evolution and possible phyleticrelationships. Furthermore, this carotid classification may be usedto show both species evolution and, ontogenetically, the course ofchanges which took place during embryonic development.This scheme has the advantage of being able to show where large(macro) or small (micro) steps in avian evolution of the aortic archsystem has taken place. It also has the particular advantage ofdemonstrating the probable ontogenetic course of events which tookplace within any single or individual specimen.Arterial arrangement-patterns in neck and thoraxClass AVESBasically bicarotid. Several functional and structural modifica-tions are found in both families and orders.As in other amniotes, the carotid, systemic, and pulmonary archesalone remain as functional derivatives of the embryonic aortic arches.The left ligamentum botalli atrophies and may become incorporatedinto the ligamentum aortae or it may be completely resorbed. Theright ligamentum botalli may remain as a persistent vestige of theductus botalli or it may be reduced to a ligamentous "button"; itmay be incorporated into the wall of the right radix aortae or becompletely resorbed. AORTIC ARCHES OF BIRDS?GLENNY 549The right systemic arch alone remains as the functional vessel carry-ing blood from the aortic root to the functional radix aortae. Biswas(1946) has reported the occurrence of both a left and right systemicarch in a specimen of Ploceus pkilippinus philippinus, along with apatent left radix aortae which was occluded at the posterior end.A left ligamentum botalli was present in this specimen. J '^ fWY Figure 112.?Arrangements of the dorsal carotid arteries and the associated cervical andthoracic arteries in Aves Unicarotidinae (ventral views). Types (for code see pp. 546,548-549): a, B-2-d; b, B-1; c, B-2-s; d, B-3a-d;