Table 4.Lengths of Leg Bones in cm.
Table 5.Leg-trunk Ratios (in percent)
Table 6.Leg-trunk Ratios (in percent)
Table 7.Actual Length and Width in mm. of Pygostyle and Proportionate Length and Width of Pygostyle in percent of Lacrimal Length
Table 8.Length of Sternum and Depth of Carina expressed as percentages of the Length of the Trunk
Table 9.Skull and Sternum, Length and Width in mm.
The length of the trunk was taken as the distance from the anterior tip of the neural crest of the last cervical vertebra to the anterior edge of an acetabulum. The number of free thoracic vertebra was five in each specimen; consequently, there was no error from this source. In the cranium, a measurement was taken from the anterior edge of the lacrimal bone to the posteriormost end of the cranium, and the resultant figure was employed for a constant in cases in which small bones were compared.
Table 10.Relative Length and Width of Skull (in percent)
skeleton of Bombycilla cedrorumFig.43. Part of skeleton ofBombycilla cedrorumshowing method of measuring the length of the trunk. Natural size.
Leg-trunk Percentages.—Table 4shows the relative lengths of the legs and of the separate bones in the legs of the different species of the Bombycillids.Table 5shows corresponding lengths for other passerine birds. The total length of the leg was computed by adding the figures obtained for the lengths of the femur, tibiotarsus andtarsometatarsus. The lengths of the toes were disregarded. Length of leg was recorded in this same way by Richardson (1942:333), who thought that only in swimming and running birds do the toes contribute to the functional length of the hind limb.
Table 4shows that of the birds compared in this paper,Dulushas the longest legs. In order of decreasing length the others are the Ptilogonatinae, and finally the Bombycillinae, which have the shortest legs of all. In Waxwings the length of the legs, expressed as percentages of the body-lengths, are identical with those birds that are similar in habits, that is to say, birds which do not use the hind limb except in perching. It can be noted by reference toTable 5thatTachycinetaandMyadestesfall into this category. This shortness of limb is obviously adaptive, and each of the segments of the limb has been correspondingly shortened, with no element reduced at the expense of the other two. The short leg can be more easily folded against the body while the bird is in flight, than can a long leg which is more unwieldy. It may be noted from tables 4 and 5 that birds which spend much time on the ground, or that hop a great deal in the underbrush, have longer legs than do birds which spend much time in flight. Two birds with noticeably long legs areHylocichla mustelina, a typical ground dweller, andParus atricapillus, which hops about in the trees and underbrush.
Insofar as the lengths of the legs show,DulusandPhainoptilaare the most generalized of the Bombycillidae, since the relative length of leg is approximately the same as that of more generalized birds such as warblers, crows and thrushes of similar locomotory habits. In other words,DulusandPhainoptilahave remained unspecialized, in contrast to the waxwings in which adaptive changes fitting them for a perching habit have taken place.PtilogonysandPhainopeplaare intermediate in length of leg betweenPhainoptilaandBombycilla, andPtilogonysandPhainopeplahave progressed from life on the ground toward the perching habit.Bombycilla cedrorumis more specialized than isB. garrulain shortness of leg, and the reduction is comparable, as is noted above, to that in the legs ofTachycineta.
In birds which have the legs much modified for walking or for hopping in the brush, such asPolioptilaandEremophila, it is noteworthy that the distal segment, the tarsometatarsus, is the longest, whereas in birds such asMyiarchusandTachycineta, that do not utilize the limbs in this manner, the tibiotarsus, the middle segment, is the longest. Mammals much modified for walking or hopping likewisehave the proximal segment, the femur, short, and the distal segment long (Howell, 1944). The waxwings have all of the segments short; these birds are modified for strong and sustained flight. Their hind limbs are used principally for landing devices and for perching. No one element of the leg has been shortened much, if any, more than any other.
leg bone lenghtsFig.44. Graph showing relative lengths of bones of the leg. The percentage values are shown on the axis of the ordinates.A.Bombycilla cedrorum; B.Bombycilla garrula; C.Dulus dominicus; D.Phainoptila melanoxantha; E.Phainopepla nitens; F.Ptilogonys cinereus; G.Ptilogonys caudatus.a. femur; b. tibiotarsus; c. tarsometatarsus; d. total.
Arm-trunk Percentages.—Tables 1 and 2show the total length of the arm, and lengths of the separate arm elements, relative to the trunk.Table 3gives the corresponding lengths for birds other than the Bombycillidae. Total length of arm was obtained by adding together the lengths of the humerus, ulna, and manus, and by dividing the figure thus obtained by the length of the trunk as was done for leg lengths intables 4 and 5. The method of adding together the component parts does not give the entire length of thewing, since the length of the feathers, which add effectively to the total length, as well as do the lengths of the small carpal elements, is lacking.
wing bonesFigs.45-46. Outlines of wings. × 1/245.Ptilogonys caudatus, showing relation of outline of wing to bones of arm.46.Bombycilla cedrorum, showing relation of outline of wing to bones of arm.
45.Ptilogonys caudatus, showing relation of outline of wing to bones of arm.
46.Bombycilla cedrorum, showing relation of outline of wing to bones of arm.
It may be noted thatPhainoptilaandBombycillahave the shortest arm in the family Bombycillidae. The humerus, radius and ulna are comparable to the same elements in thrushes and the catbird, and it is only the extremely short manus inPhainoptilathat affects the total. The manus inPhainoptilais comparatively smaller than in any other genus of the family Bombycillidae, and this indicates poor flight power.Bombycillahas a total length correspondingclosely to that in warblers, but the lengths of the distal elements correspond closely to those in the catbird and thrushes. Of the three segments, the humerus is, relatively, the most shortened. Next in order of increasing length of arm isDulus; measurements for it are roughly the same as those ofMyadestes. The wing bones of the Ptilogonatinae, other thanPhainoptila, are the longest in this series, and they most nearly resemble the same bones in flycatchers, Parids, and gnatcatchers.
arm bone lenghtsFig.47. Graph showing relative lengths of bones of the arm. The percentage values are shown on the axis of the ordinates.A.Bombycilla cedrorum; B.Bombycilla garrula; C.Dulus dominicus; D.Phainoptila melanoxantha; E.Phainopepla nitens; F.Ptilogonys cinereus; G.Ptilogonys caudatus.a. humerus; b. radius; c. ulna; d. manus; e. total.
It is notable that, in general, birds with long and narrow wings appear to have relatively the shortest humeri, with the distal bones, especially the manus, variable in length and seemingly correlated with the manner of feather attachment. Those birds with rounded and short wings have the longest humeri. In swallows, for example, the humerus is short, whereas the other arm bones are long, and the manus is unusually large and heavy. A short humerus gives better lever action in the flight stroke than a long humerus does.
MUSCULATURE
Dissections showed the same muscles to be present in all genera of the Bombycillidae. There are, nevertheless, differences in the size of the muscles in the various species, and these differences have been investigated primarily as a check on differences noted in the structure of the bones. Even slight differences in mass can be important functionally, but the difficulty in accurately measuring the mass prevents wholly reliable conclusions. The method first used in the attempt to determine the mass of a given muscle was that of immersing the muscle in a liquid-filled graduated tube, and then measuring the amount of liquid displaced. This method, although adequate for large muscles, was subject to a great amount of error in the case of small muscles, and consequently was abandoned. The technique eventually used was that previously employed by Richardson (1942). It consisted of dissecting out the muscle, placing it in embalming solution, leaving it there until a later period, and finally, weighing the muscle on scales, accurate to a milligram, after the muscle had been out of the liquid for a period of one minute. After being weighed, the muscle was measured by the displacement method in a graduated tube, as a check. The results indicate that, although the two methods give the same general results, weighing is accurate to one-hundredth of a gram, whereas the displacement method was accurate to only a tenth of a gram.
In determining the percentage of the weight of a muscle in relation to the total weight of the bird, the weight of the muscle was used as the numerator, and the weight of the preserved specimen was used as the denominator. Before weights were taken, all specimens were plucked in identical fashion.
Caudal Muscles.—The muscles of the caudal area that were used for comparison were the levator caudae and the lateralis caudae. These muscles are used by the living bird to maintain the position of the pygostyle and therefore the rectrices; these muscles are especially important to those birds that utilize the tail as a rudder in flight and as a brake. As may be seen by reference toTable 11, the two muscles are largest in proportion to body weight in the Ptilogonatinae, in which subfamily the species have long rectrices and must have correspondingly well-developed muscles in order to utilize the rectrices to best advantage in flight. The lateralis caudae differs more according to species than does the levator caudae, showing that rudder action of the tail is of primary importance in the adaptation for capturing insects. It will be remembered that thepygostyle in this subfamily has a flattened lateral surface for attachment of the levator caudae muscle, and it is therefore to be expected that this muscle will be larger in the Ptilogonatinae than it is in either the Bombycillinae or the Dulinae. The levator coccygis, together with the two muscles mentioned above, is responsible for elevation of the tail. The levator coccygis is less altered in different species of the family than is the lateralis caudae. It may be noted that the caudal muscles ofDulusandBombycillaconstitute a smaller percentage of the total weight of the bird than in any of the genera in the subfamily Ptilogonatinae.
caudal musculatureFig.48. Caudal musculature, ofPhainopepla nitens lepida, in dorsal view. × 2.a. Levator coccygis; b. Levator caudae; c. Lateralis caudae;d. Lateralis coccygis; e. oil gland; f. dorsal tip of pygostyle.
Table 11.Caudal Muscles (Actual and Relative Weights)
Table 12.Weights of Muscles (These percentages expressed in terms of weights of the body)
Pectoral Muscles.—The pectoral set of muscles varies but little in the family; flight power is seemingly not dependent upon size of either the pectoralis major or pectoralis minor. The data indicate that the insertion on the humerus, with consequent changes in the relative length of that bone, is more significant in type of flight and over-all flight power than is the actual size of the muscle mass. The deltoid muscle, for example, is smaller inBombycillathan in members of the other two subfamilies. The humerus inBombycillais shortened, and the muscle therefore does not need to be large to accomplish the same powerful stroke that would be accomplished by a longer humerus and a larger, more powerful deltoid muscle. In the case of the deltoid, the shortening of the humerus and the more complex arrangement of the points of insertion have obviated the necessity of enlarging the muscle.
Leg Musculature.—The muscles of the thigh are noticeably larger in birds that have long leg bones. (SeeTable 12for size of muscles.) On the tibiotarsus, the peroneus and gastrocnemius muscles were measured. When expressed as a percentage of the weight of the bird, the peroneus has much the same relative weight in all but one of the species, whereas the gastrocnemius varies much. The peroneus is proportionately large only inPhainoptila, in which genus all the leg muscles are well developed, but the gastrocnemius is larger in all the Ptilogonatinae and inDulusthan it is in the specializedBombycilla, in which it has probably been reduced as the leg bones and other muscles have been reduced.
The volume of the muscles of the hind limb changes more readily in response to saltation and running than do the muscles of the forelimb to flying.
DIGESTIVE TRACT
The digestive tract is relatively uniform in all genera of the family; there are only slight differences between the species. The degree of compactness of the visceral mass varies,PhainoptilaandPtilogonys caudatushaving the folds of the digestive tract loosely arranged, whereasPtilogonys cinereusandPhainopeplahave folds which adhere more tightly to the ventriculus and liver. InDulusandBombycilla, as compared with the Ptilogonatinae, the visceral mass (primarily liver and ventriculus) is situated more posteriorly in the body cavity, and is more compact, and the intestine is more tightly coiled.
The coiling of the intestine, if its degree of compactness is disregarded, is nearly identical in the birds of the family; there arefour major loops between the ventriculus and the anus. The length of this section of the tract is, however, somewhat variable, as can be seen by reference toTable 13, in which the actual and relative lengths of the intestine are given. It may be seen that inBombycillaand inPhainopepla, the tracts are much shortened. This is notable, since these are frugivorous birds, and in many frugivorous birds, the tract is lengthened for better extraction of edible portions of the food. Possibly the action of the digestive juices is correspondingly more rapid inBombycillaandPhainopepla, thereby permitting the necessary nutriment to be extracted by a short digestive tract.
In a migratory bird, or one that depends on flight power to find food and escape capture by predators, as in the case of the waxwings, the compacted and shortened visceral mass would seem to be advantageous, because of the consequent reduction in weight. I consider the longer intestine to be the ancestral condition, and that the intestine has become shorter to meet new environmental conditions.
Table 13.Digestive Tract: Actual Length, and Length Relative to Thoracic Length
Beddard (1898:30) states that caecae in the tract may be highly variable in a single family of birds. The Bombycillidae is no exception in this regard. At the junction of the cloaca and the large intestine, there are two small caecae, the function of which is unknown to me. The caecae are largest in the Ptilogonatinae, smaller in the Bombycillinae, and smallest in the Dulinae. There may be acorrelation between large caecae and more insectivorous diet and small caecae and frugivorous diet; however, the data are not conclusive in this regard.
ORIGIN OF THE SPECIES
It is here postulated that the center of origin for the ancestral stock of the Bombycillidae was in a region of North America, which at the time concerned was temperate or possibly even semi-tropical in climate. Probably Northern Mexico was the place and probably the climate was temperate. It is reasonably certain, because of the distribution of the species of the family, that they originated in the Americas. In the absence of paleontological data (Bombycillaalone is reported, in essentially its modern form, from the late Pleistocene—Wetmore, 1940a), the place and time of origin cannot certainly be determined.
The distribution of the family is such that the more primitive groups are in the south. These are the Ptilogonatinae in Central America and Mexico, and the isolated Dulinae in Haiti and the Dominican Republic. This distribution would support the view that the origin was in the south. However, the Holarctic Bombycillinae are so typically birds of northern latitudes that, were it not for such close relatives south of their range, it would appear logical to infer a northerly origin with a subsequent shifting of populations both southward and northward. The phyletic age of the family is probably great, however, as evidenced by the spotty distribution of the birds.
In the evolution of this family, population pressure possibly played the initial role in forcing members of the primitive, southern stock to seek habitable areas on the periphery of the range. Some birds also, being possessed of the "adventuresome spirit", aided the northerly movement, thus effecting an extension of the breeding ranges to the north. So far as is now known, this family did not seek living space in South America. By extending its range, a species might find more abundant food and nesting sites. This process of extending the range probably would be costly to the species concerned, because only those individuals best able to adapt themselves to the new environmental conditions would be able to survive long enough to reproduce their kind.
The return flight to the south could, in time, be dispensed with, except in the coldest weather or when the local berry- and fruit-crop failed. Birds such as waxwings are, of course, able to subsist ondried fruits and berries in the critical winter season when strictly insectivorous birds, not so catholic in their food habits, must return south. It appears that waxwings are descendants of migratory birds that have adjusted themselves to a life in the north; and they are judged not to have evolved from year-round residents of the north.
Even a short migratory journey in spring by part of a population of birds, while the other part remained in the original range, would quickly isolate one breeding population from the other, resulting in the formation of different genetic strains that lead to subspecies, species, and finally to genera and families. Any variation away from the ancestral, "sedentary" stock would become established more quickly because of such isolation at the breeding period. By the same token, the parental stock can, and no doubt does, become modified to suit its environment more perfectly, thus accelerating the tempo of this type of divergent evolution.
The original "split" of the Bombycillines is thought then to have been the result of migration on the part of some of the ancestral stock, with subsequent loss of regular migration because the need to return south was lost. Early in development, and before the migrational tendency was entirely lost, an isolated population, which later became sedentary, as it was an island population, diverged to give rise to the Dulinae. The Dulinae are a homogeneous group since on the islands now inhabited by the birds, they have not been isolated sufficiently long to produce even well-marked subspecies.
family treeFig. 49.Hypothetical family tree of the Bombycillidae.
The present dayPhainoptilais most nearly like the ancestral group, and the remainder of the Ptilogonatinae have diverged tofit conditions similar to those to which the Tyrannid flycatchers, which parallel them, are also fitted.
In comparatively recent geological time, two basic lines developed from the Bombycilline stock, the futureB. garrulaandB. cedrorum. Possiblygarrulaoriginally was isolated in Europe and Asia, and later came into contact withB. cedrorum, following the time at which the two species were genetically well differentiated. It appears certain thatB. japonicawas an offshoot of the Bombycilline stock at an early time, since it has characteristics that seem relatively unspecialized. It possibly was isolated in the Orient.
Structural affinities ofDulusandBombycillaare more pronounced than are those ofDulusandPtilogonys, for example. Many of the structural features ofDulusparallel those ofPhainoptila, and it seems likely that the Dulinae were separated early in the history of the family, perhaps as an isolated offshoot of the early migratory Bombycillinae.
CONCLUSIONS
Nomenclature, as used by a taxonomist, should of course indicate affinities as well as apply a name, and the rank of the family should be applied to a structural unit based on common anatomical characters that are more fundamental than, in my opinion, are those used by Ridgway (1904) in proposing family status for the silky flycatchers and the palm-chats. The characters in the diagnosis (page 478) of the family Bombycillidae are common features regarded as warranting a single family unit for the waxwings, silky flycatchers, and palm-chats. The differences in morphology used by previous workers to characterize each of these groups: (1) the silky flycatchers; (2) waxwings and; (3) palm-chats are regarded as more properly characters of only subfamily rank.
The existing coloration of the species of the Bombycillidae appears to have been acquired relatively late, geologically speaking. The three subfamilies responded to ecological stimuli in three different ways, and the resulting color patterns are unlike in the three groups. Dulinae to this day have a color pattern that is most like the ancestral color pattern, and this is recapitulated in the juvenal plumage of the Bombycillinae before they attain their adult plumage.
Consideration of the geographic distribution of the species of the family indicates that the center of origin of the family Bombycillidaewas south of the present range of the waxwings (subfamily Bombycillinae). Waxwings probably are the descendants of a migratory population that diverged from the primitive population at an early time in the history of the family. Owing to their adaptations to survive in the north, waxwings no longer return south in the autumn. Palm-chats (subfamily Dulinae) are descendants of an isolated population of the family stock that developed communal living habits as one specialization. Silky Flycatchers (subfamily Ptilogonatinae) became modified to catch insects, and have specializations that roughly parallel those of the Tyrannid flycatchers.
Osteologically, the various species of the Bombycillidae are remarkably similar. Small variations do exist, but these are primarily differences in relative size. The modifications of the beak enable palm-chats to feed on parts of plants, and the beak ofPhainoptilashows some similarity in this respect. Rounded wings, which cause a bird to fly by means of short, relatively weak strokes, are correlated with a comparatively long humerus, whereas long and pointed wings, which enable a bird to fly with more powerful strokes of the wing, are correlated with a relatively short humerus. There is a positive correlation between a short humerus and a long external condyle, and between a long humerus and the absence or smallness of the external condyle.
In the Bombycillidae short bones of the leg are adaptive, and long bones of the leg are the generalized condition. Although all passerine birds were differentiated relatively late in geologic time, long hind limbs still could have been present in the immediate ancestors of passerine birds. As adaptive radiation took place in the class Aves, some birds, the Bombycillidae included, became more and more adapted for an arboreal, and eventually an aerial habitat, with consequent loss of saltatorial and running ability.
Birds, like mammals, have a short femur, the most proximal element in the leg, if the species is adapted to run fast. If the species is not adapted to run fast, birds, unlike mammals, have the tibiotarsus longer than any of the other elements; in mammals that are not adapted to run fast, the femur and tibia are approximately the same length. In non-running birds as compared with running birds, the leg element distal to the tibiotarsus, and the one proximal to it, are considerably shortened. In waxwings, all three elements of the hind limb are shortened, indicating that the reduction in length has been, evolutionarily speaking, a rapid process, in order to reduce the limbs to a convenient size as soon as possible.
The shape of the pygostyle varies in the Bombycillidae, but the simple shieldlike bone ofPhainoptilais judged to resemble closely the ancestral type. InPtilogonysthere is a tall dorsal spine, coupled with a wide and heavy centrum and flattened lateral areas, for support of the long rectrices. InBombycillathe bone is small with knobs on the centrum that have been developed for muscle attachment.
The muscles were carefully dissected in each genus and in most of the species. The same homologous muscles are present in all species. Significant differences were found only in the relative size of certain muscles. No satisfactorily accurate method of measuring these differences was found. Consequently, less use was made of the results of the dissections than was originally planned.
The set of pectoral muscles varies but slightly in relative mass, and the variation is not considered significant. The deltoid muscle was selected for measurement since its point of insertion is unusually variable, while the mass of the muscle varies little. We can conclude that the extent of the area of insertion of the tendon of a muscle can determine that muscle's relative efficiency, while the muscle itself remains the same in bulk.
The muscles of the hind limb are notably larger in species that have long legs, and a good index of the hopping ability may be gained by study of certain of these muscles. In the Bombycillidae, and in those Ptilogonatinae that do not use the hind limbs for hopping, the bones are shortened, and the associated muscles are correspondingly smaller.
The gross anatomy of the digestive tract is practically identical in the members of the family. The variability noted is mainly in the degree of compactness of the visceral mass inBombycillaand inPhainopepla. Also there is a tendency for the Bombycillinae and the Dulinae to have the mass situated more posteriorly than it is in the Ptilogonatinae. Moreover,Bombycillahas a shorter intestine than do the other genera. All of this indicates that the waxwings (Bombycillinae) have the center of gravity situated more advantageously for flight than do the birds of the two other subfamilies.