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Zoologica
DORSAL-SURFACE-OF-HAZEL-DORMOUSE-TONGUE
Poloniae
(2014) 59/1-4: 35-47
35
DOI: 10.2478/zoop-2014-0004
DORSAL SURFACE OF THE TONGUE OF THE HAZEL
DORMOUSE MUSCARDINUS AVELLANARIUS:
SCANNING ELECTRON AND LIGHT MICROSCOPIC
STUDIES
K ATARZYNA W O£CZUK
Laboratory of Histology and Embryology of Vertebrates, Faculty of Biology and
Environment Protection, Nicolaus Copernicus University, Lwowska 1, 87-100 Toruñ,
Poland, e-mail. [email protected]
Abstract: The dorsal surface of a hazel dormouse tongue was examined by
scanning electron and light microscopy. The tongue of the hazel dormouse is elongated
and widened in the proximal part. On the proximal one-third of the tongue a clear
median groove is observed. The dorsal lingual surface was covered with five types of
papillae: filiform, conical, fungiform, vallate and foliate. The arrangement, shape, size
and direction of the filiform papillae vary depending on the region of the tongue. On
the proximal part of the tongue, the filiform papillae are saw-like and tilted
medioposteriorly, while on the distal part they have a fork-like shape and form a radial
pattern with their processes oriented towards the center of the tongue. Fungiform
papillae with single taste buds are evenly scattered on the anterior and middle part of
the tongue body. On the root of the tongue, three star-like shaped vallate papillae are
arranged in the form of a triangle and surrounded by conical papillae. A pair of foliate
papillae are found on both edges of the posterior area of the tongue, forming three
parallel folds separated by deep grooves. The dorsal surfaces of the vallate and foliate
papillae are covered with hard-cornified epithelium, while the lateral surfaces have noncornified epithelium with numerous taste buds. The results of our studies show that
the tongue structure of the hazel dormouse is more primitive in comparison with other
rodents which is related to their phylogeny and feeding habits.
Key words: lingual papillae, tongue, hazel dormouse
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INTRODUCTION
The tongue plays a particularly important role in the digestive process.
The organ participates in food intake and mastication and, due to the presence
of gustatory papilla, it also participates in the perception of taste stimuli. Due
to the variety of forms in which it occurs, the tongue has become an object of
many studies aimed at presenting the dependence between its morphological
structure and histology and animal adaptation to the environment and food
(E MURA et al. 2008, 2009, PASTOR et al. 2008, Y OSHIMURA et al. 2008, 2009).
Research has shown that the general structure of the tongue is similar in
all mammals and that existing differences between the species concern its shape
and size, and the structure of the oral mucous membrane in the dorsal area of
the organ (I WASAKI 2002, K OZ£OWSKA et al. 2005, J ACKOWIAK et al. 2009).
In studies of the tongue, considerable attention has been devoted to the
spatial structure of the lingual papillae in mammals, including rodents such as
rats (B ARATZ and F ARBMAN 1975, L IU and L EE 1982, I INO and K OBAYASHI 1988,
I WASAKI et al. 1997, N ASR et al. 2012), mice (KOBAYASHI et al.1989, L IU and L EE
1992, TOPRAK 2006), hamsters (KITAYIMA and KOBAYASHI 1992), guinea pigs (KAWANO
1983, KOBAYASHI 1990), flying squirrels (EMURA et al. 1999a), bank voles (JACKOWIAK
and G ODYNICKI 2005), Japanese grass voles (E MURA et al. 1999b), nutria (EMURA
et al. 2001), American beavers (S HINDO et al. 2006), capybaras (WATANABE et al.
2013) and porcupines (D INC et al. 2010, A TALAR and K ARAN 2011). Considerable
differences have been noted with regard to the number, type and arrangement
of mechanical and gustatory papillae on the dorsal surface of the tongue. It has
become clear that the tongue shape is not only strongly correlated with the
taxonomy of the animal but also its lifestyle and feeding habits (J UNG et al. 2004,
C UCCIO et al. 2010).
Therefore, structural studies of the tongue are extremely important both
from the functional morphology and evolutionary points of view.
The purpose of this study was to describe the morphological and histological structure of the tongue of the hazel dormouse (Muscardinus avellanarius)
in the light of its food habits and taxonomic position. This species is classified
in the family Gliridae whose origin still gives rise to many questions. Furthermore, opinions concerning the diet of these animals are divided. Therefore,
becoming familiar with the structure of the hazel dormouse tongue will be a
valuable contribution to the understanding of the biology of the species.
MATERIALS AND METHODS
Studies were conducted on the tongues of five hazel dormice, Muscardinus
avellanarius (Rodentia, Gliridae), specimens. The animals were caught in Borecka
Forest between 2005-2008 (permit No. DOPog – 4201-04-135/05/aj issued by the
Ministry of Environment of the Republic of Poland). Observations were performed using a scanning electron microscope (SEM) and a light microscope
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(LM). Tongues were fixed in 10% buffered formalin. The histological preparations for LM analysis were prepared using the paraffin method. The tissue was
dehydrated in a graded series of ethanol (70-99.8%) and embedded in paraffin.
The paraffin blocks were cut using a rotary microtome HM 355 S (Microm) into
serial sections 5 to 7 µm thick. The obtained sections were stained with Delafield’s
haematoxylin and alcoholic eosin.
For the SEM observation, fixed material was dehydrated in a series of
ethanol and acetone solutions, sputtered with an ultra-thin layer of gold and
observed using a LEO 1430 VP (England) microscope at the accelerating voltage
of 18.08 kV.
Morphological observations were conducted using the SEM while the
histological analysis and measurements of the mucous membrane structures
were performed using an LM Olympus CX31 light microscope with a calibrated
measuring eyepiece. The measurements were carried out at 40x, 100x and 400x
magnification. The thickness of the cornified and cellular layer of the epithelium
covering the dorsal part of the tongue and the height/length and width/diameter
of the lingual papillae were also measured. Subsequently, the average and standard deviations were calculated.
RESULTS
Shape and size of the tongue
The tongue of the hazel dormouse is spatulate in shape with a considerably elongated body and a widened apical part. The total length of the tongue
is ca. 6.45 mm, while its width, depending on the area, is as follows: 2.11 mm in
the apical part, 2.45 mm in the anterior part of the body, 2.21 mm in its middle
and 2.55 mm at the root. The dorsal area of tongue contains a clearly marked
median groove which extends from the apex up to one-third of the tongue body.
Filiform Papillae
Filiform papillae are the most numerous papillae on the entire dorsal surface of the tongue apex and body forming a dense shell. The single process
of each filiform papilla, except for those papillae situated at the posterior part
of the lingual body, is tilted medioposteriorly. In the posterior part of the lingual
body, the filiform papillae form a radiant pattern with their processes oriented
towards the center of the tongue (Fig. 1c). The shape and length of the filiform
papillae vary depending on the region of the tongue. The apex is covered with
saw-like filiform papillae with two shallow groves in its apical part (Fig. 1a). The
average length of the papillae is 225.50 ± 32.42 µm with the width in the range
of 108.50 ± 13.42 µm. The filiform papillae covering the distal part of the tongue
body are longer (241.83 ± 19.51 µm) and wider (118.16 ± 12.59 µm) than those
on its apex and have a fork-like shape with 2-3 deep groves in the apical part
(Fig. 1b).
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Fig.1 Lingual papillae on the dorsal surface of the apex and body of the tongue in
the common dormouse. a Saw-like filiform papillae on the lingual apex (SEM,
Bar = 20 µm) b Fork-like filiform papillae on the distal part of the lingual body
(SEM, Bar = 20 µm) c Radiant pattern of the filiform papillae on the posterior
part of the lingual body (SEM, Bar = 200 µm) d Hill-shaped fungiform papilla (Fu)
and filiform papillae (Fi) on the lingual body (SEM, Bar = 20 µm).
Fig.2 Lingual papillae on the dorsal surface of the root of the tongue in the common
dormouse. a Three star-shaped vallate papillae (Va), conical papillae with rounded apex
(rCo) on the middle part of the lingual root, conical papillae with pointed apex (Co)
on the posterior and lateral parts of the lingual body, von Ebner glands openings
(arrows) in the distal vallate papilla (SEM,. Bar = 200 µm) b Cross-section trough the
vallate papilla. Cornified epithelium (Ec), non cornified epithelium (Enc) with taste
buds (arrows), conical papillae (Co) (LM, H-E, Bar = 100 µm)
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Fig.3 Lingual papillae on the posterolateral surface of the tongue in the common
dormouse. a Three parallel folds (Fo) separated by deep groves (arrows) of the
foliate papilla, conical papillae (Co) (SEM, Bar = 100 µm) b Cross-section through
the foliate papilla. Cornified epithelium (Ec), non cornified epithelium (Enc) with
taste buds (arrows), excretory duct of von Ebner gland ( * ), conical papillae (Co)
(LM, H-E, Bar = 100 µm)
Conical Papillae
The middle part of the root of the tongue contains small conical papillae
with single rounded processes (Fig. 3a). Their respective dimensions are as
follows: length - 151.17 ± 18.02 µm, width - 93.00 ± 11.81 µm. The posterior and
lateral parts of the tongue root are lined with large sharply ended papillae
whose length extends to 300.40 ± 28.32 µm, and width 150.41 ± 18.36 µm (Figs. 2a
and 3a). The papillae situated in the lateral part of the root are tilted
medioposteriorly (Fig 3a).
Fungiform Papillae
Fungiform papillae are evenly scattered on the apex as well as the anterior
and middle part of the tongue body. They are few in number – 22 ± 2. Fungiform
papillae are hill-shaped and their size ranges from 134.75 ± 23.96 µm in height
and 64.75 ± 5.33 µm in diameter in the apex of the tongue up to 138.50 ± 10.75 µm
in height and 64.75 ± 5.33 µm in diameter in the body of the tongue (Fig. 1d).
Each fungiform papilla has one taste bud situated in the epithelium of the apical
part of the papillae. The dimensions of the taste buds are as follows: height 33.18 ± 6.72 µm, diameter - 26.14 ± 5.29 µm.
Vallate Papillae
There are three vallate papillae, two of which are symmetrically situated on
both sides of the front part of the root, while one papilla is situated in the
midline of the distal part of the tongue root (Fig. 2a). Each papilla has a starlike shape and an uneven, folding surface (Fig. 2a). All vallate papillae are
similar in size: their larger diameter parallel to the long axis of the tongue ranges
from 236.01 up to 309.13 µm, while the smaller one ranges from 209.03 to 272.21 µm.
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The dorsal part of the papillae is lined with a hard-cornified stratified squamous
epithelium (Fig. 2b). The taste buds are situated in the non-cornified epithelium
on the lateral surface of the papillae (Fig. 2b). The taste buds are not observed
on the lateral walls of the groove surrounding the papillae (Fig. 2b). On the
dorsal surface of the vallate papilla located in the distal part of the root of the
tongue, there are two von Ebner gland openings (Fig. 2a).
Foliate Papillae
Foliate papillae are situated on both edges of the posterior area of the
tongue. They are arranged in three parallel folds 305.00 ± 34.22 µm high and
263.75 ± 37.39 µm wide and separated by deep grooves (Fig. 3a). The dorsal
surface of the folds is covered with a hard-cornified epithelium, while the epithelium of the lateral walls of the folds is non-cornified and contains numerous
taste buds (Fig. 3b). The bottom parts of the grooves contain von Ebner gland
openings (Fig. 3b).
Interpapillary Area
The dorsal part of the tongue is covered with cornified stratified squamous
epithelium. The total thickness of the epithelium increases in size from
46.00 ± 3.94 µm in the apical part of the tongue, and 52.25 ± 10.10 µm in the
body, up to 58.25 ± 9.86 µm at the root. The thickness of the cornified layer is
similar in all tongue regions and is 14.25 ± 1.21 µm at the apex, 14.00 ± 2.93 µm
in the body and 14.25 ± 4.57 µm at the root. The largest percentage of the
cornified layer in terms of the total thickness of the epithelium is observed in
the apical part of the tongue (30.98%), while the root of the tongue has the
smallest percentage (24.46%).
DISCUSSION
In the world of mammals, there is a considerable variety of tongue shapes
which are strongly correlated with animal food preferences. In general, there are
two main types of tongue shape: fleshy tongues which are wide and flat; or,
narrow and cone-like tongues (IWASAKI 2002, K OZ£OWSKA et al. 2005). The hazel
dormouse’s tongue, with its spatulate shape and considerable body length, can
be classified, as in other rodents, as the first type of tongue. The characteristic
feature of the hazel dormouse’s tongue is the long and distinct median groove
running along it’s anterior part. The literature on this subject provides multiple
examples of the median groove as being a generally prevailing structure in many
rodent species, such as rats, mice, hamsters and bank voles, although its length
and width seems to be species-specific (G RANDI et al. 1994, I WASAKI et al. 1996,
I WASAKI et al. 1997, J ACKOWIAK and G ODYNICKI 2005).
The dorsal part of the hazel dormouse’s tongue contains five types of
papillae: filiform and conical papillae which are classified as mechanical papillae
and fungiform, vallate and foliate papillae which participate in gustation. The
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hazel dormouse’s filiform papillae densely cover the dorsal part of the apex and
body of the tongue. They present two morphologically distinct types: wide and
saw-like in the anterior part of the tongue and slim, fork-shaped in the posterior
part of the tongue. Both of these types of filiform papillae have one process as
in filiform papillae observed in other rodents (IINO et al. 1988, J ACKOWIAK and
G ODYNICKI 2005); however, they are more differentiated in shape and size in
comparison with the filiform papillae in other representatives of Rodentia. The
orientation of the filiform papillae is also noteworthy. The majority of them are
medioposteriorly oriented; however, in the back part of the tongue they are
radially arranged with their apexes oriented towards the central part of the
tongue. This characteristic arrangement of the filiform papillae has never been
described with regard to other rodent species. They are reminiscent of the
arrangement of the filiform papillae occurring in the tongue of the fruit eating
bat Rousettus aegyptiacus (J ACKOWIAK et al. 2009, A BUMANDOUR and E L -B AKARY
2013). This similarity in the tongue structure between the representatives of two
different taxa may have a functional background. It probably results from the
fact that before the food is swallowed, it is directed with the saliva to the
posterior part of the tongue body where it is gathered on the midline. It is
possible that the liquid fraction of the food for which this part of the tongue
forms a peculiar trough is collected mainly in this way.
The other type of mechanical papillae observed on the hazel dormouse’s
tongue are conical papillae situated on the root of the tongue. A similar papillae
arrangement has also been found in representatives of Sciuridae, such as the
flying squirrel, variable squirrel, and Manchurian chipmunk (K OBAYASHI et al.
1992, R ERKAMNUAYCHOKE et al. 1995, E MURA et al. 1999a), however, in the majority of rodents, their presence is limited to the intermolar prominence (I INO and
K OBAYASHI 1988, K OBAYASHI 1990, G RANDI et al. 1994, J ACKOWIAK and G ODYNICKI
2005). Their main function is to protect the oral mucous membrane while chewing and prevent retraction of the food as it passes towards the esophagus
(S HARMA et al. 1999, I WASAKI 2002).
The hill-shaped fungiform papillae are sparsely scattered on the apex and
anterior part of the hazel dormouse’s tongue body. A similar distribution of the
fungiform papillae has also been observed in another representative of Rodentia, i.e. the bank vole (J ACKOWIAK and G ODYNICKI 2005). The data available in the
literature on the topic show that their arrangement on the tongue is speciesspecific. In Microtus montebelli (E MURA et al. 1999b), rats (MILLER and P RESLAR
1975, D INC et al. 1995), mice (IWASAKI et al. 1996) and nutria (E MURA et al. 2001),
they are abundant on the tongue apex, with diminishing presence on the body
of the organ. In guinea pigs (K OBAYASHI 1990), flying squirrels (E MURA et al.
1999a) and capybaras (WATANABE et al. 2013), they are situated at the apex and
on the lateral margins of the tongue body. In porcupines, these structures are
absent in the apex and occur on the lateral margins of the tongue body (D INC
et al. 2010), but gerbils have them regularly scattered on the tongue body and
root (G RANDI et al. 1994). In the hazel dormouse, as in many other rodents, these
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structures have a single taste bud situated in the middle part of the papilla apex.
Individual taste buds are, among other things, characteristic of rats (M ILLER and
P RESLAR 1975, I INO and K OBAYASHI 1988), hamsters (K ITAYIMA and K OBAYASHI
1992) and bank voles (J ACKOWIAK and G ODYNICKI 2005). However, in capybara
two taste pores have been observed (W ATANABE et al. 2013), and as many as
4-5 (D INC et al. 2010) in porcupines. The data contained in the literature show
that the quantity of taste buds depends on the type of food consumed and it
has to be noted that fungiform papillae occurring on the tongue of herbivores
are particularly abundant in these structures (A SAMI et al. 1995, I NATOMI and
K OBAYASHI 1999, N ONAKA et al. 2008).
The root of the hazel dormouse’s tongue contains another type of gustatory papillae, i.e. vallate papillae. Similar to Sciuridae (KOBAYASHI et al. 1992,
R ERKAMNUAYCHOKE et al. 1995, E MURA et al. 1999a, Ü NSALDI 2010), the hazel
dormouse has three vallate papillae situated in a triangular arrangement with the
base oriented towards the tongue apex. In other rodents, the number of papillae
ranges from one in Cricetidae (K ITAYIMA and K OBAYASHI 1992, J ACKOWIAK and
G ODYNICKI 2005) and Muridae (MILLER and P RESLAR 1975, I INO and K OBAYASHI
1988, K OBAYASHI et al. 1989, G RANDI et al. 1994) to two in Cavidae (S ATA 1960,
K OBAYASHI 1990), Myocastoridae (E MURA et al. 2001), Chinchillidae (M ARTINEZ
et al. 2000), Hystridae (D INC et al. 2010, ATALAR and K ARAN 2011) and Spalacidae
(K LINIK et al. 2010). Taking into account the fact that three vallate papillae occur
in Marsupalia (ABE et al. 2001, K OBAYASHI et al. 2003) and some Chiroptera
(J ACKOWIAK et al. 2009, A BUMANDOUR and E L -B AKARY 2013) tongues, i.e. older
mammalian orders, it can be assumed that the hazel dormouse tongue represents
a more primitive type of structure. No doubt, it is related to the taxonomic
position of the hazel dormouse, classified as glirids - one of the oldest extant
rodent families (WILSON and R EADER 2005), as well as to the environment and
feeding habits of this species (K UBOTA 1988, A BUMANDOUR et al. 2013). Atypical,
star-shaped vallate papillae appear as a combination of the conical and vallate
papillae, while the high keratinisation of the epithelium of the dorsal area is
probably aimed at protecting the structure against damage while ensuring smooth
and efficient reception of taste stimuli.
A third type of papillae is observed on the tongue of the hazel dormouse,
i.e. foliate papillae. They are situated on the lateral parts of the tongue root and
have the shape of parallel folds of the mucous membrane separated by deep
grooves. This type of papilla has also been observed in other rodents (KOBAYASHI
1990, K ITAJIMA and KOBAYASHI 1992, G RANDI et al. 1994, J ACKOWIAK and G ODYNICKI
2005, S HINDO et al. 2006), but in the hazel dormouse, the folds making up the
foliate papillae are lined with a thick layer of keratinised epithelium which
protects the mucous membrane of the papillae during chewing. The presence of
a number of taste buds on the lateral walls allows gustation and provides
information on the type of food being crushed or munched by the molars
(I WASAKI , 2002). In some mammalian species such as koalas, opossums and
common tree shrews, the foliate papillae do not contain any taste buds (MARTINEZ
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et al. 1998, K OBAYASHI and W ANICHANON 1992, K OBAYASHI et al. 2003); nor do
they have any foliate papilla (Insectivora and Chiroptera; K OBAYASHI et al. 1989,
P ASTOR et al. 1993, E MURA et al. 2002, G REGORIN 2003, J ACKOWIAK et al. 2004,
J ACKOWIAK 2006, H WANG and L EE 2007, J ACKOWIAK et al. 2009; P ARK and L EE
2009). According to S HINDO (2006), the level of development of foliate papillae
is correlated with the type of food and the manner of its processing inside the
mouth.
The areas between the papillae are lined with keratinised epithelium whose
thickness gradually increases towards the root of the tongue. The thickness of
the keratinised layer and its percentage of the total thickness of the epithelium
are the highest at the apex. As the degree of keratinisation of the epithelium is
strongly linked with food type (I WASAKI 2002) and becomes higher in those areas
particularly exposed to mechanical traumas, it can be assumed that the anterior
part of the tongue is responsible for the mechanical processing of food, while
the posterior part performs the function of taste recipient.
In conclusion, current studies show that the tongue of the hazel dormouse
from the family Gliridae is, in many ways, similar to the tongue structure of the
other representatives of Sciuridae which may confirm the common origin of both
taxonomic units. It also has certain features which make it similar to Megachiroptera
bats, and this may be correlated with the food preferences of the animals and
their environment. According to some researchers (S ARA and S ARA 2007), it is
fruit that constitutes the principal food of the hazel dormouse and this may be
confirmed by the structure of its tongue.
Acknowledgements
The author thanks Dr A. Œwi¹tek from the Academia Pomeraniensis in
S³upsk for supplying the materials for the research.
GRZBIETOWA POWIERZCHNIA JÊZYKA ORZESZNICY MUSCARDINUS
AVELLANARIUS: BADANIA Z WYKORZYSTANIEM MIKROSKOPU
SKANINGOWEGO I ŒWIETLNEGO
STRESZCZENIE
Grzbietowa powierzchnia jêzyka orzesznicy by³a badana przy u¿yciu
skaningowego mikroskopu elektronowego i mikroskopu œwietlnego. Jêzyk orzesznicy
jest wyd³u¿ony i rozszerzony w przedniej czêœci. W przedniej 1/3 d³ugoœci jêzyka
obserwuje siê wyraŸn¹ bruzdê poœrodkow¹. Grzbietowa powierzchnia jêzyka jest
pokryta przez piêæ typów brodawek: nitkowate, sto¿kowate, grzybowate, okolone
i liœciaste. Rozmieszczenie, kszta³t, rozmiary i pochylenie brodawek ró¿ni¹ siê
zale¿nie od regionu jêzyka. W przedniej czêœci jêzyka, brodawki nitkowate s¹
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pi³kowane i zwrócone wierzcho³kami ukoœnie do œrodka i ku ty³owi jêzyka, podczas
gdy w tylnej czêœci jêzyka maj¹ kszta³t widlasty i uk³adaj¹ siê promieniœcie,
pochylaj¹c wierzcho³ki w kierunku œrodka jêzyka. Brodawki grzybowate zaopatrzone
w pojedynczy kubek smakowy s¹ równomiernie rozproszone w przedniej i œrodkowej
czêœci trzonu jêzyka. Na nasadzie jêzyka, trzy gwiaŸdzistego kszta³tu brodawki
okolone s¹ u³o¿one w formie trójk¹ta i otoczone brodawkami sto¿kowatymi. Na
obu brzegach tylnego obszaru jêzyka znajduje siê para brodawek liœciastych,
która tworzy trzy równoleg³e fa³dy odseparowane g³êbokimi bruzdami. Grzbietowa
powierzchnia brodawek liœciastych i okolonych pokryta jest silnie zrogowacia³ym
nab³onkiem, podczas gdy boczna powierzchnia ma nab³onek niezrogowacia³y,
z licznymi kubkami smakowymi. Wyniki naszych badañ pokaza³y, ¿e budowa
jêzyka orzesznicy jest bardziej prymitywna ni¿ u innych gryzoni. Jest to zwi¹zane
z filogenez¹ i zwyczajami ¿ywieniowymi orzesznicy.
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Received 2014-04-28
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