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THE ANATOMICAL RECORD 248:164–175 (1997)
Ultrastructure of the Unusual Accessory Submandibular Gland
in the Fringe-Lipped Bat, Trachops cirrhosus
BERNARD TANDLER,1 TOSHIKAZU NAGATO,2 AND CARLETON J. PHILLIPS3*
1Department of Oral Anatomy II, Kyushu Dental College, Kitakyushu, Japan
2Second Department of Oral Anatomy, Fukuoka Dental College, Fukuoka, Japan
3Department of Biological Sciences, Illinois State University, Normal, Illinois
ABSTRACT
Background: The phyllostomid fringe-lipped bat, Trachops
cirrhosus, is sui generis (in a family of ca. 138 species) in that it subsists in
part on tropical frogs. These amphibians frequently possess highly toxic
integument. We examined the salivary glands of this bat to determine if
these glands could be the source of protective factors that permit consumption of seemingly unsavory prey. The parotid and principal salivary
glands of this bat are similar to homologous glands in other phyllostomids,
but the accessory submandibular gland is unique.
Methods: The accessory submandibular glands of live-trapped T. cirrhosus were fixed and processed for transmission electron microscopy by
conventional means.
Results: The accessory submandibular gland consists of follicles and
ducts. The principal cells of the follicular walls have an abundance of
rough endoplasmic reticulum (RER), free ribosomes, and extensive Golgi
apparatuses. Typically, these cells have relatively few serous secretory
granules. The cells contain collections of peculiar lipid droplets, and some
of their mitochondria have dense crystalloids within expanded cristae. A
layer of irregular, moderately dense bodies lies immediately subjacent to
the luminal plasmalemma; it is not clear if these structures are endocytotic or exocytotic. Clusters of mucous cells, some of which have a single,
hugely distended RER cisterna, are ensconced in the follicular walls;
mucus from these cells reaches the lumen via intercellular canaliculi.
Ducts progress from simple cuboidal to simple columnar epithelium. They
lack basal striations, and their constituent cells contain relatively few
mitochondria. Follicles and ducts have numerous myoepithelial cells at
their periphery, and both are heavily innervated by hypolemmal nerve
terminals.
Conclusions: The unusual accessory submandibular gland in T. cirrhosus documents the extreme modifications in gland histology and in cell
ultrastructure that have occurred in mammalian families. The cells
composing the follicle walls and ducts bear little similarity to typical
acinar or duct cells. Duplication of the submandibular gland in some bat
lineages might be the key innovation underlying such plasticity. The
heavy innervation of both follicles and ducts also implies that these
structures are sensitive to and capable of responding to various inputs,
perhaps including dietary factors. Anat. Rec. 248:164–175, 1997.
r 1997 Wiley-Liss, Inc.
Key words: salivary glands; follicles; lipid droplets; mitochondrial crystalloids; hypolemmal nerves; frogs
Salivary glands may be the most diversified organs in
mammals. This diversification involves histological organization, cell structure, secretory and transport processes, and gene regulation (Phillips and Tandler, 1987;
Phillips et al., 1993) and is important for two principal
reasons. First, most organ systems and, more specifically, most cell types are relatively conservative. Conservatism in cell structure and cellular processes is parar 1997 WILEY-LISS, INC.
doxical in view of the evolutionary plasticity seemingly
required to achieve the diversity found within major
groups of animals (Gerhart, 1995). An unraveling of
*Correspondence to: Carleton J. Phillips, Department of Biological
Sciences, Felmley Hall, Room 206, Illinois State University, Normal,
IL 61761-6901.
Received 23 October 1996; accepted 11 December 1996.
BAT ACCESSORY SUBMANDIBULAR GLAND
this paradox requires an appreciation of the balance
between conservation and plasticity in cells, which can
be gained through comparative data on the patterns
and types of diversification that have occurred in
evolutionary lineages. Second, the multifarious biological roles of mammalian salivary glands place them at
the interface between organism and environment (Phillips and Tandler, 1996). Thus, it has been argued that
an understanding of salivary glands in the context of
diet, dentition, and behavior could lead to greater
comprehension of adaptation (Phillips, 1996).
Accessory submandibular glands are noteworthy because they are common in bats and because they have
the potential for great plasticity. Previously, we found
that the accessory submandibular glands of the phyllostomid fringe-lipped bat, Trachops cirrhosus, display
extraordinary follicular histologic organization (Phillips et al., 1987; Tandler et al., 1996). The fringe-lipped
bat is unusual because it is the only neotropical bat
(even among the ca. 138 species in its family) that feeds
almost exclusively on frogs. Because most tropical frogs
have toxic integument, we hypothesized that the unusual accessory submandibular glands in T. cirrhosus
might be associated with diet.
To test this idea, we examined three additional
species of Asian and African bats known to include frogs
in their diet and found similar histological features in
their accessory submandibular glands (Phillips et al.,
1987; Phillips and Tandler, 1996a). Because T. cirrhosus originated and evolved independently of the Old
World species with similar diets, we concluded that the
follicular salivary glands are an example of convergent
evolution associated with adaptation to a specialized
carnivorous diet (Phillips et al., 1993). The accessory
submandibular gland of T. cirrhosus thus appears to be
a model that can be employed to delineate the kinds of
ultrastructural diversification that can occur in salivary glands in correlation with diet.
MATERIALS AND METHODS
Three specimens, two males and one female, of adult
fringe-lipped bats, T. cirrhosus, live-trapped in Suriname, were anesthetized with T-61 euthanasia solution
and their salivary glands extirpated. Tissues were fixed
in triple aldehyde-DMSO (Kalt and Tandler, 1971) as
modified by Phillips (1985). After postfixation in osmium tetroxide, specimens were soaked overnight in
acidified 0.25% uranyl acetate (Tandler, 1990). Thorough rinsing in distilled water was followed by dehydration in ethanol, passage through propylene oxide, and
embedment in Epon-Maraglas (Tandler and Walter,
1977). Thin sections were stained with acidified methanolic uranyl acetate (Tandler, 1990) followed by lead
tartrate (Millonig, 1961) or lead citrate (Venable and
Coggeshall, 1965) and examined in a Siemens 101 or
JEOL 1200EX electron microscope. Semithin sections
were stained with methylene blue-azure II (Richardson
et al., 1960) and examined in an Olympus Vanox.
RESULTS
The accessory submandibular gland of Trachops consists of large, folliclelike structures corresponding to
the secretory endpieces of conventional mammalian
salivary glands and of ducts. Both of these structures
165
are shown to advantage in Figure 1, a light micrograph
of an epoxy-embedded gland. In a low magnification
electron micrograph (Fig. 2), the secretory follicles are
seen to consist largely of cells with a rich cytoplasm and
which exhibit a band of moderately dense material in
their subluminal zones. Occasional mucous cells are
inserted in the follicle walls, and myoepithelial cells
also may be present; both of these features aid in
distinguishing the accessory submandibular gland from
the look-alike thyroid gland.
The principal cells of the follicular walls have a fairly
high cytoplasmic density. They contain a few scattered
secretory granules and have all of the cytoplasmic
equipment of secretory cells in general, yet they do not
at all look like typical protein-secreting cells, even at
moderate magnifications (Fig. 3). Lipid droplets of
peculiar appearance are abundant in the perinuclear
cytoplasm (Figs. 3 & 4). These have a moderately dense,
ragged inclusion amid a collection of irregular lamellae.
The secretory cells have a modest number of mitochondria of typical structure. Some of these organelles
contain what seem to be dense rods ensconced within
expanded cristae (Fig. 5). At high magnification, these
rods are seen to consist of crystalloids with a 6.2-nm
periodicity (Fig. 6).
When the secretory cells are viewed at higher power,
they are seen to possess an extensive rough endoplasmic reticulum (RER) in the form of cisternal stacks or a
network of tubules and numerous free ribosomes (Fig.
7). Because of the relatively high density of the cytoplasm resulting from the ubiquitous ER and free ribosomes, the Golgi apparatuses usually are difficult to
detect unless their saccules are sectioned diagonally, in
which case the intrasaccule spaces are exaggerated and
the organelle stands out in a sort of ‘‘negative image’’
(Fig. 8). Some Golgi apparatuses are surrounded by
small, dense granules (pro-granules?), presumably secretory in nature (Fig. 9). These apparently increase in
size, perhaps by fusion, to form mature secretory
granules of high density (Fig. 10) that measure about
0.9 µm in diameter.
Immediately below the apical membrane are many
irregular membrane-delimited bodies whose matrix
exactly matches the luminal content in density (Fig.
11). These bodies may contain one or several inclusions
in the form of a twisted, lucent ribbon edged by a linear
density (Fig. 12) or else may contain a small lipid
droplet. Such bodies sometimes are seen open to the
lumen (Fig. 13). Many lucent lipidlike bodies are present in the follicular matrix (Fig. 14); these bodies may
represent lipid of principal cell origin that was liberated into the lumen by an apocrine process. Because the
luminal droplets are considerably larger than the cytoplasmic ones, the latter probably undergo a degree of
fusion once in the lumen.
Gap junctions are fairly common between adjacent
principal cells. These tend to be much larger than
run-of-the mill gap junctions, often measuring up to 3
µm in length and presumably in diameter (Fig. 15).
The occasional mucous cells that make up a small
part of the follicle walls are characterized by the
presence of numerous mucous droplets, which display
the familiar propensity of such secretory products to
fuse with one another (Tandler, 1993b; Fig. 16). These
droplets, which have a diameter of approximately 1 µm,
166
B. TANDLER ET AL.
Fig. 1. Photomicrograph of an epoxy-embedded accessory submandibular gland in T. cirrhosus. Two conjoined follicles (F) contain lightly
stained material in their lumina. Note the layer of light bodies just
beneath the luminal border of the follicular cells. D, duct. The arrow
points to a pair of mucous cells. Methylene blue-azure II. 3650.
Fig. 2. Survey electron micrograph of a small follicle. The lucent
bodies in both the follicular lumen and cells represent lipid droplets.
At the lower right corner, a mucous cell is housed in the follicular wall.
An extremely dense myoepithelial cell (MEC) is at the left of the
follicle. A duct is at the upper left. 32,800.
are of very low density and for the most part are
structureless, but the few droplets that exhibit a compound substructure seem to consist of two hemispheres
of slightly differing texture and density (Fig. 17). Many
of the mucous cells contain a single infra- or para-
nuclear, highly dilated RER cisterna filled with dense,
structureless material (Figs. 18 & 19). Such an expanded cisterna may be larger than the cell nucleus.
Almost no mucous cells reach the lumen of the follicles;
instead, these cells are in direct contact with at least
BAT ACCESSORY SUBMANDIBULAR GLAND
Fig. 3. Survey electron micrograph of a portion of a follicular
wall. Although the cells contain a good deal of RER, they do not
resemble typical secretory cells; only a few dense secretory granules
are present in the apical cytoplasm. Lipid droplets of peculiar
morphology are abundant in the perinuclear cytoplasm. A dense
myoepithelial cell is present at the lower border of the micrograph.
35,000.
167
Fig. 4. Cytoplasmic lipid droplets seen at a higher magnification. These
consist of lamellae and a ragged inclusion of moderate density. 317,100.
Fig. 5. A follicular cell mitochondrion that contains three dense
intracristal crystalloids. 348,000.
Fig. 6. Mitochondrial crystalloids at a high magnification. They
consist of lamellar densities with regular spacing. 3200,000.
168
B. TANDLER ET AL.
Fig. 7. The base of a follicular cell showing its well-organized and
extensive RER. 314,200.
Fig. 8. The Golgi region of a follicular cell. This organelle ordinarily
is masked by the abundant ribosomes and small elements of RER that
impart a high density to the cytoplasm. In this micrograph, however,
the Golgi apparatus has been sectioned diagonally, an orientation that
exaggerates its intrasaccular spaces, so that the obviously extensive
organelle stands out in a sort of pseudonegatively stained background.
A few dense secretory granules are seen in relation to the Golgi
apparatus. 39,500.
Fig. 9. A secretory granule in a follicular cell. It is homogeneously
dense and is delimited by a single unit membrane. Based on its
morphology, this is a serous granule, a designation confirmed by
histochemistry. 384,000.
Fig. 10. A maturing secretory granule associated with a Golgi
apparatus. Many small dense bodies are in this region. It is not clear if
these are pro-granules that will either coalesce to form further
granules or be added to the prospective granule, or if they have some
other fate. 329,300.
Fig. 11. The apical cytoplasm of adjacent follicular cells illustrating
the layer of irregular, moderately dense bodies that underlie the
luminal plasmalemma. 36,400.
Fig. 12. The apical irregular bodies at higher magnification. Two
bodies contain a lucent, twisted ribbon that sporadically is edged with
a linear density. 323,800.
Fig. 13. The apex of a follicular cell. The direction of movement of
organic material cannot be gauged with certainty. In the center is
what appears to be an erumpent secretory granule. It is flanked by
irregular apical bodies that are open to the lumen, but it is not clear
whether the lucent ribbons are being released or being taken up by
these bodies. 323,800.
Fig. 14. A lipidlike body in the follicular matrix. It is edged in part by
a thin layer of dense material. Such droplets probably gain access to
the lumen by apocrine secretion. 319,600.
Fig. 15. A gap junction of unusual length between two follicular
secretory cells. 334,000.
170
B. TANDLER ET AL.
one intercellular canaliculus, the latter structures apparently serving as conduits for mucus (Fig. 20).
The assorted secretory materials (mucus, lipids, protein, lucent ribbons, and membranes) plus cell detritus
that end up in the follicular lumina as a result of
apocrine or merocrine secretion, or both, often undergo
degenerative changes leading to the formation of large
luminal agglomerations that consist of dense lamellae
and various kinds of vesicles and vacuoles (Fig. 21).
These inclusions apparently follow the saliva during its
discharge from the gland.
The walls of the secretory follicles are very highly
innervated, with clusters of hypolemmal nerve terminals abounding (Fig. 22). Nerve clusters are composed
of naked axons and varicosities laden with clear synaptic vesicles; a smaller number of larger, dense cored
vesicles also may be present (Fig. 23).
Myoepithelial cells are arranged around the periphery of each follicle, where they are easily distinguishable from secretory cells by virtue of their high cytoplasmic and nuclear density. These cells continue onto the
ducts unchanged in morphology and are described in
connection with those structures.
Proximal ducts in the Trachops accessory submandibular gland consist of simple cuboidal epithelium
(Fig. 24); more distal ducts consist of simple columnar
epithelium (Fig. 26). In both, the duct cells have
cytoplasm that is considerably less dense than that of
the secretory cells. Duct cell cytoplasm contains scattered cisternae of RER, many polysomes, and some
elliptical mitochondria. The apical cell surface, which
generally is devoid of microvilli, frequently is underlaid
by numerous small vesicles and tubular elements of
ER. Hypolemmal nerve terminals are as abundant in
the duct walls as they are in the secretory follicles.
Where a duct cell overlies a myoepithelial cell or
process, its basal surface may have a number of folds,
but these are more slender than those in typical
striated ducts.
The ductular (and follicular) myoepithelial cells appear to be typical in shape (Fig. 25). Flattened in a
vertical direction, they consist of a perikaryon that
contains the applanate nucleus, the usual cytoplasmic
organelles, and an array of myofilaments. These cells
have long, tapering processes that clasp the contiguous
parenchymal structure, be it duct or follicle; the ‘‘grip’’
of the myoepithelial cell is maintained by desmosomes
that attach this cell to the adjacent epithelial cell.
Nerve terminals frequently occur between a myoepithelial cell perikaryon or process and the neighboring duct
or secretory cell. Such terminals also are abundant
even when no myoepithelial component is present.
We encountered one cell in a duct wall that contained
a plenitude of small, dense granules, giving it the
general appearance of an APUD cell. In addition, this
cell had a few prominent microvilli with extremely long
rootlets, a structural feature reminiscent of brush cells.
This granular cell had an apical dome that bulged into
the duct lumen.
DISCUSSION
That some bats possess a set of accessory submandibular glands has been known at least since the work of
Robin (1881). Robin’s nomenclature was based on size
and position of the respective organs, with the larger
inferior one being called the principal gland and the
smaller superior one being called the accessory gland.
In our continuing large-scale study of the comparative
ultrastructure of bat salivary glands (Tandler et al.,
1990; Phillips et al., 1993), we have encountered many
chiropteran species having two pairs of submandibular
glands. Rather than basing our labels on gross anatomical properties of the organs, we have used microscopically based criteria to sort out principal from accessory
gland. Our convention is to call that gland that exhibits
typical submandibular gland morphology the principal
gland, with the accessory being the gland that differs at
least in some respects from typical submandibular
glands. Although in a few cases the accessory gland
structurally is virtually indistinguishable from the
principal gland (even though it usually shows histochemically detectable differences in glycoconjugates;
Pinkstaff et al., 1982), the usual case is that the
accessory gland exhibits obvious structural (and presumably functional) differences from conventional
glands. The accessory submandibular glands described
here constitute the most extreme departure from the
typical major salivary gland histology yet reported.
The serous secretory cells of Trachops are extremely
unusual. Although they have abundant RER and free
ribosomes, they contain relatively few typical secretory
granules. According to Pinkstaff (1993), these granules
are more perfectly serous in nature than any other
granules he had encountered; in other words, they
contain no glycoconjugates whatsoever. The irregular
bodies at the cell apex may be involved in the uptake of
luminal material. This possibility would account for the
presence within these structures of occasional lipid
droplets and ribbonlike lucent laminae, which are quite
abundant in the colloidlike material. Such activity is
reminiscent of the action by thyroid gland cells that
endocytose thryoglobulin for further processing. The
possibility that these bodies may be involved in exocytosis of secretory material cannot be dismissed out of
hand. If they do in fact release material into the lumen,
they would constitute a novel form of secretory granule.
Some cellular components, especially the unusual
lipid droplets, appear to be released into the lumen by
an apocrine process. The scattered mucous cells also
discharge mucus into the follicles. Once liberated into
the lumen, the secretory material forms a matrix in
which are suspended spicular aggregates of laminae,
membranes, and lipid droplets. The stored secretory
material in the follicles probably is discharged into the
duct system by contraction of the numerous myoepithelial cells positioned at the follicular periphery and then
hastened on its way by contraction of the ductal myoepithelial cells.
Striated ducts constitute a significant segment of the
excurrent duct system in typical submandibular and
parotid glands in almost all mammals (Tandler, 1993b).
These ducts consist principally of tall columnar epithelial cells whose bases are interlocked in a highly
complex fashion (Riva et al., 1993) to form a series of
basal compartments in which elongated mitochondria
reside, the folded plasma membranes and vertically
oriented mitochondria being responsible for the ‘‘basal
striations.’’ These ducts, working in concert with the
excretory ducts (Schneyer et al., 1972), are thought to
be major sites of electrolyte resorption from the isotonic
BAT ACCESSORY SUBMANDIBULAR GLAND
Fig. 16. A cluster of mucous cells in a follicular wall. These cells rest
on the follicular basement membrane but almost never reach the
follicular lumen. 35,900.
Fig. 17. Mucous droplets at a higher magnification. Although most of
the droplets have a farinaceous content, granules cut in the appropriate plane (asterisks) show two distinct hemispheres of slightly differing texture and density. 331,200.
171
Fig. 18. An RER cisterna in a follicular mucous cell. The cisterna is
grossly distended with structureless dense material. 310,500.
Fig. 19. The edge of a distended cisterna in a mucous cell showing
the attached ribosomes that indelibly mark it as an element of the
RER. 357,000.
Fig. 20. Mucous cell bordering an intercellular canaliculus (ICC).
Mucus reaches the follicular lumen via such pathways. 316,800.
172
B. TANDLER ET AL.
Fig. 21. An aggregate of degenerated cellular material in the follicular lumen. It consists of dense lamellae (a form of myelin?) and clear
and dense-cored vesicles. 313,200.
Fig. 22. The periphery of a follicle showing several clusters of hypolemmal nerve terminals, including axons and varicosities. 311,500.
primary saliva, so that the final saliva that reaches the
mouth is hypotonic. Saliva from the human sublingual
glands (Riva et al., 1988) or labial minor salivary
glands (Tandler et al., 1970), both of which have a
paucity of striated ducts, is more or less isotonic.
Although the accessory submandibular gland in T.
cirrhosus has a prominent duct system, striated ducts
Fig. 23. Higher magnification of a cluster of follicular hypolemmal nerve terminals. These varicosities contain mostly clear
synaptic vesicles, with just a few dense-cored vesicles apparent.
328,500.
are noteworthy by their absence. The ducts that are
present have no basal striations, and their complement
of mitochondria seems rather skimpy. Moreover, the
ducts lack any secretory activity (unless the apical,
empty-appearing vesicles are involved in secretion),
and there is no evidence of endocytotic activity at the
luminal surface. At the same time, the ducts are heavily
BAT ACCESSORY SUBMANDIBULAR GLAND
173
Fig. 24. Survey electron micrograph of a small duct. Mitochondria
are randomly distributed in the duct cells. Hypolemmal nerve terminals are indicated by the arrows. The duct lumen contains lipid
droplets and oddments of cell debris, perhaps the result of a form of
apocrine secretion taking place in the follicles. 33,100.
Fig. 25. The perikaryon of a myoepithelial cell in a small duct. The
arrows indicate several hypolemmal nerve terminals in the duct wall.
311,500.
innervated, suggesting that these ducts may play an as
yet indecipherable role in modifying the saliva of the
accessory glands.
From an evolutionary perspective, the accessory submandibular gland in T. cirrhosus calls attention to
three important issues: (a) the significance of duplication of organs, (b) the relationship between salivary
gland structure and adaptation to specialized diets, and
(c) the potential for rapid diversification in secretory
cell structure and cellular processes.
The origin of binary salivary glands is of some
interest. Such twin organs are not necessarily the
result of a long evolutionary descent but may arise
quite suddenly in evolutionary terms. For example, the
bilaterally paired submandibular glands in human
beings normally are single organs. Recently, however, a
case has been reported of a duplicated human submandibular gland, each moiety having it own main excretory duct (Codjambopoulo et al., 1992). Other instances
of duplication of the main excretory duct of the same
gland have been reported (Myerson et al., 1966; Towers,
1971). If such duplications are not simple developmental (epigenetic or somatic) anomalies but are genetically based in the germ line and are functionally
innocuous, they could eventually spread throughout a
population. In the case of bats, accessory submandibular glands are phylogenetically widespread in the suborder Microchiroptera. Thus, such glands seem to be
symplesiomorphic, i.e., share ancestral features. Given
the importance of diet and the great diversification of
dietary habits in the microchiropteran bats (Phillips et
al., 1993), these equally diversified accessory salivary
174
B. TANDLER ET AL.
Fig. 26. A cell in a larger duct. It contains a modest number of mitochondria, which display no
preferential orientation, and some scattered, small, dense granules. There is a network of smoothsurfaced tubular reticulum immediately below the luminal membrane. 39,700.
glands might have been an innovative key to chiropteran adaptive radiation.
In the case of T. cirrhosus, we think that the unique
accessory submandibular gland is related to feeding on
tropical frogs. Typically, the tropical anuran integument is a storehouse of amines, peptides, and alkaloids;
this armamentarium of potentially toxic compounds
provides a chemical defense against predation (Phillips
et al., 1993). The fringe-lipped bat can learn to recognize different species of frogs on the basis of their
vocalizations, thus permitting the bats to select the
least toxic prey (Tuttle and Ryan, 1981). Nevertheless,
the frogs that they end up eating still present a
potential toxicological problem, so it would not be
surprising to find either gastric or salivary modifications that permit the consumption of these normally
inedible frogs. In terms of stomach morphology, T.
cirrhosus is similar to other carnivorous phyllostomid
bats in having a well-developed zone of mucous cells
and numerous mucous neck cells in its gastric glands
(Studholme et al., 1986). However, the absence of
observable specialization of gastric morphology points
the finger at the accessory submandibular gland as the
more important organ in the evolution of frog-eating in
these bats.
Our theory of cells as the centerpiece of adaptation
complexes (Phillips, 1996) calls attention to the importance of extracellular signaling, which provides the
basis for cell interaction with the environment. The
exceptional innervation of the accessory submandibular glands in T. cirrhosus provides morphological evidence of the potential responsiveness of these glands.
At present, we do not know whether the remarkable
number of nerve terminals is a reflection of multiple
independent pathways, is related to a need for multiple
impulses in short time frames, or both. The principal
cells in the walls of the follicles probably were derived
from ancestral acinar cells, possibly from intercalated
duct cells, or from both. In any case, the ultrastructure
of the principal follicular cells provides a measure of the
extent to which ‘‘typical’’ cells can become diversified.
For all practical purposes, the follicle wall cells are
unrecognizable as acinar or ductal cells. Because they
are unique to this species of bat, they possibly originated with this monotypic genus.
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