UNI(2UE morphologic specialization in a single species or genus pro-
rides one of the best approaches into the entire subject of adaptation and
the evolution of new groups. Further, if the animal possessing the
unique specialization lives in an unusual or strenuous habitat, then the
action of the evolutionary processes is frequently easier to understand.
The gray jays of the genus Perisoreus form an excellent basis for the
discussion of some of these problems as they are permanent residents
in the far northern coniferous forests--one of the most strenuous
habitats available to passerine birds. Gray jays must possess adapta-
tions to the cold of winter and the ability to utilize the limited food
supply available during the winter. The question of protection against
the cold shall not be considered as I wish to concentrate on the problem
of food gathering. This latter problem has been overlooked by orni-
thologists because the gray jays, like most other permanent residents
in the northern forests, were not known to have any marked feeding
adaptations. But the discovery of a pair of "woodpecker-sized" mandib-
ular mucous glands in the gray jays reopens the question of their
feeding habits. Mucous glands as large as those found in the wood-
peckers are, to the best of my knowledge, not known in any other pas-
serine bird. This leads to the question of whether this structure is a
special adaptation in the gray jays for life in the northern coniferous
forests. These questions cannot be answered directly because of a lack
of information on the function and biological role of the glands, but I
shall speculate on them because of their bearing on the general topic
of adaptation of birds to the northern forests as well as their importance
to the evolution of the gray jays.
DESCRIPTION OF THE GLAND
The pair of mandibular glands was present and equally well developed
in the three adult specimens of ?. can.adensis examined, indicating that
they are a normal feature of this species. The glands were also present
in the two specimens of P. infaustus dissected, but they were consider-
ably shrunken because of preservation and long storage in alcohol.
Whether the glands are present in the third species of this genus,
internigrans, is not known. Topographically, the glands lie in the same
position and have the same general appearance as do the mucous glands
of the woodpeckers. When the head is examined from beneath, the
paired mandibular glands can be seen lying between the mandible and
the hyoid bones (Figure lB). At their anterior end, a small, flattened
roedial projection may be seen. This flattened appendix extends some-
what forward of the main portion of the gland and disappears into the
floor of the mouth lateral to the tongue at a point just level with the
'center of the eye. The main collecting ducts, which lie within this
Figure 1. The mandibular gland of the Gray Jay (Perisoreus canadensis)
seen from the side (A) and from beneath (B). The gland (GL) lies
between the mandible and the hyoid bones and extends around the back of
the skull to reach a point just dorsal to the origin of the M. depressor man-
dibulae. The lines crossing the gland in the ventral view indicate the levels
at which hlstological sections were cut.
medial projection, as will be shown below, pass through the floor of the
mouth to open into the buccal cavity near the lateral edge of the tongue.
When viewed front the side (Figure 1A), the gland can be seen curving
dorsally around the posterior end of the mandible to reach a point just
above the dorsal end of the M. depressor mandibulae. When removed
from the head, this "moon-shaped" gland is seen to be twisted on its
longitudinal axis so that its posterior end no longer faces dorsally, but
somewhat medially. As would be expected, the general shape of the
gland conforms to the shape of the head that is, it fits in between the
other structures without interfering structurally or functionally with
them (see Dullemeijer, 1958, pp. 77-78). In size, the gland is approxi-
mately 24 min. long, 6 ran1. wide at its greatest width aud 4 1rim. thick
(maximran).
According to the most recent classification for the arian salivary
glands (Antony, 1920; se also Farner, 1960, pp. 413-4141, the en-
larged gland in the Gray Jay is part of the GI. mandibdaris. Most prob-
ably it is the Gl. mandibularis medialis, although it is difficult to dis-
tinguish and identify the various components (if the (;l. mandbdaris com-
plex with certainty. It should be pointed out that the Gl. mandibularis
medialis of the Gray Jay is almost certainly not homologous with the
large mucus-secreting gland in the woodpeckers. Unfortunately, An-
tony was not clear in her discussions of the "woodpecker gland." In
her listing of the salivary glands in birds (p. 5501, she considers the
"woodpecker gland" to be a completely separate gland, the Gl. picorum;
but in a table showing the distribution of the salivary .glands in the
woodpeckers, she includes the Gl. picorum as a subdivision of the Gl.
manibularis. Thus, it is not certain whether the Gl. picortm is part of
the Gl. mandibularis complex; but, even if it is, it would be an anterior
part of that gland, not a roedial and more posterior part as is the mandib-
ular gland of the gray jays.
The gross histologic structure of the mandibular gland can be understood by an
examination of the figures (see Figures 2A-2D). The collecting ducts gather
together on the medial side of the gland, formiug the flattened appendix seen in
the ventral view of the head. Iu the anterior sections, the collecting ducts com-
prise more than half of the cross-sectional area, while in the posterior slides, the
ducts become smaller, pass to the iuternal surface of the gland, and gradually
drop out with a corresp:mdiug disappearance of the nedial appeudix. The epi-
thelial cells lining the collecting ducts appear to be a pseudostratified columuar type
with a striated border. The secretory cells are arranged iu long tubules, which
run parallel to the longitudinal axis of the gland. A heavy theca of connective
tissue surrounds each tubule as veI1 as the entire gland. In the posterior half of
the gland only secretory tubules are present; the collecting ducts have dropped
out completely. Lumina and snall ducts can be seen inside the tubules. The
secretory cells appear to be arranged in rows radiating out frown the central duct
of each tubule. The cells are relatively tall for secretory cells, with rounded
nuclei that lie at the basal end of the cell, but are not pressed against the floor as
is usual for mucus-secreting cells. These observations on the cellular structure
are not conclusive because of the fixation, nor could any additional details be
ascertained. It was not possible to determine the type of secretion from a histo-
logical examination of the gland cells.
The suspected mucus-secreting nature of the gland was confirmed by the appli-
cation of several histochemical procedures (see Gomori, 1952, and Lillie, 1954, for
description of these tests). Staining with Paraldehyde Schiff reagent (PAS),
with PAS combined with a diastase digestion, and with toluidine blue were all
positive, which proves quite conclusively that the granules within the secretory
cells are mucoid and hence that this gland secretes mucus.
Figure 2. Semischematic drawings of the histological structure of the
mandibnlar gland of the Gray Jay (Perisoreus canadensis). The Figures
A to D were traced from sections cut from the levels A to D shown in Figure
lB. The sections are oriented with their ventral side upwards and their
medlal side to the left. Magnification of the sections is, for technical reasons,
not the same; Figures A and B are enlarged about two to three times more
than Figures C and D. The secretory tubules are shaded by stippling, the
MANDIBULAR GLANDS IN OTHER CORVIDS
Before it is possible to inquire into the adaptive value of the large
mandibular glands in the gray jays, it is necessary to ascertain whether
this structure is unique in this genus. Specimens of the following forms
were dissected: Garrulus glandarius, Cyanocitta cristata, C. stelleri, C.
coerulescens, Pica pica, Nucifraga columbiana, Corvus brachyrhynchos,
C. corona, and C. frugilegus. All had an area of small mandibular
glands lying in the floor of the mouth as described for various members
of this family (see, Cholodkowsky, 1892; Hblting, 1912; Greschik,
connective tissue by a broken-line pattern, and the collecting ducts are left
blank with their walls shown by vertical lines in Figures A and B. In Figure
A, the collecting ducts are bunched together on the roedial side of the
section; this is the medial projection seen in Figure lB. Note how the
collecting ducts then pass to the middle of the dorsal side of the gland
(Figures B and C) before becoming completely scattered in the posterior
part of the gland (Figure D).
1913; and Antony, 1920). Although this area is extensive in some
species, no species have a gland equal in size to that found in the gray
jays. Special care was taken in dissecting the rook because Antony
(1920, p. 600) reported the Gl. mandibularis externa in this species to
be 30 min. long and 6 min. wide. I dissected several adult rooks and
found the Gl. mandibularis externa as well as the usual field of small
mandibular glands. The G1. mandibularis cxterna is buried within the
floor of the mouth and is hidden for most of its length by the mandible.
This gland appeared to be smaller than the figures given by Antony
(precise measurements were not possible), but in any case it is con-
siderably smaller in absolute and relative size than the mandibular gland
of the Gray Jay. Although I was not able to examine all genera of
the Corvidae, it may be tentatively concluded that the large mandibular
glands in the gray jays are a unique feature in the corvids and are
probably unique in the passerine birds. Additional evidence is needed
before this conclusion can be fully accepted; this can be obtained whi'e
skinning birds as the glands lie directly under the skin. [ would like
to suggest that collectors examine all specimens of corvids, and other
passefine birds if possible, for the presence of large mandibular glands.
DISCUSSION
Why should a pair of woodpecker-sized mucous glands have evolved
in the gray jays, birds living in the far northern coniferous forests?
Normally, mucus from salivary glands has the function of lubricating
the mouth (see Farner, 1960, p. 414). Among birds with greatly en-
larged salivary glands, the mucus is sticky and serves as a cementing
substance for nest construction (e.g., swifts) or to coat the tongue,
thereby transforming it into a "lime-stick" suitable for capturing insects
or other food (e.g., woodpeckers). In the case of the gray jays, the
most reasonable working hypothesis is that the mucus coats the tongue
and changes it into a lime-stick. The tongue of these birds is a normal
corvid tongue--fiat with some fringing at the tip--which is completely
suitable for tongue probing. The use of the tongue would allow the
gray jays to obtain food such as seeds still in coniferous cones and
insects in bark crevices, which they could not reach with their short,
blunt bill. But do the gray jays obtain food by tongue-probing and
if so, why?
A search was made through the literature to ascertain whether gray jays have
been observed feeding by means of tongue probing. However, aside from numer-
ous statements on the camp-robbing habits of these birds, I have found little about
the food habits and feeding methods of the gray jays and nothing of help for
the present problem. Here I wish to enter a plea for observations on their
feeding methods, especially during the winter when food would be scarce. These
observations would be difficult to make because of the rarity of these birds and
the fact that they can be shy and elusive during parts of the year, but this infor-
mation is absolutely essential for solving the function of the maodibular glands.
Perhaps the observations could be made on captive birds by presenting them with
food (e.9., coniferous cones containing seeds) that they can only reach with their
tongues. Nevertheless, there is some indirect evidence supporting the hypothesis
of tongue probing. First is the availability of food to the gray jays during the
winter; the food supply, not the cold, is the more restricting factor to birds in
the north. While the ground is covered with snow, the food supply is almost
entirely restricted to what can be found on trees. And this food is most probably
largely limited to what is concealed in crevices in the bark and so forth; any
insects, their eggs, and so forth lying on exposed surfaces would probably be
rapidly washed away by storms or may be too small to be utilized by gray jays.
Besides insects in bark crevices, this food would include seeds still in coniferous
cones. Second, the bill of these birds is blunt and would not permit them to obtain
this food directly. Third, there are indications that the gray jays do eat pine
seeds. Peterson, et al. (1954, p. 204) make the brief statement that the Siberian
Jay is: "Agile in clinging to tips of pine branches to reach cones," which I was
able to confirm in some observations on this species in northern Sweden during
the summer of 1960. I saw several individuals of Siberian Jays clinging to the
tips of branches and seemingly feeding on the cones hanging there, but I was not
close enough to determine whether they were using their tongue in any way.
Mrs. Lawrence informed me in a letter that during the winters when evergreen
seeds are scarce, Gray Jays appeared at feeding stations in Ontario in greater
numbers, which lead her to suspect that cone seeds may contribute an important
part of the diet of these jays. She added that, unfortunately, she has never
observed them eating seeds from cones. Mr. Helminen informed me, also by
letter, that there are scattered reports of Siberian Jays in Finland eating conifer-
ous seeds or cones during the winter, but he was not able to supply any further
details. These few facts constitute all of the support for the tongue-probing
theory, which must remain as a hypothesis until more evidence has been gathered.
It is, nevertheless, of interest to speculate further on the part
played by the mandibular glands in the adaptation and evolution of the
gray jays for xvhich I shall assume the correctness of the tongue-probing
hypothesis. Next it is important to kuow xvhat percentage of their
total food is obtained in this manner. It may be assulned that, during
the summer mouths, only a small part of the food is attained by probing,
xvhile, during the winter, a major share of the total food is obtained by
tongue probing. Again, these assumptions must be verified or rejected
by direct observations, but until definite evidence is available, I shall
accept them as tentatively correct. Hence, it may be concluded that, ir
addition to other necessary adaptations such as resistance to cold, the
gray jays are able to live permanently in the northern forests because
of their ability to gather food by tongue probing. Further, it may be
concluded that these anatomical features that enable the gray jays to
tongue probe constitute the most important feeding adapations of this
genus. The mandibular glands are one of these important feeding
adaptations, and probably they are the most basic one. All of the
other anatomical features--the tongue, hyoid muscles, and so forth--
involved in tongue probing are little, if any, changed from the typical
corvid condition and may be considered to have been preadapted for the
new feeding method. Only the mandibular glands are vastly different
between the gray jays and other corvids, and they are the sole anatomical
feature (i.e., a mucus-secreting salivary gland) whose development de-
termines whether a corvid bird can probe with a sticky tongue. Thus,
the development of the mandibular glands was the critical morpho-
logic innovation in the strictest sense of the concept (see Miller, 1949)
that enabled the gray jays to enter their present ecological niche. One
of the most interesting aspects of the mandibular glands as a critical
innovation is that they are not a new structure, but only the enlarge-
ment and modification of a structure already present in the Corvidae.
The enlargement of a gland is a rather simple evolutionary change.
which shows how a simple modification can become the critical innova-
tion permitting the development of a new feeding method and the
utilization of a new ecological habitat, and might even have been the
factor responsible for the evolution of a new genus of corvid birds.
The evolution of the large mandibular glands and the establishment of the gray
jays as permanent residents in the northern forests can be easily visualized. The
ancestral form may have had a distribution such as found in some present-day jays
(e.g., Cyanocitta or Garrulus)--covering the temperate and northern forests with
the birds breeding in the northern parts of the range migrating to the southern
parts--or they may have been temperate forest birds expanding to the north.
These birds would have had the normal corvid arrangement and development of
salivary glands, and most likely made no special use of their tongue in feeding.
Yet, the tongue was probably slightly sticky because of the normal supply of
mucus to the mouth. Two associated changes, one behavioral and the other mor-
phologic, had to occur before the evolution of the large mandibular glands could
begin; both of these changes are well within the normal range of reaction or
variation of corvid birds. The behavioral change was that the birds began to
probe into crevices with their tongue to reach the food lodged there, this action
being well within the ability of these normally curious birds. The success of this
new feeding action would depend upon the stickiness of the tongue. The morpho-
logic change was an increase in the size of the mucous glands and hence the
supply of mucus; however, it did not matter vhich of the salivary glands in-
creased in size. The new, but inefficient, tongue-probing method allowed the
birds to utilize a previously unattainable food supply and may have permitted
them to remain longer in the northern parts of their range before moving south
with the onslaught of winter. If it was advantageous for the birds to remain north
longer in the fall, then the new feeding method would have a definite selective
value and those birds able to probe with their tongue would have a selective
advantage. Why the new feeding method was advantageous--whether there was
competition from other species in the temperate regions or whether the birds
breeding early in the spring left more offspring--is of no importance; it is only
necessary to assume that remaining in the northern part of the range was advan-
tageous. At first only a part of the population would possess the beginnings of
the new feeding method, and these would have been able to remain in the northern
area slightly longer in the fall. As the genetic factors controlling the increase
in the size of the mucous glands and the ability of probing with the tongue
increased in the population, the efficiency of the tongue probing increased and the
birds were able to remain in the north longer and longer in the fall until finally
some individuals, by virtue of their now better-developed ability to tongue probe,
were able to remain during mild winters. Specialization of tongue probing, in-
cluding the size of the mucous glands, has reached the point that today the gray
jays must move south only during the severest winters. From this suggested
evolutionary history, it can be seen that the behavioral and morphologic changes
occurred simultaneously and slowly during the entire phylogeny of the gray jays,
and that even the very first changes were under the control of natural selection.
It may be asked: if the large mucus-secreting mandibular glands are
essential adaptations in the gray jays, why have similar glands not de-
ve!oped in other permanent residents of the northern forests? The
answer may lie in the fact that the feeding methods of the ancestors of
most of these birds were suitable, i.e., preadapted, to life in these
forests and did not have to be altered as the birds entered the new
habitat. Woodpeckers, nuthatchers, chickadees, finches, shrikes, and
so forth all feed on food that is available in the northern forests during
the winter, so that these birds can become permanent residents if they
are able to resist the cold. Moreover, it is possible that some of these
birds have special feeding adaptations that are yet unknown. But the
most interesting fact is that Perlsoreus is, with the exception of Pinicola,
which has doubtless evolved from a northern-adapted finch, the only
genus of passerine birds endemic to the northern coniferous forests; all
other permanent residents of these forests are members of wide-
spread genera. This may be coupled with the fact that the gray jays
are the only known passerine birds with a special feeding adaptation to
this habitat. This may be only a coincidence. But in any case this cor-
relation deserves additional study.
Tichomirov (1925) has reported "larger" mandibular glands (= G1. ,nandibu-
laris externa ?) in some species of chickadees. From his figures this gland appeared
to be as large, relatively, as the G1. mandibularis externa of the rook, and hence
it is considerably smaller, relatively, than the mandibular gland of the gray jays.
It has been noted by some observers that the gray jays feed in a manner similar
to chickadees. These observations allow two assumptions. The first is that
chickadees can also tongue probe. The second is that the mucus from the large
mandibular glands in one or both forms has a totally different function.
.fix CKNOWLEDGM ENTS
I am indebted to Dr. Carl Helms, who collected the specimens of
Gray Jays (Perisoreus canadensis) used in this study, to Dr. Ruth
Willey, who stained the slides for the presence of mucus and interpreted
the results, to Dr. P. Dullemeijer (University of Leiden), who supplied
several specimens of the Rook (Corv,s fr, cdilecdus), to the officials of the
British Museum (Natural History), who gave permission for dis-
secting two specimens of the Siberian Jay (P. infaustus), and to lny
wife, Kitty, who prepared the histological slides as well as aiding in the
preparation of the manuscript and figures. My sincere thanks are ex-
tended to all. In addition I wish to thank the many people, especially
Mrs. L. de K. Lawrence and Mr. Matt/ Helminen, who have supplied
information on the feeding habits of the gray jays. This study was
started while I was working under a National Science Foundation
predoctoral fellowship at Harvard University and completed while
I was at the Anatomisches Institut der Ulfiversitiit, Frankfurt a.M.
under a National Science Foundation Postdoctoral Fellowship. I wish
to express my gratitude to both the National Science Foundation and
to the officials of the respective institutes for their generous support
and help.
SUMMARY
A pair of woodpecker-sized, mucus-secreting mandibular glands has been found in the gray jays; these are a unique feature in the Corvidae and are probably unique in the passerines. The mucus from these glands presumably coats the tongue, thereby making it sticky and suitable for probing into crevices for insects and under the scales of cones for seeds during the winter when other food is scarce. The mandibular glands are thus probably the basic feeding adaptation in these species and appear to be the critical innovation that has allowed the development of a new method of feeding and the invasion of a new ecological niche.
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Mnatomisches [nstitut der Universitiit Frankfurt a. iV[. Present
dress: Department of Zoolo9y. University of Illinois. Urbana. Illinois.