THE ADAPTIVE MODIFICATIONS AND THE TAXONOMICVALUE OF THE TONGUE IN BIRDS
By Leon L. Gardner,Of the United States Army Medical Corps
Since the work of Lucas 1 there has been little systematic investiga-tion on the tongues of birds, and with the exception of an occasionaldescription the subject has been largely neglected. It is in the hopeof reopening interest in the subject that this paper is written.As is well known the tongue is an exceptionally variable organ inthe Class Aves, as is to be expected from the fact that it is so inti-mately related with the birds' most important problem, that ofobtaining food. For this function it must serve as a probe or spear(woodpeckers and nuthatches), a sieve (ducks), a capillary tube(sunbirds and hummers), a brush (Trichoglossidae), a rasp (vul-tures, hawks, and owls), as a barbed organ to hold slippery prey(penguins), as a finger (parrots and sparrows), and perhaps as atactile organ in long-billed birds, such as sandpipers, herons, and thelike.The material upon which this paper is based is the very extensivealcoholic collection of birds in the United States National Museum,Washington, D. C, for the use of which and for his abundant aidin numberless ways I am very much indebted to Dr. Charles W.Richmond, associate curator of the Division of Birds. To Dr.Alexander Wetmore, assistant secretary in charge of the UnitedStates National Museum, I wish to express my thanks for his kindassistance in reviewing the paper and for his help in its preparation.Part of the material is from my own collection which is now filedwith the Museum and which came to me in many ways. Dr. WitmerStone, director of the Academy of Natural Sciences of Philadelphia,furnished me with much from foreign sources for which I am greatly
1 Lucas, F. A. The Taxonomic Value of the Tongue. in Birds, The Auk, vol. 13, No. 2,April, 1896, pp. 109-115.Lucas, F. A. The Tongues of Woodpeckers. Bulletin No. 7, U. S. Department of Agri-culture, Division of Ornithology and Mammalogy.Lucas, F. A. (1897). The Tongues of Birds. Report of U.S. National Museum, 1895,pp. 1003-1020.No. 2591.
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Proceedings U. S. National Museum, Vol. 67, Art. 19.43316?25 1 1
2 PROCEEDINGS OF THE NATIONAL. MUSEUM vol.67indebted. J. Eugene Law, Altadena, Calif., provided me withmuch valuable fresh material, as did also George Willett, Los An-geles, Calif., to both of whom I wish to express my thanks.Finally I am much indebted to Prof. Charles F. Baker, Los Banos,Philippine Islands, for his assistance, and to my wife for her aid inthe preparation of the illustrations.Before reviewing the variations undergone by the tongue a briefconsideration of the histology may be of interest to throw some lighton the function. ANAS PLATYRHYNCHOSA cross section through the anterior one-third of the tongue re-veals the following: The section is very irregular in shape, with adeep groove dorsally. In the center of the tongue is the single car-tilaginous and bony mass of the fused ceratohyals. Surroundingthis is a complex interlacing of adipose and connective tissue, strati-fied skeletal muscle, blood vessels, and nerve trunks. Embeddeddeeply in tissue are found groups of mucous glands, ducts of whichhere and there can be traced to the dorsal surface of the tongue.Dorsolaterally is seen a double row of cornified spines or hairs,from the base of which strands of cells are scattered deeper into thetongue. Small nerve corpuscles are seen grouped chiefly about thecornified spines. Finally the surface of the tongue is composed ofstratified epithelium through which ducts of mucous glands pass.TYTO PRATINCOLAThe extreme tip of the tongue is composed almost entirely of corni-fied epithelium. Posterior to this on section the tongue is concavedorsally, the epithelium covering this surface being a relatively thinlayer. The center of the tongue is occupied by the bony mass of theceratohyals surrounded by connective tissue with interlacing fibersof striated muscle. At the mid point between the tip and posteriormargin of the tongue mucous glands make their appearance, andfrom this point posteriorly become abundant.The glands in this species are quite superficial, being embeddedin the layer of stratified epithelium itself and opening to the sur-face through pores which are visible, with the unaided eye or asmall lens, on gross inspection. Nerve corpuscles are either absentin this species or very infrequent.PICA NUTTALLIOn section the tongue is concavo-convex, with the concavity rep-resenting the dorsal surface. The ventral surface is composed ofcornified epithelium. The dorsal surface is covered with a deeplayer of noncornified stratified epithelium. Glands in this speciesdo not appear except at the extreme posterior portion of the tongue.Nerve corpuscles are infrequent.
akt.19 CONCERNING BIRDS ' TONGUES GARDNER 3CARPODACUS MEXICANUS FRONTALISThe section is cordiform in shape. The ventral and lateral sur-faces are covered with thin cornified epithelium. The dorsal sur-face is composed of a thick knoblike mass of stratified squamousepithelium through which no glandular ducts were seen to pass.Several large nerve trunks pass through the length of the tonguebeneath the branches of the ceratohyals. Nerve corpuscles arefound in the posterior end of the tongue.It is apparent even from such a brief survey that the tongue mustserve, in part in some species at least, as an accessory salivary gland.In addition tactile sense must be ascribed to it, if not even that oftaste, as Botezat 2 suggests.The variations found in bird tongues are very extensive and oftencomplex.Embryological study shows that this organ in birds is primitivelya paired structure arising from the second and third visceral arches.This paired condition reflects itself in the hyoid bones, the two fore-most of which, the ceratohyals, being typically unfused and em-bedded in the flesh of the tongue itself. Posterior to this pairedposition is a median unpaired tract, the basihyal. Upon thisfoundation are constructed all the elaborate variations to be foundamong the tongues of birds. Thus the tongues of woodpeckers,which at first sight seem to be constructed on a wholly different pat-tern than that of a robin, are, on last analysis, seen to be but anextensive modification of this rather primitive type, the ceratohyalsbeing fused to a small spearlike tip and the basihyal greatly elon-gated. This is represented superficially by the small barbed sharptip, the true tongue, while behind this is the fleshy cylindricalextensive basihyal portion often spoken of as the tongue.As Lucas 3 pointed out in his work, the tongue of a robin (fig. 1)serves as a ground pattern for many modifications. In this bird itis a slender, horny, lanceolate organ, wider and fleshier at the basethan the tip and narrowing to the tip, which is translucent, corni-fied, somewhat split and frayed, with a tendency to curl.Posteriorly the tongue ends in a free edge which is deeply con-cave, with the concavity looking caudad and armed with many sharpconical spines which are firm in texture but bend readily. Laterally,
2 Botezat, E. Die sensiblen Nervenendapparate in den Plornpapillen der Vogel inZusammenhang mit Studien zur vergleichenden Morphologie und Physiologie der Sinnes-organe, Anat. Anz., vol. 34, 1908.Botezat, E. Die sensiblen Nervenendapparate und die Gesehmacksorgane der Vogel.Vortrag, gehalten auf der 77. Vers, der Naturf. u. Aerzte in Meran 1905. Referat in denVerhandlungen der Gessellschaft.Botezat, E. Morphologie, Physiologie und phylogenetische Bedeutung der Gesehmacks-organe der Vogel. Anatomischer Anzeiger, vol. 36, 1910, pp. 428-461.3 Lucas, F. A. The Tongues of Birds. Rep. U. S. Nat. Mus., 1895, pp. 1003-1020.
4 PROCEEDINGS OF THE NATIONAL MUSEUM vol.67the tongue ends in two main branches, tipped with heavy spinesmany times larger than the marginal spines. In this type of tonguethere is a definite line of demarcation between the fleshy body of thetongue and the translucent cornified tip which is frayed.In studying such a tongue for factors that are constant, one isforced to conclude that beyond the general shape and appearancethere is nothing that can be accepted as invariable. The numberof posterior spines is inconstant within the species, although theymay be counted on to be in a single row (in contradistinction to themultiple rows as seen in owls, for example)
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The length depends on the amount of wear. In a series of meadow-lark tongues collected in one day in South Dakota the length variesfrom 16 mm. to 20.5 mm. The birds were feeding almost entirely ongrasshoppers that were at that time a serious pest.The main posterolateral or heaviest spines are not invariablein arrangement ; while always present they may be bifid or in birds,as some of the sparrows, where they are normally split into two,there may be three or four subdivisions.The curling, splitting, and fraying is also variable within thespecies and shows individual modifications, although, as will be seenlater, these characters serve as very important adaptive features andundergo extensive variations in certain families.Bearing in mind these inconstant factors it is of interest to tracethe modifications that may be found of this fundamental pattern.With slight differences in curling, splitting, length, and arrange-ment of spines this tongue is to be found in a large number of pas-serine birds, as the warblers, vireos, thrushes, thrashers, crows, fly-catchers, shrikes, wrens, bulbuls, drongos, and the like, with Glareolaclosely simulating it. The divergence from the type, however, ismost marked and comes to its greatest development in the flower-frequenting forms.The typical tongue has an inherent tendency to curl, split, andfray, and any one or all of these tendencies may be combined to makeup the tongues of the flower frequenters.Thus splitting alone with little tendency to curl and no frayingis exemplified by the tongue of the flowerpeckers or Dicaeidae, whichis deeply split, forming very slender long forked tips, two in Dicaeumand four in Prionochilus.On the other hand marked curling is seen in the Old World sun-birds (Nectariniidae), where it may be a complete tube for thegreater part of its length, without fraying of the margins of thetube and with splitting into two tips either absent or very slight.Whether the tongue be a relatively short one, as in Hermotimia (fig.141), or very long as in Arachnothera, this perfect tubular arrange-ment exists in the anterior two-thirds of each. Splitting is not
art.. 19 CONCERNING BIRDS ' TONGUES GARDNER 5present in some individuals, or if present is not very deep, althoughAnthreptes is rather deeply cleft, forming two fringeless tubes.Curling and fraying of the lateral margins is illustrated by theDrepanididae. In Hemignathus (fig. 19), Himatione, Ghlorodre-panis, VesHaria, and Heterorhynchus it is long and slender, curledinto a complete tube, the edges of which are delicately frayed, withthe tip ending in a much frayed but not bifid brush.Finally, beginning with Dendroica tigrina (fig. 2), an interesting-series of split and frayed tongues can be demonstrated. In thiswarbler the maximum of curling in the Mniotiltidae is reached,Baird 4 going so far even as to suggest a separate genus for it.From this it is a near step to the curled tongues of Zosteropssimplex and Z. japonica, which are described by Beddard 5 as beingcurled into almost a complete tube with a much frayed tip.The next step can be traced through the Icteridae, where in Icterus(fig. 3) it is curled, in the anterior one-third to one-half, withelaborately frayed edges and somewhat split to form two semi-tubular fringed tips. The Coerebidae carry this still further.Glossoptila {Euneomis) makes no advance, with only moderatecurling, splitting and fraying at the tip. Ghlorophanes (fig. 4) iscurled in the anterior one-half and is split and frayed, but thetongue is not yet tubular nor has it reached that stage in Gyanerpes.But in Diglossa and Coereba (fig. 5) it is found to have become acomplete tube by the overlapping of the upcurled edges and thesplitting involves the entire anterior one-half of the tongue, so that,instead of one, we find two complete tubes highly fringed andfrayed. Finally this splitting has reached its maximum in theMeliphagidae, so that in Myzomela rubratra (fig. 6) it has becomea completely curled tongue in the anterior half, splitting into fourtubular frayed tips.The examples might be unnecessarily multiplied. Suffice it to saythat such a study brings to light a most interesting series of elabo-rately modified tongues, the exact correlation of diet with whichoffers material for future study.Returning to the ground pattern we can see a close resemblance be-tween it and the tongues of some of the motmots and todies (seefig. 74), in which birds it is rather flat and the thin horny trans-lucent tip constitutes as much as one-half of the organ.A curious little variation is seen in the titmice (see fig. 123). Inthese birds the cartilaginous tips of the ceratohyals project throughthe tip of the tongue and with two lateral projections form whathas been likened to a four-tined pitchfork. The nuthatches (fig.
* Baird, S. F. Review of American Birds, November, 1864, pp. 161-162.5 Beddard, F. E. Ibis, ser. 6, No. 3, 1891, pp. 510-512, Tongue of Zosterops.
6 PEOCEEDINGS OF THE NATIONAL. MUSEUM vol.67121) modify this by having six or seven tangled tips well calculatedto collect small insects and spider eggs from the crevices of tree bark.Such, in brief, is a survey of the modifications of the type patternseen among birds. There are, however, many tongues that are ap-parently fashioned on other foundations. Among these are foundmany of the shore and water birds. Thus the tongue of a gull (fig.28) (Larus) might be selected as a type. In these forms, according toGiebel,6 the ceratohyals tend to fuse into one bone. Superficiallyone sees this manifested by a rather fleshy organ which, while havinga median depression or groove running the length of the tongue, stillhas no tendency to curl and, while often very slightly incised orfrayed at the tip, is not split to any degree. Such a tongue, varyingin length and breadth, is to be found in a large series of rails, sand-pipers, terns, plovers, and the like.Some interesting adaptations are to be noted especially among thefish feeders. If the tongue is edged laterally with sharp spines forone-half or more its length we would have it as seen in the petreltribe, fulmars (fig. 25) and shearwaters; loons (fig. 23) modify thepattern by concentrating all the spines in one large sharp patchposteriorly. Finally if this process is continued so that the wholesurface of the tongue is covered with retroverted spines we wouldhave the condition as represented by the penguins.Another ground pattern is seen among the woodpeckers (fig. 13).As has been noted the basihyal has been greatly lengthened in thesebirds whereas the ceratohyals are fused as a small conical tip. Thetrue tongue then is represented by the sharp horny white tip armedwith lateral, backwardly directed spines, while behind this is thelong extensile wormlike basihyal portion which, when drawn backinto the mouth, inverts and forms a sheath into which the rest ofthe organ can be retracted. This portion is covered with minutespines scarcely visible to the unaided eye, the apparent function ofwhich is to hold the saliva, which is especially abundant in thesebirds. This pattern is characteristic of the family Picidae and isseen in no other forms.An odd pattern is assumed by the Ardeidae (figs. 31-34) in whichit is long, fleshy, and cylindrical, the characteristic feature being,however, the absence of sharp spines at the posterior margin of thetongue. Instead is found only a soft, fleshy flap, somewhat ser-rated in outline, ending laterally in large but flexible tips.Among the Anatidae (fig. 9) again this organ assumes a char-acteristic appearance undergoing many interesting variations tobe described later.
* Giebel, C. Die Zunge der Vogel und ihr Geriist, Zeitschr. fur die Gesammten Natur-wiss., vol. 11, 1858, pp. 19-53.
art, 19 CONCERNING BIRDS ' TONGUES GARDNER 7Hawks, owls, and vultures have powerful rasping tongues, astructure that does not seem to be based primarily on the funda-mental pattern. For in most of these birds the ceratohyals, accord-ing to Giebel,6 are fused the greater part of their length except atabout the mid point, where by reason of failure of fusion a holeis left.Parrots display an individuality of their own. In many of thesebirds the tongue is broader at the tip than at the base, formingalmost a finger, with the anterior margin convex. It may be flat,cupped, grooved, rolled into a tube, or even brush-tipped (figs.70-73).Finally, without considering the various rudimentary tonguesthere are a host of odd types scattered throughout the class Aves,such as the curious feathered tongues of the toucans (fig. 87) ; thatorgan as found in the puff-birds (fig. 83), the cuckoos, the flamingoes,and the like. One is constantly impressed with the fact that noreliable guess as to the tongue form can be made by the appearanceor function of the bill and that any generalization is a very un-certain procedure.The color of the tongue is interesting only in passing. Usuallyflesh colored, it may not be so, however, often taking the color of thebill or assuming a color of its own. Thus it is black in the crow andits allies ; has brown spots in some swallows ; may be entirely blackwith white spines in that odd cuckoo, the road-runner (Geococcyxcalif'ornianus) , or be almost entirely flesh-colored, mottled withblack, in other members of the same species. It is pink in the red-billed Heermann gull (Larus heermanni). It is said to be scarletin the black cockatoo. Still again a light blue is seen. Some ofthe hawks, as the marsh hawk (Circus hudsonius) , have the posteriorend and the spines this color.Out of this confusing multiplicity of form it seems possible tomake certain groupings as to function and adaptation. And ifthis is done one finds approximately eight natural groups areformed
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1. An omnivorous diet is productive of a rather generalized pat-tern. This includes the great majority of tongues found in thePasseriformes, as has been described. The chief adaptive featurelies in the presence of the posterior marginal spines. The tongue iscapable of being depressed at the tip and elevated posteriorly.When worked rapidly backward and forward it can be used toforce resistant food down the throat. The efficacy of this is mostastonishingly manifest if, for instance, a bit of cloth be fed to anestling. In such an instance it is only with difficulty that thecloth can be withdrawn from the throat without injury to the bird,so eagerly is the tongue with its spines used to resist the effort.
8 PROCEEDINGS OP THE NATIONAL MUSEUM vou 67In this group falls also the simple fleshy tongues of the gallina-ceous birds (fig. 7).2. Fish eaters, where the tongue is used to hold slippery prey.In these it is found to be plentifully supplied with sharp, stiffretrorse spines. These may be distributed over the whole sur-face, as in the penguins, edging the lateral margin only as in thefulmars and shearwaters (fig. 8), as a patch of stiff spines situatedat the base, as in the loons, or a double row on the surface, as inmergansers (fig. 10). A distinction must be drawn between fisheaters that use the tongue and those in which the food is boltedwhole, where it has lost its function and a different condition pre-vails.3. A diet of a multiplicity of small things strained from the wateris associated with the complex tongues of the Anatidae (fig. 9).Typically it is roughly rectangular in shape and is thick and fleshy.The tip is composed of a cornified rounded flaplike process. Pos-terior to this the tongue is broad with a median groove and providedlaterally with a double row of heavy hairs, the upper overhangingthe lower like a thatched roof. Toward the posterior half the upperrow, by a process of agmination of the hairs, becomes converted to aseries of large, heavy spines, which vary in number with the differ-ent species. Coincidentally the edges of the median groove becomecornified with rough, toothlike processes. Lateral to these the sur-face of the tongue is nodular or papillar and plentifully suppliedwith openings of ducts of muscous glands. The posterior portion ofthe tongue is made up of a fleshy eminence heavily armed withstrong spines.The method of use is interesting. The tongue is depressed, allow-ing water to run along the groove, it is then raised against the palate,the water squirted out from the sides through the hairy edges,straining out and leaving the solids.Considerable variation is seen, depending on the use of this organand the width of the bill. Thus in the geese and swans where it isused for tearing up weeds and grasses it has become a very power-ful tearing structure. In Cygnus buccinator, for example, theedges of the median groove instead of consisting of rather roundedeminences become very sharp, long tearing spines.A similar purpose is accomplished by Branta nigricans by con-version of the entire lateral row of hairs into spines ; in other words,all of the lateral hairs have become agglutinated into spines, and thisprocess extends quite to the tip.On the other hand the red-breasted merganser (fig. 10), havingtaken to fish fare, has developed sharp dorsal spines and lost onerow of marginal hairs, tending to approach in type the fish eaters.
art., 19 CONCERNING BIRDS ' TONGUES GARDNER 9
4. Flesh feeders or the birds of prey, including the owls, havedeveloped heavy rasping tongues. The anterior portion is oftenvery rough and hard and in some forms somewhat curled as ineagles and lammergeiers. The posterior spines, which may be in asingle or multiple row, are stiff and hard. Opening to the surfaceare ducts of many mucous glands the function of which is manifest.A curious modification of form is seen in the deep trough-shapedtongues of the vultures and the condor, which are armed with sharpmarginal spines (figs. 36-43).5. Where the food is probed for and consists largely of insects wesee the structure as exemplified by woodpeckers. Lucas 7 has dem-onstrated an interesting correlation with diet. Flickers (fig. 14),having made a departure from the regular fare and having taken toan ant diet, are found to possess a blunt-tipped tongue with but twoor three reduced barbs, while the extensibility is greatly increasedand the whole dorsal tract (basihyal position) plentifully suppliedwith minute spines to hold mucous. In these birds also the sub-maxilliary salivary glands reach their maximum development, acombination well adapted to catch ants.In Melanerpes (fig. 15), where the diet has become more gener-alized, it will be found that the extensibility is reduced and insteadof spines at the tip there has been a conversion to vibrissae or hair-like processes.Finally in the sapsuckers (fig. 16) the extensibility is reduced toa minimum. The dorsal tract is bare of spines except posteriorly,where it is widened into a shieldlike structure bearing papillae. Atthe tip and along the lateral edges there is a fine brush of hairswhich serves well for capillarity but is ill adapted to spearing grubsnor are many of these found in an analysis of stomach contents.Among this group should be classed the spearing and impalingorgans of the titmice, and nuthatches, already described.6. Seed and nut eaters have fleshy and strong tongues. In thisgroup are to be classed those of the typical parrots (fig. 17) andfinches (fig. 18). In parrots it has been described. In finches it iscylindrical or tends toward that form and slopes from base to tip.Since the ability of a bird to project the lower mandible is very lim-ited the rolling of seeds in the act of husking would be difficult.With the inclined surface of the tongue, however, acting as a sur-face against which seeds may be rolled, this is actually accomplishedmost dexterously. In many finches for reasons not entirely under-stood the tongue is often scoop-shaped or even rolled into a semi-tubular structure, as will be illustrated later.
7 Lucas, F. A. The Tongues of Woodpeckers. Bull. No. 7, U. S. Dept. of Agriculture,Dlv. Ornith. and Mammalogy.43316?25 2
10 PROCEEDINGS OF THE NATIONAL. MUSEUM vou 67
7. Flower frequenters (fig. 19) have most complex tongues.Among these we find the fringed split and tubular tongues of theDrepanididae, the Nectariniidae, Dicaeidae, some of the Icteridae,the Zosteropidae, and the Meliphagidae. In this group also fallsthe Trochilidae. Finally a most remarkable adaptation is found inthe flower frequenting parrots of the family Trichoglossidae (fig.70), where the tongue is curled at the tip and supplied with a stiffbrush of vibrissae.The correlation of such tongues with a nectar, pollen, insect, dietis easy to see. Of further interest is the fact that members of mostof these families possess the ability to very greatly extend thetongue. The hyoid bones are prolonged over the occiput in the samemanner as that adopted by the woodpeckers, and like the latter mayeven extend well down to the base of the bill.8. Rudimentary. Finally a natural group is formed of tonguesthat have lost the greater part or all of their function, a conditionfound among many families. Thus birds that bolt their food wholehave this organ often merely a little fleshy cylinder a few milli-meters long and no wider. This structure prevails in many of thefish eaters, as the booby, pelican, stork, gannet, darter (fig. 20),man-of-war bird, cormorant, and the like. Again in the huge-billedhornbills we find only a small and unimportant tongue; neither isthis organ very large or of much apparent use in their allies, thekingfishers, or again in many of the Caprimulgidae, in which familyit is often to be found small and rather simple in structure.It is apparent in such a review that in a large number of formstongue structures can be correlated with some special diet and themethod of its procurement as might well be expected of an organso intimately concerned with the function of obtaining food. Theexceptions, however, are numerous and present most interesting prob-lems. For example, no special adaptation is to be noted in thetongues of gulls, rails, sandpipers, and the like unless, as it seemsnot at all improbable, special tactile or even taste sense is located inthem. Added to these are certain odd and rather complex tonguesthe unusual shapes of which are difficult to explain. An instance isthis organ in the fruit-eating trogons (fig. 21). It is triangular,thick, heavy, horny tipped, with a central groove bordered by dis-tinct ridges and heavily armed posteriorly with spines. The mot-mots have a long slender structure, thin and horny and much frayedlaterally, somewhat resembling that found in toucans (fig. 87), inwhich birds, again, a most curious featherlike organ is found with thefrayed lateral margins directed anteriorly, the significance of whichcan not be evaluated at present.
art, 19 CONCERNING BIRDS ' TONGUES GARDNER 11In addition a most difficult problem is the explanation of varia-tions in closely related birds where presumably the diet is verysimilar. Thus Lucas 8 called attention to the variation foundin the genus Melospiza. In M. fasciata a much-frayed tip isfound, while in M. lincolmi the tip is only slightly bifid and notfrayed. To this may be added the genus Zosterops, with a forkedand smooth tongue in Z. lateralis, while it is much curled andfrayed in Z. simplex and Z. japonica. Still again among thewarblers of the genus Dendroica it varies from a flat and onlyslightly split organ in D. petechia (fig. 155) and D. fusca (fig. 158)to a much curled split and frayed one in D. tigrina (fig. 2).The taxonomic value of the tongue in birds is an interestingquestion which can only be answered by a systematic survey. It isevident that the most useful characters for classification are thosefounded on strict morphological bases and any structure highlymodified in response to external stimuli is of the least value. Butno one organ has ever been found that can serve as a completebasis for classification. The history of ornithology evidences manymistakes due to the use of one character alone, as witness the oldgroup Pinnatipedes, including phalaropes, coots, and grebes, throughsimilarity of foot structure. In considering the value of the tongueit must be recognized that it is a highly adapted organ, but thisshould not rule it out from all taxonomic consideration. If everystructure adaptively modified be omitted no part of a bird can beused, since to a greater or less extent this includes the wholeorganism. Lucas,s taking note of the adaptive modifications, givesit very little taxonomic value. There is, however, need of a sys-tematic study of this organ in every group, with an evaluation of itin each one. While tongues are adaptively modified it may well bethat these changes are constructed on a type pattern distinctive ofthe group to which the bird belongs and thus indications of affinitybe given. Order COLYMBIFORMESLoons are distinguished from grebes by the fact that the tonguesof the former have a large patch of spinose processes at the base,while the grebes have but a single row posteriorly. Gavia immer(fig. 23) has a relatively large patch, while this is not so prominentin the Pacific loon, Gavia pacifica (fig. 22). Podilymbus podicepsand sEchmophorm oecidentalis among the grebes have but a weakrow of spines, which in the eared grebe Colymbus nigricollis cali-fomicus (fig. 24) are prominent but broad and flat.
8 Lucas, F. A. The Taxonomic Value of the Tongue in Birds. The Auk, vol. 13, No. 2,April, 1S96, pp. 109-115.
12 PROCEEDINGS OF THE NATIONAL MUSEUM vol.67Order SPHENISCIFORMESThe penguins so far as known have a characteristic tongue. Itis rather long and pointed and the surface is entirely covered withlarge stiff conical retroverted spines.Order PROCELLARIIFORMESIn this group there is considerable variation. On the whole ittends to be rather small in comparison to the bill and gape. InBulweria bulweri it is very small, approaching rudimentary,while in Macronectes and Prion it is larger and more nearly matchesthe bill in size. In some genera it is well armed with spines, notonly posteriorly but along the sides almost to the tip. Thus Ful-marus glacialis glupischa (fig. 25), Pterodroma hypoleuca, andPuffinus cuneatus have lateral spines for the posterior third, whileBulweria bulweri extends this to one-half and Puffinus griseus (fig.8) and Prioftnus cinereus are supplied the whole length of thetongue. This characteristic does not hold good for the entirefamily Procellariidae, however, since lateral spines are lacking inHalobaena coerulea and Prion desolatus. In the former onefinds a rather small, cylindrical, fleshy tongue armed with a singlerow of very weak spines and tapering to an unsplit tip. The latterhas lost most of the posterior row, so that this edge is often a smooth,rounded margin. Occasionally one finds a few inconspicuous spinesburied in tissue, the value of which must be negligible.The Hydrobatidae have very small tongues. Oceanites oceanicusand O. gracilis possess small fleshy cylinders with a weak rowof spines. Order CICONIIFORMESThis is a rather unwieldy group with tongues that vary fromminute rudimentary structures to the large fleshy one of theflamingoes.The Steganopodes are characterized without exception, so far asis known, by rudimentary tongues. In Phalacrocorax, Sula, Pele-canus, and Anhinga it is a mere toothpick of flesh. Anhinga anhinga(fig. 20) has a curious little tonguelike eminence on the dorsum ofthe cylindrical rudiment. Phalacrocora-x has a tongue composed oftwo plates of cornified tissue meeting in the midline and slopingsharply like a steep roof. Fregata minor presents a small triangularstructure which has not as yet lost all form and on the surface ofwhich posteriorly are to be found abortive spines.The Ardeidae have a most characteristic organ already described,the most outstanding feature of which is the soft fleshy posterior
art. 19 CONCERNING BIRDS ' TONGUES GARDNER 13flap connected with flexible lateral "horns." So far as has beendetermined this is a form not approached by any other family ofbirds and once having been seen is so characteristic that it couldnot be confused with any other form, most especially with the storkswith which herons have often been classed and with which theyagree in feeding habits. It is long in Ardea herodias (fig. 32) andshorter in Nycticorax nycticorax naevius (fig. 31) but with the samegeneral structure throughout, including Egretta candidissima, Cas-merodius egretta., Botaurus lentiginosus (fig. 33), and Butoridesvirescens anthonyi (fig. 34).Of great interest is the fact that in that odd-billed form theboat-billed night heron {Cochlearius zeledoni) the same structureis preserved. The tongue is very short but is constructed exactlyas in the other herons, much as if the tongue of Ardea was cut tothe length of an inch or less.The storks (Ciconiidae) have rudimentary tongues, as do theIbididae (Threskiornithidae). Ciconia ciconia (fig. 26) has a flatalmost formless structure, while Plegadis guarauna has one that isvery small but with some semblance of structure, as there are well-defined spines present which, however, are flexible and functionless.The flamingoes (Phoenicopteridae) are characterized by fleshytongues supplied on the dorsum with conical spines and posteriorlywith a patch of spinose processes. These curl downward, as do thebills. Figure 11 illustrates the tongue of Phoenicopterus ruber.It is interesting to note that the four suborders are readily sepa-rated by tongue form. The Steganopodes by rudimentary cylindricalones (except Fregata), Ardeae by their characteristic ones, Ci-coniae by flat rudimentary, and Phoenicopteri by large fleshytongues. Order ANSERIFORMESThe screamer (Chauna chavaria) of the Palamedeidae has a flattongue with a single row of spines posteriorly not at all like theAnatidae, but resembling more that organ in the gallinaceous birds.The Anatidae have a characteristic organ which, while modified inresponse to diet, is readily recognizable as distinct from all others.Most mergansers have a long slender structure with but one row oflateral hairs, while Mergus serrator (fig. 10) has a double row alongthe entire dorsal surface.In Branta canadensis and B. nigricans, for tearing purposes, allof the hairs of the two lateral rows have been converted intostrong backwardly directed spines, one row on each side, whilethe dorsal surface is smooth, without the usual gutter. Such anorgan is incapable of much if any sifting.
14 PROCEEDINGS OF THE NATIONAL, MUSEUM vol.67Chloephaga leucoptera has a very curious flat tongue. Ante-riorly there is a single row of very weak lateral spines or hairswhich a little further back develops into three heavy conical tearing
" teeth." Posteriorly it ends in a patch of small spines. This is,so far as has been seen, the simplest form found in the family.The swans have the typical structure found in the family, whichis modified, however, by having heavy tearing " teeth " along theedges of the median groove. This is true of Gygnus gibbus, G.buccinator, and C. columbianus.Coscoroba coscoroba has a very heavy organ, but the edges of themedian groove are smooth without corrified processes.Cereopsis novaehollandiae has a most aberrant form of tongue.Typically there is a very weak row of lateral spines, which may beentirely worn away as in the specimen illustrated (fig. 35). Pos-teriorly there are various fleshy processes which may be covered withweak spines, absent in the one figured however.The number of lateral "teeth" vary throughout the family androughly follows subfamily groups.Thus the Fuligulinae tend to have from three to five, usually fouron each side. While members of the same species may not show aconstant number the variation will be found to be within these limits.This is true of Oidemia, C'haritonetta, Histrionicus, Arctonetta,Marila, and Erismatura jamaicensis (fig. 29).On the other hand the Anatinae present from 5 to as high as12 lateral spines. This is true of Dendrocygna, Anas, Dafila,Poecilonetta, Mareca, Nettion, and Querquedula cyanoptera (fig. 9).Spatula, being a broad and long tongued form, has as many as 12on each side.Aix, Plectropterus, Cairina, and Dendronessa average four to theside, while typically this group is marked by an absence of cornifica-tion of the edges of the median groove.Throughout this group there is a similarity of tongue form thatmakes each one recognizable as belonging to the family Anatidae.The modifications that exist are all based on a type pattern whichis characterized briefly as a fleshy organ with at least one, andusually two, rows of lateral hairlike processes, a few or all of whichmay be agglutinated to form solid cornified toothlike projections.In these instances it is notable that dissimilarity of diet has notdestroyed evidences of relationship. Conversely, similarity of dietas compared with unrelated forms outside the family has not pro-duced similar tongues. As instance witness on the one hand thetongues of several fish eaters?mergansers, loons, and grebes?andon the other the ruddy duck with its diet closely following that ofthe American coot, and yet without paralleling it in tongue pattern.
ABT\i9 CONCERNING BIRDS ' TONGUES GARDNER 15Within the family there is no reliable basis for separation ontongue form alone. The mergansers are recognizable as a separategroup, as are the heavy tearing tongues of the geese and swans, androughly the Fuligulinae may be distinguished from the Anatinaeby the number of lateral " teeth." But with the exception of certainvery odd types that mark special genera, as Ghloephaga and Cere-opsis, or a characteristic wide tongue as in Spatula, there is oftendoubt as to what genus and subfamily a single specimen should bereferred. Order FALCONIFORMESIn this group the tongue is a heavy rasping organ. The Cathar-tidae and the Vulturidae have a deeply curled organ, trough-shaped,with the upcurled margins armed with strong rasping spines. Theserange in size from the relatively small one of the buzzard, Cathartesaura septentrionalis (fig. 38), to the large powerful object of thecondor, Sarcoramphus gryphus and Gyps fulvus, with extreme uni-formity of pattern.In the hawks the posterior border of the tongue may consist ofone row of spines or of many, and on this character they may bedivided into two natural groups; that is, the Buteonidae, with asingle row, and Falconidae, with many spines distributed over thebasal portion, as was first suggested by Beddard.9Among the Buteonidae the following genera have been found topresent but a single row of spines posteriorly
:
Milvus.Circus {Jiudsonius, fig. 40).Leucopternis.Spizaetus.Archibuteo.Dryotriorchis.Morphnus.Asturina.Urubitinga.Gypohierax.
Accipiter (cooperi, fig. 43).Astur.Elanus.Vrospiza fasciata.Ictinia.Rupornis.Buteo.B. Uneattis elegans (fig. 12).B. borealis calurus (fig. 37).B. albicaudatus (fig. 42).Pandion haliaetus has a single row, but occupies a family ofitself.The following Falconidae have been found to have many spinesdistributed over the posterior portion of the tongue
:
Tinnunculus alaudarius.Milvago chimango.Hieracidea berigora.Polyborus (plancus, fig. 41).Falco. F. sparverius phalaena (fig. 39).
9 Beddard, F. E. On the Modifications of Structure in the Syrinx of the Accipitres,with Remarks Upon Other Points in the Anatomy of That Group. Proc. Zool. Soc. Lon-don, 1903, vol. 2, pp. 157-163.
1Q PROCEEDINGS OF THE NATIONAL MUSEUM vol. 67The tongue of the lammergeier Gypaetus barbatus (fig. 36) isvery much curled in the anterior third and converted into a scoopor trough-like structure.In searching for evidences of affinity one is struck by the close simi-larity of the heavy, rasping, mucous gland bearing, spinose tonguesof the owls, which with their multiple rows of spines, resemble theFalconidae. A connecting link to the Buteonidae indeed wouldseem to be shown through the hawk owl (Surnia ulula, fig. 44).Since other evidence does not support this appearance of relation-ship it is apparent that convergent evolution and similarity of diethave so altered this organ in these divergent types that little de-pendence may be placed on it outside of limited groups.The Galliformes, so far as has been determined, all have fleshytongues, varying with the length of the bill, usually somewhatgrooved and provided with a single row of rather prominent pos-terior spines.The hoatzin Opisthocomus cristatus (fig. 45) has a triangular-shaped flat tongue the surface of which is set with small spinules.Order GRUIFORMESThe Rallidae have simple fleshy tongues varying in length withthe length of the bill. They are 'upcurled along the edges to formlong, slender, guttered or grooved organs that are usually frayed atthe tip and provided posteriorly with short and rather inconspicuousspines. They are long and slender in Pardirallus r. rytirhynchos,Rallus levipes (fig. 47) , Neocrex erythrops, and Hypotaenidia waken-sis, while in the coots (Fidica americana, fig. 53) and gallinules(Gallinula galeata, fig. 30, and Ionomis martinica, fig. 59) they areshorter and broad, and the same holds true for Porzana Carolina.The Weka rail Ocydromus earli has a rather large and heavy onewhich anteriorly is trough shaped, the edges and tip of which aresplit to form stiff forwardly directed fimbriations.Aramidae: Aramus vociferus (fig. 49) has a long slender tongueconsiderably split at the tip.Psophiidae: Psophia leucoptera has rather prominent posteriorspines. The tip is characteristically frayed and the general appear-ance not at all unlike that seen in rails.Otididae : Otis tarda has a flat tongue that is heavily armed withpowerful spines along the posterior edge and the lateral bordersfor two-thirds of the distance between base and tip. This is rathersuggestive of the tearing organ seen in the geese.Rhinochetidae : Rhinochetus jubatus has a long, slender tonguewith weak posterior spines, very slightly grooved and ending in acornified tip that is somewhat frayed.Eurypygidae: Eurypyga helias (fig. 52).
akt,i9 CONCERNING BIRDS ' TONGUES?GARDNER 17Order CHARADRIIFORMESThe tongues of the Limicolae very much resemble those of therails. They usually are commensurate in length with the bill, al-though in Numenius, Recurvirostra amerlcana (fig. 50), and Meso-scolopax borealis they lie only in the floor of the mouth and do notextend far toward the tip of the bill. The last-named species hasan exceedingly narrow tapering organ that in the anterior portionbecomes almost threadlike and does not measure more than one-third the length of the bill. In the rails the tip was found oftento be split and frayed while the sandpipers generally have a tipentire. Usually the tongue is guttered or grooved but in the generamentioned above it tends to be flat. It may be very long as in Cato-ptrophorus semipalmatus inornatus, and the long-billed dowitcher{Limnodromus griseus scolopaceus, fig. 48) and less so the wander-ing tattler, (Heteroscelus incanus, fig. 46), while it is very short inthe semipalmated plover {Charadrius semipalmatus, fig. 60).Other variations are seen in Actitis macularia (fig. 54), Oxyechusvociferus (fig. 58), Haematopus palliatus (fig. 61), and Ereunetespusillus (fig. 57). There is nothing unusual about this organ inOreophilus ruficollis ruficollis, Pisobia minutilla, Grocethia leucop-tera, or Squatarola squatarola. In this group, as in the hawks andowls, due to convergent evolution or to the fact that feeding habitsare alike there has developed a very close resemblence to the tonguesof rails and an indication of affinity when in fact it is not as realas this organ would lead to believe. So close is the appearancebetween the groups that given a single tongue one would often bein doubt as to its true connection.The gulls have a rather broad fleshy tongue that is somewhatgrooved and is often forked at the tip, as illustrated by La?ms heer-manni (fig. 27) and L. occidentalis (fig. 28). The terns have long,slender, often forked tongues {Sterna forsterl, fig. 56) and S. antil-larum, fig. 55). Gygis alba kittlitzi has remarkable fine backwardlydirected serrations for the anterior one-half of this organ.Rynchops nigra (fig 51) has a rather short, wide tongue, some-what scoop shaped.Pigeons have flexible tongues that are grooved and posteriorly aresupplied with soft spines that are without resistance. These areillustrated in the following figures, Zenaida vinaceorufa (fig. 65),Columba gymnophthalma (fig. 66), Histriophaps histrionica (fig.63), and Geopelia cuneata (fig. 64), while Nesopelia galapagoensisis very similar.4331G?25 3
18 PROCEEDINGS OF THE NATIONAL MUSEUM vou 67Order CUCULIFORMESIn the cuckoos the tongue is rather heavy, long-, and well providedwith spines. There may be considerable variation in length in thesame species, as illustrated by that odd form Geococcyx califomianus(figs. 67, 68), while the color may be entirely black with white spinesor flesh colored with a few black spots. SaurotJiera dominicensis(fig. 69) has much fimbriated edges which are directed forward.Coccyzus melacoryphus has a very similar structure. Carpococcyxradiatus is well armed posteriorly, but the edges are not split nor isthe tip. Order PSITTACIFORMESThe parrots are characterized by considerable differences intongue shape. In the common grass parakeet (Melopsittacus un-dutatus, fig. 72) it is flat and broad, while it is broad but hollowedout in Aprosmictus cyanopygius (fig. 71), Conurus auricapillus (fig.17), and Poioceplialus senegalensis. It is tightly rolled in Calopsittanovaehollandiae (fig 73), while, as is well known, it is brush tippedin the Trichoglossidae, as illustrated by Psitteuteles chlorolepidota(fig. 70), Glossopsltta, Hypocharmosyna, and Triehoglossus, and inwhich group the tongue is used as the main taxonomic feature.Order CORACIIFORMESCoracias caudata has a lingual structure very similar to that of arobin, with a horny split tip. It is not commensurate in size withthe heavy bill, while posteriorly there are very few spines.Eurystomus. In this large heavy-billed form the tongue is wideand flat, the anterior one-half is horny and frayed, while at the backthere are three to four large heavy spines on each side.The motmots have flat, heavy tongues that are considerably frayedlaterally with laciniae that are directed forward. In Eumomotusswperciliaris this is carried to such a degree that it strongly sug-gests the feathered structure seen in the toucans. Momotus caerulei-ceps is not unlike the tongue of Saurothera in its general appear-ance.The todhs have the anterior half thin, horny, and translucent, butthe edges are merely roughened and irregular and not deeply in-cised. Todvs id ult trotor (fig. 74) is illustrative.In kingfishers (Alcedinidae) this organ has become rudimentary.In Ceryle oleyon (fig. 75) it is flat without the posterior row ofspines although Ceryle rudis may show a few. The large billedPelargopsis (Ramphalcyon) has a structure very similar to Cerylewith the exception that the tip is either square or even somewhat
art., 19 CONCERNING BIRDS ' TONGUES GARDNER 19indented while the whole organ is quite rudimentary. There is nosuggestion of affinity between these forms and the motmots.The hornbills (Bucerotidae) also have rudimentary tongues, al-though they are not without form. Thus in Lophoeeros nielarwl-eucus(fig. 84) it is flat, slender, and square tipped, while in the huge billedHydrocorax mindanensis it is rather triangular, fleshy and suppliedAvith a few small spines, and this is true also for Dichoceros bi-comis.Upupidae: The hoopoes have exceptionally small rudimentarytongues which are reduced to a mere triangle of flesh without formor function.Such a review shows that a wide range of variation is seen in thesuborder Coraciae, with few indications of affinity shown and inmany forms a rudimentary structure through loss of function.The suborder Striges have tongues very closely resembling thoseof hawks, a suggestion of affinity that is misleading.They are horny tipped and well beset with papillae, while mucousgland pores are abundant, an appearance much like that of theFalconidae and due either to convergent evolution or to the rap-torial diet. There is usually a certain degree of curling and the tipis often somewhat incised. As examples are shown Tyto pra.tincola(fig. 78), Speotyto cunicularia hypugaea (fig. 76), Otus asio bendi/ei(fig. 79), Spiloglmix novae zealandiae (fig. 80), and Asio wilsoman us(fig. 77). The hawk owl (Surnia ulula, fig. 44) has but one row ofspines posteriorly, the reason for which is not apparent. The hornedowl (Bubo virginianus) has a broad, flat tongue well covered withspines. Suborder CaprimulgiIn this group, Wetmore 10 finds four main types of tongues. Firstthat of Nyctibius, which he describes as " small in proportion to themouth cavity as in other Caprimulgi. In form it differs consider-ably from the tongues of related genera. The tip of the tongue inNyctibius is somewhat elongate, with the lateral outlines at firstconcave. The postero-lateral margins are produced as elongatepoints that equal the anterior portion in length. The outline of thelateral margin of these is convex. In general the form of the tongueis that of the head of a spear point, with a deeply incised base,spreading posterior angles, and slender point." He finds the lateralmargin supplied with spines and a few minute spines on the uppersurface.Podargus is described as having an elongate tongue, being " muchlarger in proportion to the size of the mouth cavity than in other
10 Wetmore, A. On the Anatomy of Nyctibius, with Notes on Allied Birds. Troe.U. S. Nat. Mus., vol. 54, pp. 577-586, 1918.
20 PROCEEDINGS OF THE NATIONAL MUSEUM vol.67forms examined. The anterior end of the hyoidean apparatus formsa thickened, pointed projection in the tongue base. * * * Ante-rior to this strong base the tongue is thin and translucent, being notmuch thicker than a sheet of ordinary writing paper."Steatomis caripensis shows a "tongue shaped like an arrowhead,with rather elongate, bluntly pointed tip, convex lateral outlines,and spreading, somewhat slender posterior processes that projectbeyond the hinder border. The margins of these posterior processesare armed with soft, slender, backward projecting papillae, andsmaller papillae of the same nature are found on the upper surfaceof these projections."The tongue of Phalaenoptilus nitidus " is small, measuring 9.5 mm.long by 3 mm. broad. The postero-lateral spinose processes areelongate and pointed. The lateral margins in outline are approxi-mately straight lines. Spinose backward projecting papillae beginat a point anterior to the center and become stronger and heaviertoward the base of the tongue. The upper surface of the tongue forits basal two-thirds is thickly set with small horny papillosities allprojecting backward. Because of the posterior elongation of thelateral processes, the basal margin appears deeply incised."This is the general form of the remaining genera of the Capri-mulgidae. The tongue of Chordeiles virginianus is described asshowing a " slightly different development. This organ in thenighthawk is small in comparison to the size of the mouth opening,but is strong and heavy. It measures approximately 9 mm. long by4.7 mm. broad at the base, so that it is short and broad in comparisonwith the lingual appendages of other genera in this family that havebeen described. * * * In outline the tongue of Chordeiles virgin-ianus is triangular with the lateral margins slightly concave. * * *The lateral margins of the tongue are armed with spinose papillaewhich are small and weak anteriorly and become strong and heavytoward the base. Stronger processes arm the posterior margin, andthe broadened basal third of the tongue has its dorsal surface cov-ered with pointed harsh papillosities all directed toward thepharynx." With this description the tongue of Chordeiles acuti-pennis texensis (fig. 81) agrees, with the exception that there areno papillosities on the dorsal surface.The tongues of Nyctidronius albicollis, Caprimulgus europaeus,and Setochalcis vocifera are described by Wetmore as resembling inform that of Phalaenoptilus nitidus, while that of Chordeiles acuti-pennis is like that of C. virginianus.It can thus be seen that there are considerable differences mani-fested in this group not easy of explanation and which do not giveany important information as to affinities.The Cypselidae do not show any striking tongue characters. Insome forms there is a close resemblance to tongues of swallows, as
art. 19 CONCERNING BIRDS ' TONGUES GARDNER 21Lucas 11 pointed out in the case of Gollocalia (fig. 85, after Lucas)while others have a longer, more slender tongue somewhat curledas in the tree swift Macrofteryx coronata (fig. 82).The humming birds (Trochilidae), however, have most character-istic tongues, which are distinct from any others in the class ofBirds. The cartilaginous portions of the ceratohyals are divided inthe anterior half of the tongue to form separate shafts. These areinvested with a membranous covering which is expanded as a lateralflange at the tip, but which inrolls as the base of the tongue isapproached to form a rolled membranous tube on each side. (Seefig. 86, Calypte anna.)It is not composed of parallel muscular tubes, as has often beendescribed, for the cartilaginous shafts of the tongue are solid ; but itis the inrolled fringe of membrane along the lateral margins ofthese shafts that make up the capillary tubes. This is an entirelydifferent condition than prevails in the passerine flower frequenterswhere two or more muscular tubes are formed by splitting and curl-ing of the body of the tongue itself.It is very elastic in the humming birds and capable of great pro-trusion, the hyoid apparatus also being especially long to permit ofthis action.This is a most characteristic organ which readily identifies anybird possessing it as a member of this family, and while markedlymodified in response to flower-feeding habits is nevertheless dis-tinctive of the group and hence of taxonomic value.The trogons have flat, heavy tongues supplied with numerousspines and with a cornified tip. There is a central groove borderedby raised margins, a condition most unusual and not seen elsewhere,except in members of the next group. [Pyrotrogon neglectus, fig. 21.)The puff-birds (Bucconidae) have odd flat tongues that about thecenter widen to form prominent shoulders, gradually narrowingfrom this point anteriorly to a blunt tip. The surface is flat exceptin the anterior third, where a groove is seen, the margins of whichare raised forming parallel prominent ridges on the surface. This iswell illustrated by Bucco oicinctus (fig. 83) and is also seen inNotharchus dysoni and Nystalus maculatus striatipectus. These arevery unusual appearing structures the exact functions of which arenot known.The Ramphastidae are characterized by exceptionally odd feath-ered tongues which are long and narrow and with deeply incisedlateral margins forming anteriorly directed laminae. The fleshyhyoidean portion forms but a small part of the tongue posteriorlywhile anterior to this it becomes thin, horny, and translucent. This
11 The Auk, vol. 13, pp. 109-115, April, 1896.
22 PROCEEDINGS OF THE NATIONAL MUSEUM vol. 67change is marked by the dotted line on figure 87, of the tongue ofPteroglossus frantzii. This is so striking and characteristic an ap-pearance that it would seem useful for taxonomic purposes.The Picidae possess a tongue so distinctive of the group, thatwhile modified in response to diet, it could in no way be con-fused with that of any other family. Even the odd little piculetPicumnus, with its rounded tail so unlike that of woodpeckers, hasa tongue which, except for its small size, is perfectly typical of thegroup as exemplified by Dryobates. This is the more interestingsince the diet of so small a bird must much more nearly approxi-mate that of the creepers, titmice, and nuthatches than of its largerallies and yet the tongue remains in all respects truly that of awoodpecker.Typically the tongue is very extensile and the tip is armed withsix or seven sharp backwardly directed barbs. This is found inDryobates villosus hyloscopus (fig. 88), Dryobates nuttalli (fig. 89),Picus, Gecinus, Xenopicus albolarvatus (fig. 13), Geocolaptes, Den-drocopus, Centiirus, Chryserpes, Alicropternus, Dyctiopicus, andYungipicus. Picokles americanus dorsalis has a rather small tonguefor so large a bird, while the barbs at the tip are delicate. Veni-liomis cecilii has a small tongue with but a few barbs and the sameis true for Nesoctites ?nicro?negas. It is also surprising to note thatthe very large Phloeotomus ptleatus, with its large, heavy bill, hasan astonishingly small tongue in comparison with the rest of thebody. The tip is very short and small and is armed with but fouror five barbs.Colaptes cafer collaris (fig. 14) has the most extensible tongue,but it is not so well accommodated for impaling objects as the tip isnot as sharp, nor are the barbs prominent, being reduced to buttwo or three.Melanerpes {formicivorus bairdi, fig. 15) has converted the barbsto hairlike processes and Sphyrapicus (thyroldeus, fig. 16) has ex-tended this process for the greater part of the length of the tongue,while the ability to project this organ is much reduced.The wrynecks or Jyngidae are distinguished from the other mem-bers of the family by the fact that while the tongue is long, worm-like, and extensile, the sharp tip is not supplied with barbs. In thisgroup they are lost, and the tip while sharp, is smooth.It is interesting to note that in these birds as in the piculets thetail is soft without spiny shafts, which is misleading from a taxo-nomic standpoint, and that thus in both of these groups the tongueis a better guide to relationship.Furthermore the Dendrocolaptinae possess stiff spiny tails whichwould mislead one in the conclusion that they are allied to wood-peckers when no relationship exists; whereas, in spite of the fact
art., 19 CONCERNING BIRDS ' TONGUES GARDNER 23that feeding habits are similar to the latter, the tongues are whollyunlike and therefore yield more reliable evidence.In this family the tongue fulfils all the requirements for taxonomicuse in that differences in feeding habits in related forms hare notaltered the fundamental pattern in the group, so that the tonguealone is sufficient in all instances to refer its owner to the familyand in many instances to the correct subfamily and even genus.Conversely, similar feeding habits in unrelated forms (Dendro-colaptinae) have not produced tongues like these, and this is the morestriking since the tail, in response to such habits, has taken on thespiny character so common to that of woodpeckers.Order PASSERIFORMESIn this heterogeneous group where so much variability is foundin all of the anatomy it is not surprising to find the tongue takingpart in this diversity in form. A brief survey of this has alreadybeen given in an earlier part of this paper; it remains to classifyand group such differences.In many families the thin horny tongue, slightly curled andfrayed at the tip, as described for the robin, is found with but slightdifferences in length and width. Such a tongue has no outstandingcharacter sufficient to identify the particular family to which itbelongs and serves to do no more than to indicate a member of theorder. As example Pitta erythrogaster (fig. 90) is illustrative.The flycatchers (Tyrannidae) have tongues which are often broad-ened at the middle, somewhat curled, incised at the tip and oftenslightly frayed. As examples, are Myiochanes richardsoni (fig. 91),Pyrocephalus rubinus mexicanus (fig. 92), Sayomis sayus (fig. 93),and S. nigricans (fig. 94), NuttaUornis borealis (fig. 95), Empi-donax griseus (fig. 96), Tyrannus verticalis (fig. 97), and Tol-marchus gabbi (fig. 98). The tongue of Chdicivora stenura is verysimilar to these forms as is that of Muscisaxicola maculirostris. Seefigure 99 which illustrates Myiarchus dominicensis.There is nothing remarkable about the organ in Pachyramphusviridis viridis.The South American bell bird, Chasniorhinchus, has a rathersimple flat tongue that is slaty black, matching the gape in color.The postero-lateral branches are long armed with slender spineswhile the tip is slightly incised and the whole organ is comparativelysmall in relation to the size of the mouth.The Dendrocolaptidae are interesting in that the feeding habitsof many of them are similar to woodpeckers without developingtongues like the latter. In most of these the anterior two-thirdsor more of the tongue is thin, horny, and translucent, and somewhat
24 PROCEEDINGS OF THE NATIONAL MUSEUM vol.67frayed, while the whole organ is of good length in proportion tothe length of the bill. This is true of Dendrocolaptes picunvnusand several species of Picolaptes. But one specimen of Drymomisbridgesi was available and in an excellent state of preservation.In this bird the tongue was exceptionally small, out of all proportionto the huge sickle bill and not at all like the above-mentioned genera.The appearance was much as if the horny anterior end of the tonguewas either absent or had been shed. Whether this is an accidentalor natural state is not known. Figure 100 illustrates the tongue ofFurnarms agnatm, which is somewhat fleshier than ordinary and isnot supplied with so great a proportion of horny tip. This is truealso of Cinclodes. Figure 101 illustrates JSittasomus, species. ( ?
)
The Formicariidae have thin horny tongues that are frayed some-what more than the ordinary, extending well back along the sides,as exemplified by that of Gymnocichla nudiceps (fig. 102). Tham-nophilus bridgesi (fig. 103) shows much the same structure.Figure 104 illustrates the tongue of Oligura superciliaris, one ofthe Timaliidae.Among the Pycnonotidae, Pycnonotus shows a simple flat tonguethat is bifid but not frayed, while lole philippinensis has one some-what curled and both forked and frayed at the tip.There is little to characterize the Muscicapidae, as the tongues seenare with minor variations much like the standard pattern.The thrushes and their allies depart from the usual structure bythe addition of papillosities on the dorsal surface of the tonguearound the basal portion. This is exemplified by Hylocichla guttata(fig. 106), Myadestes townsendi (fig. 105), Mimus polyglottos leu-copterus (fig. 107), and Sialia mexicana (fig. 108).Polioptila caerulea obscura (fig. 116) does not have this arrange-ment, but is supplied with only a single posterior row while the tipis considerably frayed.Ginclus mexicanus (fig. 110), of the family Cinclidae, has a simplerather fleshy tongue slightly curled and frayed.The wrens, Troglodytidae, are marked by very thin, horny, trans-lucent, long tongues through which the contained bones are plainlyvisible. The posterior spines are prominent and needlelike, whilethe main postero-lateral projections consist of prominent roundedhorny spines; an apperance that is quite characteristic, and is notlacking even in that nonwrenlike form Heleodytes hnmneicapilluscouesi. Figures 112 and 111 represent this organ as seen in Catherpesmexicanus punctulatus and Thryomanes bewicki charienturus, re-spectively.Chamaea jasciata has a trough-shaped square-tipped tongue wellsupplied with entangling hairlike processes very suggestive of that
art. 19 CONCERNING BIRDS' TONGUES?GARDNER 25
seen in the nuthatches. The tract between the base of the tongueand the glottis has many pores of mucous glands.Swallows have a simple flat tongue somewhat split at the tip, asillustrated by Petrochelidon hmifrons (fig. 115), and very similarin appearance to Collocalia (fig. 85, after Lucas).The ''cuckoo-shrikes'' (Campephagidae) have tongues of thestandard pattern, with perhaps more fraying than usual. At leastthis is true of P&ricrocotus exsul and Malindangia macgregori.Lalage niger shows very fine lateral fraying, while Graucalus hasmuch the same appearence, the tongue, however, not matching insize the large bill.In the drongos (Dicruridae) this fraying becomes in some formsvery elaborate. Thus, in GMbia Tiottentotta, the tongue is deeplysplit and the sides are incised, forming long, delicate, forward-pointing hairlike fringes, the delicate strands of which are veryuniform in size and length. This is only slightly less marked inDicrurus longicaudatus while in Bhringa remifer the processes arevery short and delicate. Dissemurus paradiseus is much the same,while Bhuchanga Tonga has considerably less fraying.Some of the Bombycillidae have simple flat tongues (Bombycilla),in appearence much like those of swallows, while Dulus dominicus(fig. 117) has a much curled tip, which is frayed.The shrikes are an ill-defined group, Laniidae. There is littlecharacteristic about the tongue. That of Strepera graculina is il-lustrated in figure 133, while Lanius ludovicianus gambelii is illus-trated in figure 114.The vireos have simple flat tongues, as represented in figure 11!?.Yiico. species from Tortuga Island. Lawrencia nana (fig. 118), andby figure 120, Vireo belli pusillus.The Sittidae as well as the Paridae have impaling organs throughthe ends of which the cartilaginous tips of the cer.atob.yals oftenproject. This is illustrated in figure 121, Sitta carolinesis aculeata,and figure 122, Sitta pygmaea. The titmice and chickadees havefour-pronged tongues. See figure 124, Baeolophus inornatus, andfigure 123, Penthestes gambeli baileyae.The verdin, Auriparus flaviceps (fig. 12G), and the bush-tit.PsaltHparus minimus californicus (fig. 125), have very irregularlacerated tips, while Certhia familiaris zelotes (fig. 113) is not farremoved.The Corvidae have a tongue the anterior third of which is com-posed of thin, translucent, horny tissue which is often rather deeplyincised and is whipped out. The main postero-lateral spines arebifid or double, while over the surface around this region there aremany small papillosities. As examples are Aphelocoma californica(fig. 128), Cyanocitta stelleri frontalis (fig. 130). Nucifraga colum-43316?25 4
26 PROCEEDINGS OF THE NATIONAL MUSEUM vol.67biana (fig. 132), and Pica nuttalli (fig. 1'29). The entire appearanceis very characteristic.The tongues of some of the Sturnidae are of the standard patternas exemplified by Scissirostrum dubium (fig. 131), while Lmnproco-rax chalybea and L. metallicus are very similar.The tongues of the next six families are some of the most elaborateand marvelous throughout the Class of Birds.The Dicaeidae have small tongues that are flat posteriorly but atabout the middle become abruptly narrower and begin to curl intoa semitube which is deeply cleft at the tip, the margins of whichare smooth, forming two slender semitubular tips. This is found inDioaeum cruentatum, D. sarigumolentum, D. fiam??ieum, and D. cele-bkum. In Acmonorhynchus aureolimbaius the same holds true ex-cept that the edges of each tube show a slight notching, with an at-tempt at the production of four tips, while in Prionochilus thesenotches have deepened to actual splitting with the formation offour semitubular fringeless projections.The tongue of Dicaeum trigonostlgma as figured by Gadow 12
-hows a complete tubular arrangement by overlapping of the up-curled edges, which are not frayed. The tip is deeply bifurcated,forming two equal tubes, and the tip of each one of these again iscleft, forming a quadruple tongue.The Zosteropidae.?As to this family some are simple in struc-ture, being rather flat with only a slight tendency to curling,while the tip is deeply slit. Gadow 13 finds this true of Z. simplex.Z. atrifrons (fig. 135) shows some fraying of the margins, whichis true also of Z. sarasinorum. This may be carried to the pointwhere, with curling added to the process, elaborate curled split andfimbriated tongues are found as described of Z. simplex and Z.juponica by Beddard.11The Nectariniidae.?In this family curling is the outstandingfeature, so that the anterior one-half to two-thirds is a completelylolled tube the upcurled margins of which are overlapped and arenot fringed or frayed. In some species there is some forking at thetip to form two tubular projections.Arachnechthra asiatica has a very long tube for the anterior two-thirds, without splitting or fraying. Arachnothera, species ( '?) has avery long tube slightly frayed at the tip. Ginnyris {Cyrtostomus)pectoralis and G. jugularis woodi have slender tubes, both somewhatforked at the tip. Hermotimia, species (?) (fig. 141) shows the samearrangement.
3 Gadow, II. Structure of Certain Hawaiian Birds. The Birds of the SandwichIslands, Wilson and Evans, London, 1890-99, pp. 219-241.Gadow, H. L'roc. Zool. Soc, London, 1883, p. G3." Beddard, F. E. Ibis, .ser. 6, No. 3, 1891, pp. 510-512.
art. 19 CONCERNING BIRDS' TONGUES GARDNER 27Gyanomitra vertiealis lias a long slender tongue, longer than thebill, completely tubular, and .somewhat forked, and this is true alsofor Chalcomitra fuliginosa and Aethopyga boltoni. In Anthreptesfraseri, malaccensis, and wiglesicorthi, the bifurcation is moremarked than in any of the others, so that practically a doubletongue is formed.On the other hand the tongue of Clialcoparia phoenicotis (fig. 139)is not at all like the above, and this fact together with other evi-dence has led Oates 15 to separate this species from the family. Inview of the fact that there is such a regularity of tongue form inthis family the divergence from it as seen in Ghalcoparia may wellhave the significance that Oates gives it.The Drepanididae typically have tubular tongues. These areformed as are all tubular ones by an upcurling of the margins ofthe horny anterior part which constitutes the major portion of thetongue in these birds. The edges of the dorsally rolled sides meet inthe midline and finally overlap. As the tip is approached the edgesbecome broken up and split, forming delicate laciniae. At first oneside completely overlaps the other but as these fimbriations becomemore prominent they interlace in a complex manner finally formingat the tip a whipped-out brush.This is the fully developed tongue and is well illustrated in thelong-billed Hemignathus procerus (fig. 19). This same appearanceis seen also in Vestiaria coccinea, Glxlorodrepanis, and Himationesanguined, all of these, however, being shorter than the above. InHeterorhynchus wilsoni it is completely tubular only in the anteriorthird and is bifurcated.Loxioides bailleui, which Doctor Gadow 16 first classed among theFringillidae, is described by him as follows. The tongue isThick and fleshy, much shorter than the bill, very slightly protractile,tip rounded off and ending- in a neat horny scoop, which is formed by thelower horny covering of the tongue projecting a little ; the brim of this scoopis slightly frayed out, as is the case in many Fringillidae.Oreomyza {Oreomystis) bairdi he describes as:A little shorter than the bill, thin and horny but at first sight apparentlydifferent from that of the Drepanid'dae. However, the lateral horny marginsare raised up dorsally and frayed out. The distal fourth of the tongue isslightly split into a right and left half but far less than in Coereba. Thisbroader, shorter, and decidedly less tubular tongue is in conformity with theslightly broader bill.Loxops coccinea he describes as " short, in conformity with thebill, but ending in a frayed-out single brush, which, like the whole
15 Fauna of British India. K. W. Oates. Birds, vol. 2, p. 372.16 Gadow, II. Structures of Certain Hawaiian Birds. The Birds of the SandwichIslands, Wilson and Brans, London, 1890-99. pp. 219-241.
28 PROCEEDINGS OF THE NATIONAL MUSEUM vol. 67
organ, is formed exactly like that of the other Drepanididae." Thetongue of Hcmignathus olivaeeus is "short and less tubular, beingintermediate in structure and appearance between those of Hhn-atione and Yestiaria.Psittirostra psittacea (fig. 140) has a flat, fleshy tongue in whichthe long, horny curled portion is absent. The tip is blunt and notfrayed. The appearance is almost exactly as if the tubular portionof the tongue of Hemignathus procems had been cut away leavingthe basal uncurled portion.An entirely different arrangement is seen in the finchlike Tele-spyza cantans, however (fig. 136). Here the entire tongue is thickand fleshy, much as in some of the finches (compare Passerculusrostratus, fig. 137), with an uprolling of the thick margins to forma fleshy rolled tubular tongue not at all the same in appearance orarrangement as the tubular tongues of the foregoing forms, madeup, as they are, by a prolongation and curling of the natural thinhorny tip of the standard tongue.It is apparent, therefore, that in this family there is a wide rangein tongue forms, from which no reliable evidence as to relationshipis to be drawn, as is evidenced by the error made by Doctor Gadowin the case of Loxioides.The Coerebidae have tongues that are curled, split, and frayed,but not all to the same degree, and a fine series of modificationscan be traced through this family. Thus in Glossoptila (Eimeorvis)campestris the tongue is practically flat in the posterior two-thirds.The anterior third shows a moderate upcurling of the lateral mar-gins, with delicate fraying into a fringe that rolls inward but doesnot meet the opposite side. The tip is bifid, thus converting thisportion into two very imperfect semitubular fringed projections.Oyanerpes cyanea (fig. 138) has the anterior one-half curled in muchthe same manner, while the tip may or may not be bifurcated.Cyanerpes lucidus shows very little fraying of the margins ofthe tube, while C. caeruleus is deeply cleft and frayed. In Chloro-phanes spisa (fig. 4) the tube is becoming more perfect by a closeapproximation of the upcurled edges. Finally in Goereba bana-nivora (fig. 5) the edges completely overlap, forming a true tubewhich by splitting becomes double tubes, the curling margins ofwhich are much frayed. This same appearance is seen in Coerebaportoricensis and Diglossa plumbea, the latter of which shows asurprisingly long tongue in comparison to the short bill.The Meliphagidae have elongate quadruple tongues. The curledtongue first splits into a right and loft half with marked frayingof the edges, forming two fringed tubes, and these are againdeeply split and frayed, so that four elaborately frayed brushy tipsare formed. The whole organ is as long or longer than the bill.
aet,19 CONCERNING BIRDS' TONGUES GARDNER 29The appearance is illustrated by Myzomela rubratra (fig. 6), andthe same appearance is seen in M. nigriventris and M. sanguinolenta.Whether the bird and tongue be a large one, as Tropidorhynchusand Microphilemon, or of moderate size, as Meliphaga (Ptilotis)carunculata, there is a surprising conformity to the pattern de-scribed. This same long quadruple tongue is present also in Meli-ornis australasiana, Acanthorhynchus tenuirostris, Myzantha gar-rula, and Acrulocercus braccatus.So far as is known this extraordinary quadruple brushy tongueis limited to and characteristic of this family. It is an interestingfact that the formation of the multiple tubular and brushed tonguesof these several families of flower-frequenting birds follows differentlines of development using one or more of the fundamental tendenciesof the type tongue to curl, split, and fray. Thus, as has been demon-strated, the Nectariniidae have almost purely tubular tongues, theDrepanididae tubular tongues with frayed margins, the Coerebidaecombine curling, splitting, and fraying, to form double tubes, whilethe Meliphagidae carry this to the degree that four curled brushytips are formed.Among the Mniotiltidae there is a rather wide range of variation.As is the case with the type pattern these are tipped with horny thintranslucent tissue which may form nearly one-half of the organ(see fig. 142, Dendroica dominica) or may be absent, which was thecase in a second specimen of the same species and is also illustratedby Vermivora celata lutescens (fig. 143) and Dendroica petechiagundlachi (fig. 144). The tongue may be a thin, flat structure as inCatharopeza bishopi (fig. 145), Dendroica occidentalis (fig. 146),and Dendroica palmarum (fig. 147), or curled at the tip as in Grana-tellus francescae (fig. 148), by upcurling of the fraying margins aprocess which is carried to its greatest extreme in this family byDendroica tigrlna (fig. 2). There may be rather marked differencesin shape as is evidenced by a tongue of Wilsonia canadensis (fig.149), which is very broad at the middle, while others from the samespecies showed this to a lesser degree or not at all. Certhidea sdlvini(fig. 150) has a rather thick fleshy tongue, grooved shallowly andrather suggestive of the fringilline type.There is thus in this group considerable variation even in such asmall series as in the one genus Dendroica, as may be observed bythe following figures: D. nigrescens (fig. 151), D. auduboni (fig.152), D. vigorsii (fig. 153), D. discolor (fig. 154), D. petechia (fig.155), D. striata (fig. 156), D. castanea (fig. 157), D. fusca (fig. 158),and D. virens (fig. 159). Other members of this family are Teretis-tris fe?mandinae (fig. 160), T. fornsi (fig. 161), Wilsonia citrina (fig.162), Wilsonia pileolata pileolata (fig. 163), Vermivora luciae (fig.164), Gompsothlypis americana (fig. 165), Oporomis toVmiei (fig.
30 PROCEEDINGS OE THE NATIONAL MUSEUM vol.67166), Helmitherus vermivorus (fig. 169), Icteria virens (fig. 168),and Oreothlypis gutturalis (fig. 167).Family Tanagridae.?In some of this group the tongue is flat andthin, as in Tachyphonus (fig. 170) and in Tanngra (Euphonia)violacea (fig. 171). In others it is fleshy, as in Thraupis darwini(fig. 172), Stephanophorus leucocephalus (fig. 173), and Rampho-celus brasilius (fig. 174), while in the very large billed Pitylusgrossus (fig. 175) the tongue is cylindrical and fleshy while theanterior half is hollowed out and scoop-shaped, very suggestive ofsome of the finches. Phaenicophilus poliocephalus has a longertongue (fig. 177), which is considerably frayed at the tip.The Ploceidae have a structure very similar to the finches, with acylindrical fleshy tongue having a depression anteriorly to forma scoop. This is illustrated by Munia punctulata (fig. 178). Thehorny under surface is often folded over the dorsum to form agrooved tongue as in some of the finches and as is illustrated bySteganura paradisea (fig. 179). This is seen also in Ploceus megar-hynchus, P. bengalensis, and a species of Foudla from St. HelenaIsland.The Icteridae, as typified by Icterus cucullatus nelsoni (fig. 180),and Icterus icterus (fig. 3), have upcurled frayed margins to thetongue which may be deeply split to form double frayed semitubu-lar tips. This is found also in /. parisorum, I. wagleri, I. bullocki,I. mesomslas, and /. north ropL all of which have tongues very sug-gestive of the Coerebidae with less advanced degrees of curling.The blackbirds, as exemplified by Molothrus atronitens (fig. 181 ) 7have upcurled margins without fraying, forming a guttered organwith the tip somewhat whipped out. This is seen in Agelaiusphoeniceus, A. tricolor, Molothrus ater, and Dolichonyx orysivorus.Gymnostinops montezumae has little curling; the tip is bifurcatedand frayed, while Megaquiscalus major macrourus has a bifidcurled and much frayed organ, much like Icterus. Pseudoleistes(fig. 182) has a thin tongue somewhat curled and whipped out atthe tip.The Fringillidae have cylindrical fleshy tongues, which showmuch variation. Ordinarily the horny under surface projects beyondthe tip, and this is often frayed and somewhat curled so that a smallscoop-shaped end is formed. This same horny under surface investsthe lateral margins of the tongue and often curls over the dorsal sur-face as indicated in Loxia leucoptera (fig. 185). The tongue mayhave long posterior branches as in the odd form assumed by Passerdomesticus (fig. 183), or, as is usually the case, they are closely com-pressed to the basihyal portion. It may have simply a flat surface,as indicated in Oberholseria chlorura (fig. 186), or there may be adeep groove formed as in Zamelodia melanocephida (fig. 191). In
aut.19 CONCERNING BIRDS ' TONGUES GARDNER 31the genus Passerculus the grooving is very marked so that in someof the species a rolled or tubular tongue is formed (see fig. 137 Pas-serculus rostratus)
.
In conclusion it is obvious that the tongues of birds subservemany different uses, a wide range of function that is paralleled bychanges in form, ranging from simple rudimentary nodules of fleshto the highly complex multiple tongues of the flower-frequentingbirds. Furthermore, when classified as to adaptations, eight naturalgroups are formed, to which many of these differing patterns maybe assigned.The type pattern of tongue is composed of a fleshy basal partwhich is tipped with a more or less extensive thin horny translucentanterior portion, which has an inherent tendency to curl, bifurcate,and fray laterally. One or all of these tendencies are utilized toproduce many adaptive modifications, a fine series of which may betraced through the flower-frequenting birds, where they undergothe greatest development, producing elaborate and complex tubular,brushy, and multiple tongues.Fundamentally the tongue is a paired structure arising, as itdoes, from the second and third visceral arches, and upon this founda-tion must be constructed all the variations seen. Practically, how-ever, in the fully developed organ the alterations have become sogreat, through fusion of some parts and suppression or exaggerationof others, that it is not possible to select a fundamental pattern fromwhich all others may be derived, but, instead, many of these must berecognized.With regard to the taxonomic value of this organ in birds the evi-dence is conflicting. Much of it tends to support the conclusionthat it is of little or no value, since, either from similarity of dietor' due to convergent evolution, appearances of affinity are formedwhere no true relationship exists. Furthermore, differences in struc-ture are seen in closely allied birds where presumably the diet is thesame.On the other hand, in many families, in spite of changes in re-sponse to diet a uniform and characteristic pattern is traceablewhich gives definite indications of affinity and provides valuabletaxonomic features. Among the groups in which this is true are theArdeidae, Phoenicopteridae, Anatidae, Picidae, Trichoglossidae,Buteonidae, Falconidae, Trochilidae, and possibly the Meliphagidae,Bucconidae, Ramphastidae, Corvidae, and Nectariniidae. To thesewith more study, others may be added.
BIBLIOGRAPHYBaikd, S. F.1864, November. Review of American Birds, pp. 161-2.Bath, W.1906. Die Geschmacksorgane der Vogel and Krokodile. Arch. Brontologie,vol. 1, pp. 1-47.Beddakd, F. E.1891. On the Tongue of Zosterops, Ibis, ser. 6, no. 3, p. 510.1898. Note on the tongue of Podargus. Structure and Classification ofBirds, p. 234.1903. On the Modifications of Structure in the Syrinx of the Accipitres,with Remarks Upon Other Points in the Anatomy of That Group.Proc. Zool. Soc. London, 1903, vol. 2, pp. 157-163.1903. A Note Upon the Tongue and Windpipe of the American Vultures,with Remarks on the Interrelation of the Genera Sarcorhamphus,Gypagus and Cathartes. Proc. Zool. Soc. London, 1903, vol. 2,pp. 386-392.BOTEZAT E.1910. Morphologie, Physiologie und Phylogenetische Bedeutung der Gesch-macksorgane der Vogel. Anatomischer Anzeiger, vol. 36, pp. 42S-461.Chaine, M. J.1904. Remarques Sur La Musculature de la Langue des Oiseaux, ComptesRendus de la Societe de Biologie, Paris, vol. 56, pp. 991-2.1905. La Langue des Oiseaux, Bull. Scient. de la France et de la Belgique,vol. 39, pp. 487-504.Evans, A. H.1899. Birds. Cambridge Natural History. Macmillan & Co.Gadow, H.1883. On the Suctorial Apparatus of the Tenuirostres. Proc. Zool. Soc.London, 1883, pp. 62-69.1890-99. Structure of Certain Hawaiian Birds. The Birds of the Sand-wich Islands. Wilson and Evans, London, pp. 219-241.Garrod, A. H.1873. Tongue of Steatornis caripensis. Proc. Zool. Soc, London, p. 531.Giebel, C.1858. Die Zunge der Vogel und ihr Geriist, Zeitschrift fur die GesammtenNaturwissenschaften, vol. 11, pp. 19-53.1862. Zur Anatomie der Papageien. Zeitschr. fur die Ges. Naturw., vol.19, pp. 133-152.Kallius, E.1905. Beitrage zur Entwickelung der Zunge Anas boschas L. Passerdomesticus L., Anat. Hefte, vol. 28, pt. 2. Vogel, pp. 311-586.Liebeb, Adolph.1907. Vergleichende Anatomie der Spechtzunge. Zoologica, vol. 20, pt. 51,.Stuttgart '07.32
abt\19 CONCERNING BIRDS ' TONGUES GARDNER 33Lindahl, Joshua.1879. Some New Points in the Construction of the Tongues of Wood-peckers. Amer. Naturalist, vol. 13, p. 43^14.Lucas, F. A.1896. The Taxonomic Value of the Tongue in Birds. The Auk, vol. 13,No. 2, April, 1896, pp. 109-115.The Tongues of Woodpeckers, Bulletin No. 7, U. S. Dept. of Agric,Division of Ornithology and Mammalogy.1897. The Tongues of Birds. Report of U. S. National Museum, 1895, pp.1003-1020.MacGhxivray, William.1839. Note on tongue of Setochalcis vocifera. In Audubon, J. J., Ornitho-logical Biography, Edinburgh, 1839, vol. 5, p. 306.1839. Description of tongue of Antrostomus carollnensis. Audubon, J. J.,Ornithological Biography, Edinburgh, 1S39, vol. 5, pp. 402^103.1839. Tongue of Chordciles virginianus. Same reference, p. 407.1840. Tongue of Caprimulgus europaeus. History of British Birds, Lon-don, vol. 3, pp. 630 and 634.Marshall, M. E.1905. Note on the Tongue of Phalaenoptilus. Proc. Amer. Philos. Soc,vol. 44, p. 215.Mudge, G. P.1901. Lingual Myology of Parrots. Proc. Zool. Soc. London, vol. 1, p.277-8.Oates, E. W.Tongue of Chalcoparia. Fauna of British India. Birds, vol. 2, p. 372.Wallace, A. R.1870. Note on the tongue of Chalcoparia, Ibis, p. 49.Wetmore, Alexander.1918. On the Anatomy of Nyctibius with Notes on Allied Birds. Proc.U. S. National Museum, vol. 54, pp. 577-586.
EXPLANATION OF FIGURES ILLUSTRATING BIRD TONGUESPlate 1No. 1. Planesticus migratorius.2. Dendroica tigrina.3. Icterus icterus.4. Chlorophanes spiza.5. Coereba bananivora.6. Myzomela rubratra.34
U. S. NATIONAL MUSEUM PROCEEDINGS, VOL. 67, ART. 19 PL. Ipv J
Wfi
, v V
Series Illustrating Multiple Tubular Tongues, Modifications of aGeneralized Type Pattern. (X3)For explanation of plate see page 5
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TONGUES ADAPTIVELY MODIFIED FOR AN OMNIVOROUS DIET, FlSH FARE,RAPTORIAL FEEDING, OR FOOD STRAINED FROM WATER. iNO II ONE-HALF Natural Size, Others x3)For explanation of plate see page 8
Plate 2
.No. 7. Callipepla squamata.8. Pufflnus griseus.9. Querquedula cyanoptera.10. Mergus serrator.11. Phoenicopterus ruber.12. Bnteo lineatus elegans. 35
Plate 3No. 13. Xenopicus aloolarvatus.14. Colaptes cafer collaris.15. Melanerpes formicivorus bairdii.16. Sphyrapicus thyroideus.17. Conurus auricapillus.18. Carpodacus cassini.19. Hemignathus procerus.20. Anhinga anhinga.21. Pyrotrogon neglectus.36
U. S. NATIONAL MUSEUM PROCEEDINGS, VOL. 67, ART. 19 PL. 3
r
Spearing Tongues, Tongues of Seed and Fruit Feeders, FlowerFrequenters, and rudimentary Types. (X3jFor explanation of plate see page 9
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Tongues of Various Water Birds (X2)For explanation of plate see page II
Plate 4No. 22. Gavia pacifica.23. Gavia itnmer.24. Colymbus nigricollis californicus.25. Fuhnarus glacialis glupischa.26. Ciconia ciconia.27. Larus heermanni.28. Larus occidentalis.29. Erismatura jamaicensis.30. Gallinula galeata. 37
Plate 5No. 31. Nycticorax naevius.32. Ardea herodias.33. Botaurus lentiginosus.34. Butorides virescens anthonyi.35. Cereopsis novaehollandiae.38
U. S. NATIONAL MUSEUM PROCEEDINGS, VOL. 67, ART. 19 PL. 5
31
34Tongues of Various Birds. (No. 35 Natural Size. Others X2)For explanation of fE SEE PAGE 13
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Tongues of Various Birds. (No. 42 2, Others X3)For explanation of plate see page 15
Plate 6No. 36. Gypaetus barbatus.37. Buteo borealis calurus.38. Cathartes aura septentrionalis.39. Falco sparverius phalaena.40. Circus hudsonius.41. Polyborus plancus.42. Buteo albicaudatus.43. Accipiter cooperi.44. Surnia ulula.45. Opisthocomus cristatus.201. Chrysolophus pictus. 39
Plate 7No. 46. Heteroscelus incanus.47. Rallus levipes.48. Limnodromus griseus scolopaccus.49. Aramus vociferus.50. Recurvirostra amerwana.51. Rynchops nigra.52. Eurypyga helias.53. Fulica americana.40
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46
*?*A
k A
49
Tongues of Gruiformes and Charadriiformes (Nos. 49 and 52 x 2,Others 3)For explanation op plate sfe page 16
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56
TONGUES OF VARIOUS BIRDS. <NCS. 59 AND 61 X 2, OTHERS X3>For explanation of plate see page 17
Plate 8
.No. 54. Actitis macularia.55. Sterna antillarum.56. Sterna forsteri.57. Ereunetes pusillus.58. Oxyechus vociferus.59. Ionornls martinica.60. Charadrius semipalmatus.61. Haematopus palHatus.62. Colinus virginianus cubensvs.63. Histriophaps histrionica.64. Geopelia cuneata.65. Zenaida vinaeeornfa
.
66. Columba gymnopJithalma. 41
Plate 9No. 67. Geococcyx californianus.68. Geococcyx californianus. (to show differences in length).69. Saurothcra dominicensis.70. Psitteuteles chlorolepidota.71. Aprosmictus cyanopygius.72. Melopsittacus undulatus.73. Calopsitta novaehollandioe.74. Todus multicolor.75. Ceryle alcyon.76. Speotyto cunicularia Jiypugaea.77. Asio wilsonianus.42
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Tongues of Various Birds. (X3)For explanation of plate see page l?
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Tongues of Caprimulgi. (X3)For explanation of plate see page 19
Plate 10No. 78. Tyto pratincola.79. Otus asio bendirei.80. Spiloglaux novaezealandiae.81. Chordeiles acutipennis texensis.82. Macropteryx coronata.83. Bucco Mcinctus.84. Lophoceros melanoleucus.85. Collocalia, sp (from Lucas).86. Calypte anna.87. Pteroglossus frantzii.88. Dryobates villosus hyloscopus.89. Dryobates nuttalli. 43
Plate 11No. 90. Pitta erythrogaster.91. Myiochanes richardsoni.92. Pyrocephalus rubinus mexicanus.93. Sayornis sayus.94. Sayornis nigricans.95. Nuttallornis borealis.96. Empidonax griseus.97. Tyrannus verticalis.98. Tohnarchus gabbi.99. Myiarchus dominicensfe.100. Furnarius agnatus.101. Sittasomus, sp.102. Gymnocichla nudiceps.103. Thamnophilus bridgesi.104. Oligura superciliaris.105. Myadestes townsendii.106. Hylocichla guttata.107. Mimus polyglottos leucoptcrus.44
U. S. NATIONAL MUSEUM PROCEEDINGS. VOL. 67, ART. 19 PL. II
104
Tongues of Passeriformes. (X3)For explanation of plate see page 23
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Tongues of Passeriformes. (X3)For explanation of plate see page 25
Plate 12No. 10S. Sialia mexicana.109. Toxostoma redivivum pasadenense.110. Cinclus mexicanus.111. Thryomanes bewtcki charienturus.112. Catherpes mexicanus punctulatus.113. Certhia familiaris selotes.114. Lanius ludovioianus gambeli.115. Petrochelidon lunifrons.116. Polioptila caerulea obscura117. Dulus dominions.119. Fireo, sp.118. Lawrencia nana.120. Ftreo 6eHi pusillus.121. &??fa carolinensis aculeata.122. &i??a pygmaea.123. Penthestes gambeli baileyae.124. Baeolophus inornatus.125. Psaltriparus minimus californicus.126. Auriparus flaviceps.127. Xanthoura luxuosa (apparently injured).128. Aphelocoma califomica. 45
Pf.ATE 13No. 129. Pica nuttalli.130. Cyanocitta stelleri frontalis.131. Scissirostrum dubium.132. Nucifraga Columbiana.133. Strepera graculina.134. Stumella neglecta.135. Zosterops atrifrons.136. Telespysa cantans.137. Passerculus rostratus.138. Cyanerpes cyanea.139. Chalcoparia phoenicotis.140. Psittarostra psittacea.141. Hermotimia, sp.46
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Tongues of Passeriformes. (No. 133 2, Others x3For explanation of plate see page 26
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147
Tongues of Passeriformes. (X3)For explanation of plate see page 29
I 'I,ATE 14No. 142. Dendroica dominicia.143. Vermivora celata lutescens.144. Dendroica petechia gundlachi.145. Catharopeza bishopi.146. Dendroica occidentalis.147. Dendroica palmarum.148. Granatellus franciscae.149. WiZsonia canadensis.150. Certhidea salvini.151. Dendroica nigrescens.152. Dendroica auduboni.153. Dendroica vigorsii.154. Dendroica discolor.155. Dendroica petechia.156. Dendroica striata.157. Dendroica castanea.158. Dendroica fusca.159. Dendrmca virens.160. Teretistris fernandinae.161. Teretistris fornsi.162. WiZstmia citrina.163. TPiZscmia p. pileolata.164. Vermivora luciae.165. Compsothlypis americana.166. Oporornis tolmiei.167. Oreothlypis gutturalis.168. Icteria virens.169. Helmitherus vermivorus.170. Tachyphonus, sp. 47
Plate 15No. 171. Tanagra (EupJionia) violacea.172. Thraupis darwini.173. Stephanophorus leucocephalus.174. Ramphocelus brasilius.175. Pitylus yrossus.176. Tanagra, sp.177. Phaenicophilus poliocephalus.178. Munia punctulata.179. Steganura- paradisea.180. Icterus cucullatus nelsoni.181. Molothrus atronitens.182. Pseudoleistes, sp.183. Passer domesticus.184. Tiaris olivacea.185. Loxia leucoptera.186. Oberholseria chlorura.187. Ammodramus savannarum bimaculatus.188. Spinus pinus.189. Passerculus savannarum alaudinus.190. Oryzborus, sp.191. Zamelodia melanocephala.48
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190 VTongues of Passeriformes. (X3)For explanation of plate see page 30
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Tongues of Passeriformes. (X3)For explanation of plate see page 30
Plate 16No. 192. Pipilo aberti.193. Chondestes grammacus strigatus.194. Passerculus beldingi.195. Amphispisa belli.196. Spizella passerina arisonae.197. Passerella iliaca stephensi.198. Junco hyemalis thurberi.199. Passerella iliaca.200. Pipilo crissalis senicula.43316?25 4 49o