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Ultrastructure of lingual salivary glands in the American chameleonAnolis carolinensis.

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THE ANATOMICAL RECORD 229:489-494 (1991)
Ultrastructure of Lingual Salivary Glands in the
American Chameleon: Anolis carolinensis
Departments of Pediatric Dentistry (T.R.) and Oral Biology (B.T.), School of Dentistry,
Case Western Reserve University, Cleveland, Ohio
That portion of the dorsal surface of the tongue of Anolis carolinensis that is covered by plumose papillae is underlaid by a series of tubular
salivary glands that open between the papillae; glands persist into the posterior
zone of the tongue, where they open between cylindriform papillae. Anterior
glands are serous in nature-they consist of simple columnar epithelial cells that
contain abundant secretory granules exhibiting a variety of substructural patterns. The Golgi apparatus is large and of unusual appearance, with numerous
closely packed terminal dilatations and condensing vacuoles. Near the posterior
border of the lingual zone covered by plumose papillae, mucous cells begin to
appear in the glandular epithelium. More posteriorly, the apical portions of the
glands consist entirely of mucous cells, whereas the blind ends of the glands are
composed of serous cells. The most posterior glands are of the pure mucous variety.
The glands finally disappear a short distance posterior to the cylindriform papillae.
The functions of the abundant and highly differentiated salivary glands of the
Anolis tongue remain obscure.
The dorsum of the tongue of the American chame- jaws from decapitated animals were fixed by immerleon has a complex morphology (Rabinowitz and Tan- sion in a triple aldehyde-DMSO mixture (Kalt and
dler, 1986; Kurabachi and Aiyama, 1987). Based on Tandler, 19711, then postfixed in osmium tetroxide.
papillary structure, the lingual dorsum can be divided Specimens were embedded in Epon-Maraglas (Tandler
into four consecutive zones of approximately equal size. and Walter, 1977). Thin sections were examined in a
The tongue tip (the first zone) is relatively smooth, Siemens Elmiskop l a or 101 electron microscope; thick
while the second and fourth zones are covered by cy- sections stained with methylene blue-azure I1 (Richlindriform papillae. The third zone is festooned with ardson et al., 1960) were examined in a Zeiss Ultraphot
papillae of novel morphology, which we have named 11.
“plumose papillae” (Rabinowitz and Tandler, 1986).
These papillae have peculiar surface epithelial cells,
which are connected to the underlying epithelial cells
Glands are absent from the anterior portion of the
by slender stalks and which have a bulbous free end
where the nucleus resides. A single skeletal muscle tongue and from much of the second zone, which is
fiber is connected to the epithelial basement membrane covered by cylindriform papillae. Glands first appear
at the tip of each papilla and extends within the con- slightly anterior to the plumose papillae. Initially
nective tissue core to mingle with the intrinsic muscu- rather short, the glands quickly reach their maximum
length (4.3 mm) beneath the plumose papillae (Fig. 1)
lature in the body of the tongue.
Starting just anterior to the line of junction between and maintain this length through a good part of the
the second and third zones and extending beyond the next zone. Near the posterior border of this fourth zone,
posterior border of the fourth zone is a series of tubular the glands become progressively shorter and finally
salivary glands that open between the papillae in a n disappear.
All the glands consist entirely of secretory cells ararrangement that recalls that of crypts of Lieberkuhn
and villi in the small intestine. Because in a sense ranged in a simple columnar epithelium. From the
these glands are the evolutionary forerunners of mam- most anterior point where they occur to a transverse
malian salivary glands, i t was felt that a n electron line midway through the zone occupied by plumose pamicroscopic examination of them was warranted. Al- pillae, the glands are pure serous in nature (Figs. l , 2).
though histologically simple, these lingual glands are At that line of demarcation, mucous cells begin to appear in small clusters among the serous cells (Fig. 3) or,
cytologically complex.
more generally, at the stomata of the glands (Fig. 4).
The American chameleons (Anolis carolinensis) used
in this study were treated according to the protocol
detailed in our previous report (Rabinowitz and Tandler, 1986). To recapitulate briefly, the ablated lower
Received April 24, 1990; accepted September 14, 1990.
Address reprint requests to Dr. Bernard Tandler, School of Dentistry, Case Western Reserve University, Cleveland, OH 44106.
Figs. 1-4.
49 1
Fig. 5. Electron micrograph of a portion of the glandular epithelium showing the simple columnar
serous cells. The apical half of each cell is dominated by secretory granules. A large Golgi apparatus lies
between the granules and the basally placed nucleus. The edge of a myofiber that extends into a plumose
papilla is present a t the lower border of the micrograph. X 5,600.
Proceeding posteriorly, the mucous cells gradually supplant the serous cells, so that the posterior glands are
pure mucous in nature. Serous cells contain small, discrete, densely stained secretory granules (Fig. 2). In
contrast, the secretory product in mucous cells is less
well defined (Fig. 4) and shows a pronounced metachromasia in sections stained with methylene blueazure 11. Both serous and mucous glands exhibit occasional clear (unstained) cells within their epithelial
lining (Fig. 2).
Electron Microscopy
(Figs. 1-4) Fig. 1. Photomicrograph of the dorsum of an epoxy-em-
bedded Anolis tongue showing the closely packed plumose papillae
and the intervening tubular lingual glands. Methylene blue-azure 11.
x 190.
Fig. 2. Longitudinal section through several serous glands. The
apex of each secretory cell contains a n abundance of densely stained
serous granules. A clear cell (possibly a plasma cell precursor) is indicated by the arrow. Several skeletal muscle fibers are present in the
connective tissue matrix in which the glands are embedded. Methylene blue-azure 11. x 440.
Fig. 3. Longitudinal section through a gland near the posterior border of the zone of plumose papillae. The arrow indicates a cluster of
three mucous cells within the glandular epithelium, which is still
overwhelmingly serous in nature. Methylene blue-azure 11. x 375.
Fig. 4. Longitudinal section through a lingual gland that is predominantly mucous in nature. A few serous cells remain at the blind end
of the gland; arrows indicate the point where the cells change in
nature-mucous cells are above the arrows, and serous cells, below.
This gland is almost at the line of demarcation between the two zones,
respectively characterized by plumose papillae and by cylindriform
papillae. Methylene blue-azure 11. x 480.
The tall, prismatic serous cells have a smooth base
that is linked to the basal lamina by hemidesmosomes,
lateral processes that interfoliate with similar processes from adjacent cells, and a luminal surface that
has numerous microvilli, including some bifid forms. A
prominent junctional complex marks the apical perimeters of these secretory cells. Each cell has a single,
irregularly shaped nucleus that invariably is situated
at the base of the cell (Fig. 5). Lateral to and for some
distance above the nucleus there is a well-developed
rough endoplasmic reticulum (RER). A large Golgi
zone with an unusual-appearing Golgi apparatus surmounts the RER and seems to bisect the cell (Fig. 5).
Because of the odd structure of the Golgi apparatus, it
is quite difficult to decipher which side is cis and which
is trans. The Golgi apparatus consists of several stacks
of saccules and a closely packed congeries of terminal
dilatations and early condensing vacuoles (Fig. 6). As
the condensing vacuoles mature, their punctate con-
Fig. 6. The Golgi apparatus of a serous cell. Although there are
nPvPral parallel sarcules, it. ronsists mainly of imbricated terminal
dilatations and condensing vacuoles. x 20,000.
tents become somewhat denser and more compacted,
leaving a light peripheral halo. As these prospective
granules continue to develop, the matrix becomes even
denser and the haloes are reduced by accretion of further dense material.
Mature serous granules measuring about 1 pm in
diameter occupy the apical half of each cell. While a t
low magnification these granules appear to be uniformly dense (Fig. 5), at higher magnification many
are seen to show characteristic substructural patterns.
All mature serous granules in the lingual glands have
a dense matrix; embedded within this matrix may be
nodose lucencies arranged in one or two concentric
shells adjacent to the limiting membrane of the granule (Fig. 7). Because individual granules are intersected at random by the knife, numerous designs are
generated (Figs. 8, 9). Secretory granules in the more
posterior serous glands tend to show a cribriform pattern (Fig. 10). Regardless of their structure, serous
granules are delivered to the gland lumen via typical
exocytosis (Fig. 11).
Mucous cells are rather similar to serous cells in
their general organization. The basal nucleus is surrounded by extensive RER and is topped by a prominent Golgi apparatus. Mucous droplets, which measure
up to 1.5 pm in diameter, have a dense, structureless
content and are closely packed together. Many mucous
cells have a deeply scalloped free surface, indicative of
recent exocytosis (Fig. 12).
Our study has shown that the tongue of Anolis carolinensis possesses a large number of tubular glands,
which, because they empty their secretions into the
oral cavity, can be considered to be salivary glands.
These glands apparently produce a copious flow, since
examination of the dorsal surface of the tongue under a
dissecting microscope reveals it to be covered by an
abundant, glistening film of saliva. The saliva secreted
by the Anolis lingual glands probably serves one or
several general functions. The serous cells may be zymogenic and thus be involved in digestion. Alternatively, they may produce odiferous substances that can
influence behavior or territoriality. Mucus from the
mucous glands may be utilized in capture of prey and
in swallowing. Moisture secreted by the lingual glands
may be necessary to maintain the structural integrity
of the plumose cells covering the plumose papillae;
these delicate cells with their large surface area otherwise might quickly become desiccated.
Discharge of secretions from the lingual gland lumina may be brought about by contraction of the skeletal muscle fibers within the papillae. Shortening of
the papillae and the intervening glands would, as a
matter of course, force preformed saliva onto the
tongue surface. In such a case, the papillary muscle
fibers would be functioning in a manner analogous to
that of myoepithelial cells in mammalian salivary
Although the anole lingual glands are salivary
glands, they are very different in histological organization from mammalian salivary glands. The latter organs are organized spatially in a fashion that permits
separation of physiological function-secretory cells
arranged in acini and tubules elaborate an initial saliva, which generally contains a variety of organic molecules and has plasma-like concentrations of electrolytes. As the saliva passes through the duct system,
duct cells modify the saliva by removal and addition of
electrolytes and organic substances (Young and van
Lennep, 1978). In the lingual glands of the American
chameleon, there are no ducts, so that the initial saliva
probably remains unmodified as it passes out of the
In contrast to the lingual glands in Anolis carolinensis, the labial salivary glands of this species are tubuloacinar glands, each of which is connected to the
mouth by its own duct (Aiyama et al., 1985). Moreover,
these glands have typical myoepithelial cells, structures that are lacking in the lingual glands. Thus, the
lingual glands of the American chameleon are very
much simpler in histological organization than are the
labial glands.
Tubular lingual glands occur in a variety of reptiles
[see reviews by Gabe and Saint Girons (1969) and
Kochva (1978)l. According to Kochva (19781, in certain
species, the deeper cells in these glands are mucous,
whereas those closer to the surface are serous. In Anolis, the opposite situation prevails in the mixed lingual glands, with serous cells the deeper and mucous
cells the more superficial. In fact, some of the mixed
glands in the Anolis tongue are reminiscent of mammalian fundic glands, where gastric pits lined by mucous cells are succeeded by gastric glands composed in
part by the serous-type chief cells.
The lingual mucous cells of A. carolinensis closely
resemble mammalian goblet cells in the appearance of
their mucous droplets and in the formation of apical
Figs. 7-9. Serous granules displaying a variety of internal configurations resulting from the plane in which each was sectioned. Fig. 7,
x 16,400; Fig. 8, x 27,800; Fig. 9, x 15,600.
Fig. 10. Secretory granules from a posteriorly situated serous gland.
Granules in this location tend to show a cribriform patterning.
x 18,800.
Fig. 11. An example of a serous granule in the process of exocytosis. x 32,200.
Fig. 12. Mucous cells in glands situated among the cylindriform papillae. These cells clearly have
undergone a round of mucus discharge, as evidenced by their scalloped free surfaces. x 6,200.
channels as a result of exocytosis (Specian and Neutra,
1980). The serous cells are notable because of their
peculiar Golgi apparatus. In this species, nascent granules form a large agglomeration in close relation to the
Golgi saccules. These partially developed granules may
represent a storage form of secretory products. When
mature granules are depleted by exocytosis presumably stimulated by feeding, the nascent granules may
rapidly complete their development to restore the normal complement of secretory granules.
With the exception of those found in the venom
glands of certain snakes (Warshawsky et al., 1973),
serous granules in the relatively few reptilian oral
glands that have been examined by electron micros-
copy tend to be dense and structureless. In contrast,
serous granules in Anolis lingual glands have a distinctive and characteristic substructure. It recently has
been demonstrated that secretory granules in mammalian salivary glands have species-specific internal patterns and that these patterns are related to evolutionary and taxonomic kinships (Tandler et al., 1986;
Phillips and Tandler, 1987; Tandler et al., 1990). Perhaps further study of salivary glands in reptiles, particularly those glands that contain serous cells, may
show that in this class of vertebrates, as in mammals,
granules with substructure are more widespread than
has heretofore been appreciated and that these patterns are not haphazard.
Expert technical assistance was provided by Carol
Ayala and Douglas Johnston. This work was supported
in part by NIDR Grant DE-07648 to B.T. and by NIH
Biomedical Research Support Grant RR-05335.
Aiyama, S., S. Kurabuchi, T. Nagumo, H. Sugiyama, and T. Tsutsumi
1985 Electron microscopic observation on the labial gland of lizard, Anolis carolinensis. Jpn. J . Oral Biol., 27t857-869.
Gabe, M., and H. Saint Girons 1969 Donnees histologiques sur les
glands salivaires des lepidosauriens. Mem. Mus. Nat. Hist. Nat.,
Paris, 58tl-118.
Kalt, M.R., and B. Tandler 1971 A study of fixation of early amphibian embryos for electron microscopy. J. Ultrastruct. Res., 36t633645.
Kochva, E. 1978 Oral glands of the reptilia. In: Biology of the Reptilia,
Val. 8, Physiology B. C. Gans and K.A. Gans, eds. Academic
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Kurabuchi, S., and S. Aiyama 1987 Scanning electron microscopy of
the lingual dorsal surface of Anole Lizard, Anolis carolinensis.
Jpn. J. Oral Biol., 29593-600.
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ultrastructure, carolinense, chameleonanolis, gland, linguam, salivary, american
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