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Light and Scanning Electron Microscopic Study on the Structure of the Lingual Papillae of the Feathertail Glider (Acrobates pygmeus Burramyidae Marsupialia).

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THE ANATOMICAL RECORD 290:1355–1365 (2007)
Light and Scanning Electron
Microscopic Study on the Structure of
the Lingual Papillae of the Feathertail
Glider (Acrobates pygmeus,
Burramyidae, Marsupialia)
HANNA JACKOWIAK* AND SZYMON GODYNICKI
Department of Animal Anatomy, Agricultural University of Poznan, Poznan, Poland
ABSTRACT
The structure of the tongue of the marsupial feathertail glider (Acrobates pygmeus) was observed under a light and scanning electron microscope. The elongated tongue with a sharpened apex is ca. 10 mm in
length. Only the posterior half of the tongue is attached to the bottom of
the oral cavity by the frenulum, which facilitates considerable mobility of
the anterior free part of the tongue. On the dorsal surface of the tongue,
three types of lingual papillae were distinguished, that is, mechanical filiform papillae and gustatory fungiform and vallate papillae. The arrangement, shape, and size of filiform papillae and the direction of their keratinized processes change depending on the part of the tongue, so that the
surface of the apex and the body of the tongue resembles a brush adapted
to effective holding of semiliquid food and collection of pollen. The fungiform papillae have a single taste bud and are uniformly scattered
between filiform papillae only on the anterior half of the tongue. On the
smooth root of the tongue, three oval vallate papillae are arranged in the
form of a triangle, similarly as it is the case in other marsupials. The posterior biggest vallate papilla is oriented perpendicularly to the smaller
anterior papillae. The results of the study on the feathertail glider show
that the special arrangement of lingual papillae is strongly adapted to
feeding behavior of this nectar-eating and frugivorous animal. Anat Rec,
290:1355–1365, 2007. Ó 2007 Wiley-Liss, Inc.
Key words: tongue; lingual papillae; feathertail glider; marsupials; LM; SEM
The arrangement and structure of gustatory lingual
papillae, responsible for the reception of gustatory sensations, and mechanical lingual papillae, aiding the
transfer of food, documented in vertebrates, constitute
general traits typical of individual taxonomic units, for
example, orders or families (Chamorro et al., 1986; Iwasaki et al., 1987; Iwasaki and Miyata, 1989; Azalli et al.,
1991; Kobayashi and Wanichanon, 1992; Kobayashi
et al., 1995; Kumar et al., 1998; Emura et al., 2000,
2002; Eerdunchaolu et al., 2001; Yoshimura et al., 2002;
Jackowiak and Godynicki, 2004). On the other hand, an
important factor affecting the structure of the lingual
mucosa is the type of ingestion of food, the method of its
grinding in the oral cavity, as well as the method of its
passage to further segments of the alimentary tract.
Ó 2007 WILEY-LISS, INC.
Thus, in comparative studies on morphological traits of
the tongue conducted so far on mammals, the degree of
adaptation of the animals to a given alimentary group,
that is, carnivores, herbivores, or omnivores, is also
investigated (Doran, 1975; Thome, 1999).
*Correspondence to: Hanna Jackowiak, Department of Animal Anatomy, Agricultural University of Poznan, ul. Wojska
Polskiego 71 C, PL 60-625 Poznan, Poland.
Fax: 0048-061-8487623. E-mail: hannaj@au.poznan.pl
Received 17 October 2005; Accepted 10 August 2007
DOI 10.1002/ar.20606
Published online in Wiley InterScience (www.interscience.
wiley.com).
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JACKOWIAK AND GODYNICKI
Figure 1.
1357
LINGUAL PAPILLAE IN THE FEATHERTAIL GLIDER
The object of the investigations in this study is the
feathertail glider, an arboreal marsupial living in eastern Australia, belonging to Burramyids, which is
described as the world’s smallest gliding mammal (Flannery, 1994; Starck, 1995). Among marsupials, the structure of lingual papillae has been investigated so far in
such species as the wombat, wallaby, kangaroo, koala,
and opossum (Kubota et al., 1963; Beg and Qayyum,
1976; Krause and Cutts, 1982; Abe et al., 2001; Kobayashi et al., 2003). Due to the geographic isolation of Australia, marsupials exhibit a wide morphological diversification, depending on the ecological niche they occupy
and their anatomical structure, including also the morphology of the alimentary tract, with features found in
the representatives of orders in Eutheria. Results of previous microscopic observations showed in marsupials
that some characteristics of the structure of the tongue
and the mucosa covering it are closely correlated with
their diet and similar to those found in large ruminants
or carnivores (Kubota et al., 1963; Kobayashi et al.,
2003). Most species belonging to Burramyids are omnivorous, but in the feathertail glider, living in dry sclerophyl forests and woodlands, pollen and nectar feeding is
characteristic (Turner and Mckay, 1989).
In the present study, the aim was to describe the morphology of the tongue in the feathertail glider and examine the distribution and microstructure of lingual papillae on the dorsal surface of the tongue of the feathertail
glider (Acrobates pygmeus) in view of the adaptation to
its diet.
MATERIALS AND METHODS
The study was conducted on 7 tongues of adult feathertail gliders (Acrobates pygmeus), donated by the Zoological Garden in Poznan (Poland). Three dissected
tongues were cleaned in saline and fixed by immersion
in Bouin solution for observations under a light microscope. Fixed samples of the tongue were dehydrated in a
graded series of ethanol (70–99.8%) and embedded in
Paraplast. The 4-mm serial sections were stained with
hematoxylin–eosin (HE) and Masson–Goldner trichrome,
mounted with DPX, and examined under an Axioscope 2
plus microscope (ZEISS, Germany). The morphometric
data were obtained using a KS 400 computer morphometry system (ZEISS, Germany).
Samples from four tongues for scanning electron microscopic (SEM) study were fixed in 10% neutral formalin. After dehydration in an ethanol series, tissues
were processed with acetone, and subsequently dried
at critical point using CO2 (Critical Point Dryer K850,
EMITECH, England). The specimens were mounted on
aluminium stubs covered with carbon tabs, sputtered
with gold (Sputter Coater S 150B, EDWARDS, Eng-
Fig. 1. a: Scanning electron micrograph of the apex (A) and body
(B) of the tongue in the feathertail glider. The surface is covered predominantly by filiform papillae (Fi), which processes are tilted towards
the posterior part of the tongue. Arrows show fungiform papillae. 372;
Scale bar = 200 mm. b: A higher magnification of the surface of the
apex of the tongue in the feathertail glider covered by filiform papillae
with thorn-like processes (Fi); Fu – elongated fungiform papilla. 3566;
Scale bar = 30 mm.
land), and observed under a ZEISS 435 VP (Germany)
scanning electron microscope at the accelerating voltage of 15–20 kV.
RESULTS
The tongue of the feathertail glider has a markedly
elongated lingual body and a short pointed apex (Figs. 1a,
2a). The tongue of the feathertail glider is approximately
9–11 mm long, while the width of the tongue is constant,
amounting to ca. 2.3–2.4 mm. The posterior part of the
root of the tongue, with the length of 2 mm, located under
the pharyngeal–palatal arch, is narrowed to 0.7 mm
(Fig. 4a). Macroscopically, the whole dorsal surface of the
lingual mucosa, apart from the root of the tongue, is covered with papillae, giving it a rough appearance (Figs. 1a,
2a, 3a).
The ventral surface of the mucosa is smooth without
papillae and covered by a multilayered nonkeratinized
epithelium, 40–52 mm in height. No lingual lyssa is
observed. The tongue is connected with the bottom of
the oral cavity in the posterior part of the body of the
tongue by a thin, folded, ca. 1.5–2 mm frenulum of the
tongue.
Apex of the Tongue
On the apex of the tongue, mechanical filiform papillae and gustatory fungiform papillae are found. Filiform
papillae on the sharpened lingual apex in the feathertail
glider are elongated, thorn-like structures (Fig. 1a–c).
They are distributed only in the area within approximately 1.2 mm from the tip of the tongue. The total
height of filiform papillae is ca. 240 mm and the mean
density ca. 158/mm2.
Each papilla has a short base and is split into three to
four processes of identical, ca. 80–135 mm length
(Fig. 1c,d). Processes protruding over the surface of the
tongue are composed only of keratinized cells, forming
scales with a flat surface. There are no microridges on
the surface of horny cells.
Fungiform papillae on the apex of the tongue are
evenly distributed between filiform papillae and have a
markedly elongated basal part, so that the protruding
apex of the papillae is distinctly visible between long
processes of filiform papillae (Fig. 1b–d). The fungiform
papillae are as much as 107–120 mm high, while their
diameter ranges from 65 to 85 mm. The mean density of
fungiform papillae is 20/mm2. The elongated connective
tissue core of the fungiform papilla is covered by a thin
layer of keratinized epithelium, ca. 23–27 mm in height
(Fig. 1d). The keratin layer is 4–5 mm thick. On the dorsal surface of each fungiform papilla only a single taste
bud is observed (Fig. 1d). Taste buds are situated very
deep in the epithelium, so that small taste pores are
very hard to localize between superficial keratinized epithelial cells observed on SEM.
Body of the Tongue
On the body of the tongue of the feathertail glider,
two zones may be distinguished, differing in the
arrangement and morphology of filiform papillae.
The mean density of filiform papillae on the body of
the tongue is 237/mm2. Figures 1a and 2a present filiform and fungiform papillae covering the dorsal surface
1358
JACKOWIAK AND GODYNICKI
of the anterior part of the body of the tongue, reaching
approximately up to three-quarters the length of the
tongue (Figs. 1a, 2b). Filiform papillae of this region of
the tongue are higher than papillae located on the
apex, as the total height of papillae is ca. 370 mm.
From the base of papilla rise three to four flattened
processes with pointed tips, which are tilted toward the
back of the tongue (Fig. 2b,c,e). A single posterior process is dominant in size, while two or sometimes three
lower anterior processes overlap it. The structure of
the multilayered epithelium differs in the anterior and
posterior processes. (Fig. 2d). Anterior processes are in
fact thin laminae formed of a homogenous keratin
layer.
The structure of the epithelium on the posterior process of filiform papillae differs on both sides. On the anterior surface of this process, the epithelium has a
clearly visible cornified layer with cells containing keratin granules. On the posterior surface of processes, the
keratin layer of the epithelium is a homogenous lamina
(Fig. 2d). The surfaces of superficial cells on the anterior
and posterior side of the processes are flat or occasionally small hollows are present (Fig. 2f). The dimensions
of filiform papillae in the medial part of the tongue are
as follows: the length of the posterior process ranges
between 78 and 114 mm, while the length of anterior
processes is 57–71 mm, respectively. The width of the
base of filiform papillae is 30–47 mm. At the margins of
the body of the tongue, anterior processes of filiform
papillae are generally slightly wider and lower than in
the papillae located in the medial part of the body of the
tongue (Fig. 2c).
Both on the apex and the body of the tongue the mucosal epithelium covering the interpapillary areas is parakeratinized and its thickness ranges from 100 to 120
mm. On the surface of cells in this epithelium, which
retain cellular nuclei, there is a labyrinth-like pattern of
microridges.
Fungiform papillae on the body of the tongue are ca.
120–140 mm in height and their diameter is ca. 57–71 mm.
The density of fungiform papillae is 9–11/mm2. The
papillae are uniformly distributed between filiform
Fig. 2. a: Scanning electron micrograph of the surface of the anterior part of the body of the tongue in the feathertail glider. Between filiform papillae numerous fungiform are observed (arrows). Arrowheads
show the position of post mortal impression of palatine rugae. 374;
Scale bar = 200 mm. b: Scanning electron micrograph of the surface
of the body of the tongue in the feathertail glider. Round fungiform
papillae (Fu) are surrounded by filiform papillae with 3–4 flattened
processes. 3400; Scale bar = 50 mm. c: A higher magnification of the
margin of the body of the tongue in the feathertail glider. The filiform
papillae have a short anterior processes (A); P – posterior processes
of the filiform papilla. 3862; Scale bar = 20 mm. d: A higher magnification of the middle area of the body of the tongue in the feathertail
glider. Anterior processes of filiform papillae are elongated; P – posterior
process of the filiform papilla. 3862; Scale bar = 30 mm. e: A higher
magnification of the surface of fungiform papilla in the body of the
tongue in the feathertail glider. Between borders of epithelial cells no
pores of taste buds were noted. Fi – tips of processes filiform papilla.
31850; Scale bar = 10 mm.
LINGUAL PAPILLAE IN THE FEATHERTAIL GLIDER
Figure 2. (Continued from the previous page).
1359
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JACKOWIAK AND GODYNICKI
Figure 3.
LINGUAL PAPILLAE IN THE FEATHERTAIL GLIDER
papillae (Fig. 2b). On the dorsal surface of fungiform
papillae also only one taste bud is found.
In the posterior part of the body of the tongue, in the
area of approximately 2 mm in front of the root of the
tongue, the arrangement and structure of filiform papillae change radically. Figure 3a presents two groups of
filiform papillae, on the left and right side of the tongue,
the bases of which are situated lateral and the apexes
of the papillae tilted perpendicular to the median line of
the tongue. Each filiform papilla is divided already at
the short base into two to four narrow, keratinized processes, reaching as much as 166–291 mm in length (Fig.
3b). The mean density of these papillae is 130/mm2. The
SEM of the surface of the keratinized processes shows
horny scales coiling around the axis of the process and
desquamate as horny tubules (Fig. 3c). No fungiform
papillae are observed between these filiform papillae.
On both edges of the posterior part of the tongue,
where filiform papillae adjoin the smooth lateral surface
of the tongue, papillae resembling the fungiform type
due to their shape and convex surface are found (Fig. 3b).
On the cross-sections of the epithelium covering those
papillae taste buds are not observed, which may indicate
that they may be reduced, undivided filiform papillae.
1361
340 mm. Taste buds are distributed in the epithelium of
the body of papillae on the bottom of the groove (Fig.
4c). Single taste buds are present also near the dorsal
surface of the body of posterior vallate papillae
(Fig. 4d,e).
Vallate papillae, similarly to the root of the tongue,
are covered by a parakeratinized epithelium (Fig. 4c,f).
As is case of the epithelium in the interpapillary areas
of the previous parts of the tongue, SEM observations
reveal the presence of microridges on the surface of superficial cells (Fig. 4g). The thickness of the multilayered
epithelium covering the surface of vallate papillae is ca.
60–63 mm and on the root of the tongue it is 70–93 mm.
DISCUSSION
The mucosa of the root of the tongue in the feathertail
glider is smooth and devoid of mechanical papillae (Fig.
4a). On the surface of the root of the tongue, three oval
papillae are found together with openings of lingual papillae (Fig. 4a,e). Vallate papillae are arranged in the
form of a triangle (Fig. 4a). Two smaller anterior vallate
papillae are distributed symmetrically on the left and
right side of the root of the tongue (Fig. 4a,b). The larger
diameter of the body of the papillae is 94–100 mm, while
the smaller is ca. 58 mm.
The third, largest vallate papilla is located centrally
in the posterior part of the root of the tongue (Fig. 4a).
The longer axis of this papilla is located perpendicularly
to the anterior vallate papillae. The larger diameter of
the body of this papilla is 320–340 mm, while the smaller
is 200 mm. All the vallate papillae are surrounded by a
continuous groove, and the pad of each papilla is flat or
slightly protruding over the surface of the mucosa (Fig.
4a,b,d). The height of vallate papilla ranges from 280 to
To date, results of morphological studies of the tongue
of marsupials indicate that there is no taxonomic relationship among marsupial species, and the primary factor is the kind of food. Thus, the tongues in individual
species are characterized, for example, by a varied shape
and relief of the dorsal surface of the mucosa and the
muscular coat of the tongue. Hence, the described
shapes of the tongue adopt from ovoid up to elongated
with a rounded or sharp-ended tip, and on the surface of
the tongues in the herbivorous species, such as the koala
and gray kangaroo, there are various protrusions are
observed on the lingual body, resembling lingual prominence in great ruminants (Kubota et al., 1963; Krause
and Cutts, 1982; Kobayashi et al., 2003). The structural
variation on the dorsal surface of the tongue in Marsupialia is found also in the distribution of lingual papillae, variation of types of papillae and their microstructure.
Our study on the feathertail glider revealed structural
adaptations of the tongue, which are closely related with
the feeding behavior of this nectar-eating and frugivorous species. A typical method of food uptake in these
animals is licking of honeydew, eucalyptus pollen, fruit
exudates and/or scraping fruit pulp, and feeding on
arthropods such as lerps, soft-bodied termites, or white
ants (Turner, 1984; Turner and Mckay, 1989; Goldingay
and Kavanagh, 1995). Under keeping conditions of the
Zoological Garden, artificial feed for feathertail gliders
are mixed chopped fruits, honey, lactogen, baby cereal,
moths, and fresh high nectar flowers, if available.
Fig. 3. a: Scanning electron micrograph of the posterior part of the
body of the tongue in the feathertail glider. Arrows show the direction
of arrangement of filiform papillae. R – smooth root of the tongue with
two anterior vallate papillae (V). 372; Scale bar = 200 mm. b: A higher
magnification of the right margin of the posterior part of the body of
the tongue in the feathertail glider. Arrows show fungi- and conical-like
papillae on border of filiform papillae distributed along the border
of the smooth lateral and dorsal surface of lingual mucosa covered
with filiform papillae with elongated processes (Fi). 3295; Scale bar =
100 mm.
Fig. 4. a: Scanning electron micrograph of the surface of the root
of the tongue in the feathertail glider. Vs – small, anterior vallate papillae; Vl – large posterior vallate papilla; Fi – filiform papillae of the posterior part of the lingual body; A – parts of dissected palatoglossal
arch. Arrows show opening of lingual glands. 3100; Scale bar =
200 mm. b: A higher magnification of the small anterior vallate papilla
surrounded by a scarcely visible mucosal pad (P). B – oval body of
vallate papilla; Fi – filiform papillae; Arrows show reduced filiform
papillae on the border of the body of the tongue; 3355; Scale bar =
100 mm. c: A higher magnification of the large posterior vallate papilla
surrounded by flat mucosal pad (P). B – oval body of vallate papilla;
insert mark pores of the taste bud. 3355; Scale bar 100 mm. d: A
higher magnification of the insert from Fig. 4C. The arrow shows pores
of a taste bud on the dorsal surface of the body of the papilla (B). P –
pad of the papilla. 31910; Scale bar = 10 mm. e: A higher magnification of the smooth surface of the root of the tongue in the feathertail
glider with round opening of lingual glands. Arrows show the surface
of cornified epithelial cells with characteristic pattern of microridges.
34150; Scale bar 5 5 mm.
Root of the Tongue
1362
JACKOWIAK AND GODYNICKI
Figure 4. (Continued from the previous page).
LINGUAL PAPILLAE IN THE FEATHERTAIL GLIDER
Figure 4. (Continued from the previous page).
1363
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JACKOWIAK AND GODYNICKI
It needs to be noted that characteristic behavior in
these animals is frequent self-grooming, mainly using
claws, but during this procedure pollen gathered on the
fur is mixed with saliva and the tongue transfers it to
the mouth (Turner and Mckay, 1989). We have found
that the macro- and microscopical features of the tongue
contribute to the effective performance of these activities. In this respect, a long frenulum of the tongue
needs to be mentioned, reaching to half of the tongue,
thus increasing mobility and manipulation ability of the
tongue.
The dorsal surface of the tongue in the glider is characterized by numerous, densely arranged mechanical
papillae represented only by filiform papillae. In the
feathertail glider, the variability of structure of filiform
papillae is connected with the shape and length of keratinized processes of filiform papillae. Light microscopic
and SEM micrographs of the epithelium covering processes of the filiform papillae show that it presents the
commonly observed in mammals dual pattern of keratinization, where cells produce soft and hard keratin,
determining the biomechanical qualities of filiform papillae such as hardness, but also a specific elasticity
(Farbman, 1970).
A unique feature, which has not been reported so far
in marsupials or any higher groups of mammals and
which in our opinion results from the influence of the
increased adhesability of semiliquid food, is the arrangement of filiform papillae on the whole surface of
the tongue in three directions. The presence of filiform
papillae directed perpendicularly to the median line of
the tongue may canalize the food into the root of the
tongue before the passage to the pharynx. A comparison of the types, distribution, and structure of mechanical papillae in the feathertail glider and other Marsupials shows great differences. In the previously investigated marsupials, filiform papillae usually resemble
lingual papillae in carnivores. Both in the koala and in
the opossum filiform papillae are composed of a large
main posterior process and several slender long anterior processes (Kubota et al., 1963; Krause and Cutts,
1982; Kobayashi et al., 2003). In the abovementioned
species, apart from filiform papillae on the tongue also
conical papillae were observed, whereas in the koala,
they are found in the posterior part of the tongue, as
in carnivores, and in the opossum they form a specific
patch in the anterior part of the lingual body. The
processes in all of these papillae are oriented only
posteriorly.
Gustatory papillae in the feathertail glider are represented by fungiform and vallate papillae. The arrangement of uniformly scattered fungiform papillae between
filiform papillae in the feathertail glider is also found in
other marsupial species (Sonntag, 1924; Kubota et al.,
1963; Krause and Cutts, 1982; Kobayashi et al., 2003;
Thome, 1999). However, a typical feature of this nocturnal species is their distribution limited only to the anterior half of the tongue, what may be connected with the
need for enhanced perception of substances in the
ingested food. It is important to note the greater density
of fungiform papillae on the apex of the tongue. Additionally, in fungiform papillae, we observed only a single
taste bud, which so far has been considered typical of
certain rodents (Miler and Preslar, 1975; Grandi et al.,
1994; Jackowiak and Godynicki, 2005).
The occurrence of three vallate papillae, differing in
size and arranged in the form of a triangle, found in the
feathertail glider, is a feature commonly observed in all
marsupials (Kubota et al., 1963; Krause and Cutts,
1982; Abe et al., 2001; Kobayashi et al., 2003). However,
if we compare the morphology of vallate papillae in marsupials it turns out that their shapes are species-specific.
According to Kobayashi et al. (2003), in the koala, round
or slit-like vallate papillae are found with a distinctly
marked pad of papilla. In the opossum and kangaroo
bodies of papillae, similarly as in the feathertail glider,
are rounded (Krause and Cutts, 1982). Among mammals
the arrangement of three vallate arranged in the form of
a triangle is found only in bats (Azalli et al., 1991;
Emura et al., 2002). A rare feature among mammals,
found in the feathertail glider, is the occurrence of pores
of taste buds not only in the bottom of the papillary
groove, but also near the dorsal surface of the body of
the posterior vallate papilla, which may also be an element facilitating tasting of food.
Despite that in Acrobates and other species of marsupials Sonntag (1925) describes the occurrence of the socalled lateral organ, which is analogous to the foliate
papillae in other mammals, in our investigations on the
posterolateral surface of the tongue, we did not observe
either the presence of any structures that could point to
the presence of foliate papillae or any slits, commonly
found in marsupials, which are the places releasing the
secretion of lingual glands.
In conclusion, observations on the tongue in the feathertail glider showed a unique pattern of the distribution
of the lingual papillae, well-adapted to the efficient
ingestion of liquid or comminuted food. Analogous studies on other species may show how frequent and typical
this pattern is in other nectar-eating and frugivorous
animals. The premise for this statement can be the
occurrence of such an arrangement of filiform papillae in
a frugivorous Egyptian Fruit Bat (Rousettus aegyptiacus), where the arrangement of elongated filiform papillae in the posterior part of the body of the tongue is similar as in the feathertail glider, while between filiform
papillae scarce fungiform papillae are reported (Jackowiak et al., 2006).
ACKNOWLEDGMENTS
Authors thank Dr. Paweł Botko and Dr. Ewa Trze˛sowska from Zoological Garden in Poznan for supplying the
specimens for the research and discussion about the
biology of the feathertail glider. We also thank Mrs.
Katarzyna Jackowiak for excellent technical assistance.
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papilla, feathertail, light, electro, glider, burramyidae, acrobates, structure, pygmeus, stud, microscopy, linguam, scanning, marsupialia
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