=======================+=======+=============+=================+======
Species | Femur | Tibiotarsus | Tarsometatarsus | Total
-----------------------+-------+-------------+-----------------+------
Corvus brachyrynchos | 71 | 120 | 77 | 268
Corvus corax | 73 | 139 | 78 | 290
Dendroica audubonii | 62 | 109 | 81 | 252
Setophaga ruticilla | 66 | 127 | 94 | 287
Myadestes townsendi | 61 | 99 | 60 | 220
Sialia sialis | 66 | 111 | 72 | 249
Hylocichla mustelina | 75 | 133 | 97 | 305
Parus atricapillus | 78 | 138 | 99 | 315
Tachycineta thalassina | 61 | 97 | 56 | 214
Myiarchus crinitus | 68 | 106 | 74 | 248
Dumetella carolinensis | 73 | 136 | 94 | 303
Polioptila caerulea | 75 | 144 | 113 | 332
Eremophila alpestris | 73 | 113 | 115 | 301
Muscivora forficata | 62 | 98 | 61 | 221
-----------------------+-------+-------------+-----------------+------
Table 7. Actual Length and Width in mm. of Pygostyle and Proportionate
Length and Width of Pygostyle in percent of Lacrimal Length
=========================+========+=======+=========+=========
| | | Length, | Width,
Species | Length | Width | percent | percent
-------------------------+--------+-------+---------+---------
Ptilogonys caudatus | 9.8 | 3.9 | 45 | 18
Ptilogonys cinereus | 8.8 | 4.1 | 41 | 19
Phainopepla nitens | 8.4 | 3.9 | 41 | 19
Phainoptila melanoxantha | 8.5 | 3.5 | 35 | 14
Dulus dominicus | 8.5 | 2.9 | 38 | 13
Bombycilla garrula | 7.0 | 3.5 | 31 | 15
Bombycilla cedrorum | 7.1 | 2.9 | 35 | 14
-------------------------+--------+-------+---------+---------
Table 8. Length of Sternum and Depth of Carina expressed as
percentages of the Length of the Trunk
=========================+=========+========
Species | Sternum | Carina
-------------------------+---------+--------
Ptilogonys caudatus | 85 | 28
Ptilogonys cinereus | 91 | 32
Phainopepla nitens | 81 | 26
Phainoptila melanoxantha | 76 | 25
Dulus dominicus | 107 | 28
Bombycilla garrula | 88 | 33
Bombycilla cedrorum | 82 | 31
-------------------------+---------+--------
Table 9. Skull and Sternum, Length and Width in mm.
=========================+========+=======+=========+=========
| Length | Width | Length | Width
Species | of | of | of | of
| Skull | Skull | Sternum | Sternum
-------------------------+--------+-------+---------+---------
Ptilogonys caudatus | 34.9 | 15.6 | 23.9 | 7.8
Ptilogonys cinereus | 33.4 | 14.7 | 24.3 | 8.5
Phainopepla nitens | 33.3 | 15.1 | 21.3 | 6.9
Phainoptila melanoxantha | 39.7 | 16.0 | 24.8 | 8.2
Dulus dominicus | 36.4 | 16.6 | 30.5 | 8.0
Bombycilla garrula | 37.0 | 16.8 | 30.0 | 11.2
Bombycilla cedrorum | 34.0 | 15.5 | 25.3 | 9.6
-------------------------+--------+-------+---------+---------
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)
=========================+========+=======
| Length | Width
Species | of | of
| Skull | Skull
-------------------------+--------+-------
Ptilogonys caudatus | 160 | 72
Ptilogonys cinereus | 158 | 69
Phainopepla nitens | 162 | 73
Phainoptila melanoxantha | 161 | 65
Dulus dominicus | 164 | 75
Bombycilla garrula | 164 | 74
Bombycilla cedrorum | 162 | 74
-------------------------+--------+-------
[Illustration: Fig. 43. Part of skeleton of _Bombycilla cedrorum_
showing method of measuring the length of the trunk.
Natural size.]
_Leg-trunk Percentages._--Table 4 shows the relative lengths of the
legs and of the separate bones in the legs of the different species of
the Bombycillids. Table 5 shows 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 and
tarsometatarsus. 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 4 shows that of the birds compared in this paper, _Dulus_ has
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 to Table 5 that
_Tachycineta_ and _Myadestes_ fall 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 are _Hylocichla
mustelina_, a typical ground dweller, and _Parus atricapillus_, which
hops about in the trees and underbrush.
Insofar as the lengths of the legs show, _Dulus_ and _Phainoptila_ are
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, _Dulus_ and _Phainoptila_ have remained unspecialized, in
contrast to the waxwings in which adaptive changes fitting them for a
perching habit have taken place. _Ptilogonys_ and _Phainopepla_ are
intermediate in length of leg between _Phainoptila_ and _Bombycilla_,
and _Ptilogonys_ and _Phainopepla_ have progressed from life on the
ground toward the perching habit. _Bombycilla cedrorum_ is more
specialized than is _B. garrula_ in shortness of leg, and the
reduction is comparable, as is noted above, to that in the legs of
_Tachycineta_.
In birds which have the legs much modified for walking or for hopping
in the brush, such as _Polioptila_ and _Eremophila_, it is noteworthy
that the distal segment, the tarsometatarsus, is the longest, whereas
in birds such as _Myiarchus_ and _Tachycineta_, that do not utilize
the limbs in this manner, the tibiotarsus, the middle segment, is the
longest. Mammals much modified for walking or hopping likewise have
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.
[Illustration: Fig. 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 2 show the total length of the
arm, and lengths of the separate arm elements, relative to the trunk.
Table 3 gives 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
in tables 4 and 5. The method of adding together the component parts
does not give the entire length of the wing, 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.
[Illustration: Figs. 45-46. Outlines of wings. x 1/2
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 that _Phainoptila_ and _Bombycilla_ have 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 in _Phainoptila_ that affects the
total. The manus in _Phainoptila_ is comparatively smaller than in any
other genus of the family Bombycillidae, and this indicates poor
flight power. _Bombycilla_ has a total length corresponding closely 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 is _Dulus_; measurements for it are roughly
the same as those of _Myadestes_. The wing bones of the
Ptilogonatinae, other than _Phainoptila_, are the longest in this
series, and they most nearly resemble the same bones in flycatchers,
Parids, and gnatcatchers.
[Illustration: Fig. 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 to Table 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 the
pygostyle 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 of _Dulus_ and _Bombycilla_
constitute a smaller percentage of the total weight of the bird than
in any of the genera in the subfamily Ptilogonatinae.
[Illustration: Fig. 48. Caudal musculature, of _Phainopepla nitens
lepida_, in dorsal view. x 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)
=============================================
Species | Levator | Lateralis
------------------------+---------+----------
Ptilogonys caudatus | .145g. | .022g.
| .092% | .045%
| |
Ptilogonys cinereus | .030g. | .010g.
| .076% | .026%
| |
Phainopepla nitens | .025g. | .008g.
| .096% | .029%
| |
Phainoptila melanoxantha| .040g. | .015g.
| .063% | .014%
| |
Dulus dominicus | .028g. | .006g.
| .063% | .014%
| |
Bombycilla garrula | .034g. | .010g.
| .048% | .014%
| |
Bombycilla cedrorum | .026g. | .008g.
| .050% | .014%
---------------------------------------------
Table 12. Weights of Muscles (These percentages expressed in terms
of weights of the body)
Key to Table
A) Deltoid
B) Thigh
C) Peronus
D) Gastrocnemius
====================================================================
Species |P. major|P. minor| A | B | C | D
---------------+--------+--------+--------+--------+-------+--------
Ptilogonys | 2.42g. | .29g. | .55g. | | |
caudatus | 4.94% | .59 | 1.12% | .43g. | .15g. |
| | | | .88% | .31% | .96%
Ptilogonys | 2.19g. | .28g. | .53g. | | |
cinereus | 5.57% | .71% | 1.35% | .30g. | .08g. |
| | | .71% | .21% | 1.02%
Phainopepla | 1.30g. | .20g. | .30g. | | |
nitens | 4.99% | .77% | 1.15% | .28g. | .10g. |
| | | | 1.12% | .40% | 1.42%
Phainoptila | 3.93g. | .44g. | .92g. | | |
melanoxantha | 6.18% | .69% | 1.45% | 1.09g. | .48g. |
| | | | 1.61% | .75% | 2.97%
Dulus | 2.09g. | .22g. | .50g. | | |
dominicus | 4.81% | .50% | 1.15% | .73g. | .18g. |
| | | | 1.68% | .41% | 1.01%
Bombycilla | 3.85g. | .45g. | .55g. | | |
garrula | 5.31% | .62% | .76% | .50g. | .15g. |
| | | | .69% | .18% | .59%
Bombycilla | 2.58g. | .35g. | .50g. | | |
cedrorum | 5.00% | .68% | .97% | .37g. | .10g. |
| | | | .73% | .19% | .83%
---------------+--------+--------+--------+--------+-------+--------
_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 in _Bombycilla_ than in
members of the other two subfamilies. The humerus in _Bombycilla_ is
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. (See Table 12 for 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 in _Phainoptila_, in which genus all the leg muscles are
well developed, but the gastrocnemius is larger in all the
Ptilogonatinae and in _Dulus_ than it is in the specialized
_Bombycilla_, 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, _Phainoptila_ and _Ptilogonys
caudatus_ having the folds of the digestive tract loosely arranged,
whereas _Ptilogonys cinereus_ and _Phainopepla_ have folds which
adhere more tightly to the ventriculus and liver. In _Dulus_ and
_Bombycilla_, 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 are
four 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 to Table 13, in which the actual and relative
lengths of the intestine are given. It may be seen that in
_Bombycilla_ and in _Phainopepla_, 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 in _Bombycilla_ and _Phainopepla_, 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
=========================+========+==============
| | Relative
Species | Length | length
| in mm. | (in percent)
-------------------------+--------+--------------
Ptilogonys caudatus | 134 | 476.9
Ptilogonys cinereus | 111 | 415.6
Phainopepla nitens | 94 | 357.5
Phainoptila melanoxantha | 150 | 457.1
Dulus dominicus | 130 | 451.0
Bombycilla garrula | 102 | 298.2
Bombycilla cedrorum | 95 | 309.5
-------------------------+--------+--------------
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 a
correlation 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 (_Bombycilla_ alone
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 on
dried 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.