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ORIGINAL ARTICLE
Morphological Characteristics of the Vallate Papillae of theOne-Humped Camel (Camelus dromedarius)A. A. El Sharaby1*, M. A. Alsafy2, S. A. El-Gendy2 and S. Wakisaka3
1 Addresses of authors: 1 Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Damanhour University, Damanhour, Egypt;2 Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Alexandria University, Alexandria, Egypt;3 Department of Oral Anatomy and Developmental Biology, Osaka University Graduate School of Dentistry, Osaka, Japan
*Correspondence:
Tel.: +2 0106 4191 119;
fax: +2 045 3591 017;
e-mail: [email protected]
With 7 figures
Received September 2011; accepted for
publication February 2012
doi: 10.1111/j.1439-0264.2012.01149.x
Summary
In this study, the morphology of the vallate papillae of camel was investigated
using gross, light and scanning electron microscopy as well as immunohisto-
chemistry. Vallate papillae were arranged along an identical line on each side
of the lingual torus and revealed remarkable individual differences. However,
each papilla – round or flat, small or large, single or paired – was surrounded
by a prominent groove and an annular pad. Based on our findings, postnatal
development and formation of new papillae occur in camel. Microscopically,
taste buds were constantly observed along the medial wall epithelium, and in
the papillary wall epithelium on both sides of the secondary groove apparently
separating the vallate papillae. In addition, an aggregation of taste buds was
occasionally observed at the bottom of the lateral wall epithelium. Using SEM,
we observed several pits and microplicae on the surface of papillae as well as
distinct taste pores on the peripheral parts of the dorsal surface. We demon-
strated immunoreactivity of a-gustducin only in mature taste buds. We con-
clude that the morphological features and microstructure of vallate papillae are
a characteristic feature in camel compared to other ruminants. These features
might have evolved to assist the camel in the manipulation and tasting of thin
organic stiff plants that grow in its environment and therefore might have
related to the feeding habits of the animal.
Introduction
The morphologies of papillae on the dorsal tongue sur-
face have previously been researched across numerous
animals, enabling differentiation of papillae type and
morphology according to animal food habits (Kubota,
1988). The one-humped camel (Camelus dromedarius) is
a native animal to the dry climates, where thorny plants
with rough and hard stems grow. Thus, the camel’s
mouth is very sturdy and is developed to maintain effi-
cient feeding of these plants and is rubbery so that thorns
and branches won’t damage it (Sui et al., 1983). Up to
our knowledge, few reports are available on the morpho-
logical features of the camel tongue (in adult: Qayyum
et al., 1988; Erdunchaolu et al., 2001;1 Peng et al., 2008;
and during the fetal period: Doughbag, 1988; Salehi et al.,
2010). Likewise other ruminants, the foliate papillae are
absent in camel and in place there are plenty of vallate
papillae on the lingual torus. About 12–16 large flattened
circumscribed papillae are arranged in two lines on both
rims of the lingual torus, and each papilla is separated
from a surrounding thick annular pad by a prominent
gustatory groove. The vallate papillae on the outer line of
papillae appeared to be larger than those in the inner line.
Nevertheless, the nature and/or morphologies of the val-
late papillae have not been previously investigated.
According to Kubota (1988), there is an intimate rela-
tionship between the habitat, the feeding habits and the
development of vallate papillae. In the process of species
evolution, the number of vallate papillae increased like
occurred in ruminants (Qayyum and Beg, 1975; Prakash
and Rao, 1980; Chamorro et al., 1986; Scala et al., 1995;
Kumar et al., 1998; Emura et al., 2000b; Tadjalli and Paz-
hoomand, 2004; Kurtul and Atalgin, 2008). The purpose
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© 2012 Blackwell Verlag GmbH
Anat. Histol. Embryol.
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Anatomia, Histologia, Embryologia
A H E 1 1 4 9 B Dispatch: 16.3.12 Journal: CE: GeethaPriya P.
Journal Name Manuscript No. Author Received: No. of pages: 9 PE: Gayathri
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of the present study is to examine and compare with
those in other ruminants the morphological and micro-
structural characteristics of the vallate papillae in the one-
humped camel. As well, the relationship between these
features and the feeding behaviour in ruminant animals is
discussed.
Materials and Methods
Material collection and tissue preparation
The tongues of 15 clinically healthy camels of both sexes
and different ages (2.5–7 years) were used in this study.
Tongues were collected from Cairo slaughterhouses
directly after slaughtering the animals and rinsed with
0.1 m phosphate buffer saline (PBS, pH 7.4). Regions of
lingual torus containing vallate papillae were carefully dis-
sected out and kept in neutral buffered formalin for at
least a week prior to the subsequent processing. The gross
morphology of all the tongues was carried out on both
fresh and fixed specimens.
Light microscopy
For histological observation, tissue blocks were fixed in
Bouin’s solution at room temperature for 2–3 weeks and
processed in an automatic tissue processor (Histomatic
Tissue Processor Y, Model 166MP, Fischer Scientific2 ) to
dehydrate them in ascending grades of ethanol, and clear-
ing with xylene. These specimens were oriented trans-
versely and serially sectioned using a microtome at
10 lm. The serial sections were collected on glass slides
with 4–6 sections per slide, dried, and stained with hae-
matoxylin and eosin. The sections were examined at vari-
ous magnification levels on the light microscope (Zeiss
Photomicroscope III).
Scanning electron microscopy (SEM)
The whole tongues were rinsed with 0.1 M phosphate buf-
fer (pH 7.4), and all the vallate papillae were dissected
out and fixed in a modified Karnovsky’s solution (Kar-
novsky’s, 1965) for overnight at 4°C. Samples were then
post-fixed with 2% tannic acid and 1% OsO4 solution.
After dehydration through a graded ethanol series at
room temperature, specimens were substituted with 100%
ethanol : t-butanol (1:1) for 1 h and t-butanol for 1–
1.5 h at about 30°C and then kept overnight in t-butanol
below 4°C (Inoue and Osatake, 1988; Kobayashi et al.,
2003). The specimens were thereafter dried in t-butanol
freeze dryer (JFD-300; Jeol, Japan3 ) and mounted on metal
stubs and sputter-coated with platinum/carbon (plasma
multicoater, PMC-5000; Meiwa4 ). The mounted specimens
were observed at various angles under a scanning electron
microscope (JSM-5310 LV SEM, Jeol) at accelerating volt-
ages of 5 ± 10 kV.
Immunohistochemistry
We used polyclonal anti a-gustducin (Santa Cruz Bio-
technology Inc., Santa Cruz, CA, USA) to estimate the
maturation of taste buds. Preparation of the antibodies
and the procedures of avidin-biotin complex (ABC)
(a)
(b) (b) (c) (c)
(d) (d) (e) (e)
(f) (g)
Fig. 1. Vallate papilla of camel: (a) The tongue of adult camel has
many vallate papillae on the lingual torus. (b, c and b′, c′) Profiles of
vallate papillae found on the right and left sides of the young camel
tongue, respectively. (d, e and d′, e′) Profiles of vallate papillae found
on the right and left sides of adult tongue, respectively. (f, g) Vallate
papillae, which are found on the lingual torus of the oldest camel
tongue.
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method we used in this study were achieved according to
El Sharaby et al. (2006).
Results
Gross anatomy
The tongue of camel was elongated and dorsoventrally
flattened along its cranial two-thirds with a rounded apex
and a well-developed torus (Fig. 1a). There were 4–6
large vallate papillae arranged on each side closer to one
another forming two lines almost parallel to the rim of
lingual torus. The shape and size of the papillae revealed
remarkable differences; they were not identical or sym-
metrical in the two lines in the same specimen (Fig. 1b–g).
The cranially situated papillae were found most frequently
smaller in size as compared to the caudal papillae of
the same side. Accessory papillae, smaller in size, were
frequently observed medial to the main papillae. Their
number, size and shape as well as their relations to the
larger papillae were also variable. In some specimens, two
papillae were observed while being surrounded by a com-
mon annular pad and primary grooves. These papillae
were separated by secondary grooves. Several profiles of
vallate papillae were observed in young (Fig. 1b–e) and
old animals (Fig. 2a–i): (1) Flattened papilla either
rounded or oval in shape was centrally concave and sur-
rounded by a complete groove and distinctly prominent
annular pad (Fig. 2a). This was the most commonly
observed papilla having 80–160 mm length and 50–85
mm width. (2) A prominent small-sized papilla was oval
or rounded in shape and surrounded by a narrow shallow
groove and annular pad (Fig. 2b). It was observed most
frequently at the rostral or caudal aspect of the papillary
line. (3) Flattened papilla was small in size and projected
beyond the annular pad (Fig. 2c). (4) Centrally depressed
papilla with peripheral edges at the same level with the
annular pad (Fig. 2d). (5) Flattened papilla at early stage
of developing an additional annular pad (Fig. 2e). (6)
Two papillae very close to each other shared in part the
annular pad, but each was surrounded by independent
groove (Fig. 2f). Sometimes, a small or accessory papilla
might be associated. (7) Two papillae were enclosed
together by a common annular pad (Fig. 2g). (8) Two
papillae were apparently fused and enclosed by a com-
mon annular pad (Fig. 2h).
Scanning electron microscopy
Small-sized papillae were observed in both the young and
old animals. SEM observations revealed this papilla with a
visibly elevated central-shaped doughnut region sur-
rounded by a deep groove and annular pad. The surface
of the papilla had micropapillae but lacked the taste pores
(Fig. 3a,b). Medium-sized papillae were flattened oval in
shape and separated from a prominent annular pad by a
shallow groove. The peripheral parts of the surface were
smooth, while the central parts had shallow grooves and
micropapillae (Fig. 3c,d). Numerous, wide orifices of lin-
gual glands, with diameters reaching about 50–100 lm,
(a) (b) (c)
(d) (e)
(f) (g) (h)
Fig. 2. Vallate papilla of the camel: (a) Typical
vallate papilla in adult tongue. (b–h) Various
profiles of vallate papillae in tongue of young
(b–e) and old (f–h).
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A. A. El Sharaby et al. Morphology of Camel Vallate Papillae
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were located on the dorsal surface of the papilla. Some
taste pores were found at the peripheral areas close to the
grooves (Fig. 3e). In old specimens, two flattened papillae
were enclosed by a prominent annular pad and distinct
primary and secondary grooves (Fig. 4a). The papillary
surface had micropapillae and showed openings of the lin-
gual glands (Fig. 4b). It was wrinkled and divided by shal-
low grooves of variable lengths and directions especially
toward the peripheral parts of the papilla. Several pits of
the surface were frequently observed close to the primary
and secondary grooves, where they were associated with
taste pores of about 30–50 lm in width (Fig. 4c,d).
Light microscopy
Histological observations showed that the vallate papillae
were generally lined with keratinised stratified squamous
epithelium, which was composed by basal, spinosum,
granulosum and corneum layers (Fig. 5a). Lingual glands
located in the deeper parts of the papillae, and they
opened into the annular groove. The surface epithelium
was less keratinised compared to that of the surrounding
annular pad except the peripheral parts of the papilla.
Dermal inter-digitation of variable sizes into the epidermis
was observed along the whole surface. Few taste buds were
observed along the medial papillary wall epithelium of the
small-sized papillae, which was surrounded by shallow
groove (data not shown). In the typical papillae, several
taste buds with prominent taste pores were found along
the whole length of the medial papillary wall epithelium.
However, they were concentrated at the deeper parts of
the medial wall (Fig. 5b,c). The taste buds were spindle-
or columnar-shaped, 50 lm in width, and 50–150 lm in
height. A taste pore was approximately 4 lm in diameter.
In some specimens, an aggregation of taste buds was occa-
sionally observed deeply at the bottom of the lateral
groove wall close to the duct of Ebner glands (Fig. 5d). In
some old specimens, two vallate papillae became very close
to each other (separated or apparently fused) and sur-
rounded by a common groove and annular pad (Fig. 6a).
The papillae were separated from the surrounding lingual
epithelium by primary groove; meanwhile the two papillae
were separated from each other by secondary groove
(Fig. 6a). In some specimens, the latter leaded to a sinus
deep to the two papillae. Taste buds were constantly
observed in the entire length of the medial wall of the pri-
mary groove (Fig. 6b,d), and in the two side epithelium of
the secondary groove (Fig. 6c). Meanwhile, we did not
observe taste buds along the dorsal surface epithelium of
the vallate papillae in the investigated specimens.
Immunolabelling of a-gustducin
The immunoreactivity for a-gustducin (�IR) was not
observed in the small-sized or accessory papillae. In the
medium-sized papillae, a-gustducin-IR was recognised
within the taste buds only (Fig. 7a,b). The number of
�IR cells per taste bud was variable according to the size
of the papilla. Each �IR cell was spindled-shaped, longi-
tudinally oriented having ovoid nuclei and a smooth reg-
ular outline throughout their length with a larger
diameter at the nuclear region tapering to a smaller diam-
eter at either ends. A pronounced �IR was evenly distrib-
uted throughout the cytoplasm from the apex, where
apical processes converged at the taste pore to the basal
region of the taste bud.
Discussion
In agreement with the previous studies (Qayyum et al.,
1988; Erdunchaolu et al., 2001; Peng et al., 2008), the
(a) (b)
(c) (d)
(e)
Fig. 3. Surface morphology of vallate papillae of young camel. (a, b)
A small-sized papilla is prominent and surrounded by a wide groove
(a). The surface of the papillary dome has many micropapillae and mi-
crovilli, but no taste pores are found (b). (c–e) A medium-sized (typi-
cal) papilla is flattened oval in shape, centrally concave and separated
from a prominent annular pad by a clear groove (c). The peripheral
parts are smooth, meanwhile the central parts are divided by shallow
grooves and having micropapillae and desquamated cells (d). Some
taste pores are found at the peripheral areas of the papilla close to
the annular groove (e, arrows). The head arrows (c & e) refer to the
orifices of lingual glands, with diameters reaching about 50–100 lm,
which were frequently located toward the peripheral parts of the dor-
sal surface of the papilla.
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Morphology of Camel Vallate Papillae A. A. El Sharaby et al.
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present results demonstrated that the morphological fea-
tures and microstructure of the vallate papillae are a char-
acteristic feature in camel.
Spatial distribution and microstructure of the vallate
papillae
It is well known that the number and distribution of val-
late papillae varied between species from entirely absent,
as in cape hyrax (Emura et al., 2008), single in mouse,
rat and hamster (Iwasaki et al., 1997) to abundant as in
ruminants (Qayyum and Beg, 1975; Prakash and Rao,
1980; Chamorro et al., 1986; Scala et al., 1995; Kumar
et al., 1998; Emura et al., 2000b; Tadjalli and Pazhoo-
mand, 2004; Kurtul and Atalgin, 2008), and about 60 in
the black rhinoceros (Emura et al., 2000a). In the present
study, we found between 8 and 12 vallate papillae were
lined up on the both rims of the lingual torus, which
were frequently associated on their medial aspect with
smaller papillae. This formation, which coincides with the
findings of Qayyum et al. (1988) and Erdunchaolu et al.
(2001), is the unique characteristic of the camilidae fam-
ily, seems to compensate the absence of foliate papillae as
suggested by Kubota (1988).
We observed annular pad in close association with each
vallate papilla, which is said to regulate the access and
retention of the saliva in the trench (Chamorro et al.,
1986). The surfaces of vallate papillae were very irregular
showing micropapillae and grooves and were not smooth
as mentioned by Qayyum et al. (1988). We also found
deep pits closely associated with taste pores and openings
of the lingual glands, Ebner’s glands, on the peripheral
(a) (b)
(c)
(d)
Fig. 4. Surface morphology of the vallate
papillae of old camel. (a) Two flattened papil-
lae are enclosed by a prominent annular pad
(AP) and distinct primary (PG) and secondary
(SG) grooves. The surface of the papillary
dome is wrinkled and divided by grooves of
variable lengths and directions. (b–d) Micro-
papillae and pits are frequently observed on
the papillary surface close to the grooves,
where they are associated with taste pores (P)
and openings of the lingual glands (d). Head
arrows in (b) refer to the orifices of lingual
glands, which were associated with desqua-
mated epithelial cells.
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A. A. El Sharaby et al. Morphology of Camel Vallate Papillae
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parts of the surface epithelium. These micropapillae and
the grooves on the surface must protect the superficial
cells keeping them moist by the secretion of lingual
glands. They also direct the fluid toward primary and sec-
ondary grooves to wash away the gustatory materials
from the taste buds that face the groove. Then, the taste
buds can receive fresh stimulation by gustatory materials.
The distribution of taste buds shows some differences.
Our results demonstrated numerous taste buds constantly
along the entire length of the medial papillary wall, which
coincide with those reported in camel (Qayyum et al.,
1988; Erdunchaolu et al., 2001), cattle (Tabata et al., 2003;
Karadag et al., 2010) and deer (Adnyane et al., 2011). In
addition, we also observed taste buds on both sides of the
(a)
(b) (c) (d)
Fig. 5. Histology of vallate papillae in young camel: (a) Vallate papilla is wide and surrounded by a shallow groove (G). A small degree of dermal
inter-digitation into the surface epidermis was seen (arrows). Pits were clearly demonstrated on the surface (arrowheads) especially on the periph-
eral edges of the papilla (b, arrowhead). (c) Taste buds with prominent taste pores were observed along the whole length of the medial groove
wall epithelium, especially along the deeper parts. (d) In some specimens, an aggregation of taste buds was observed deeply at the bottom of
the lateral groove wall (arrow). Eb, Ebner gland and its duct. a: 92.5; b: 910; c, d: 920.
(a)
(b) (c) (d)
Fig. 6. Histology of vallate papillae in old camel. (a) Two fused vallate papillae. They were separated from the surrounding lingual epithelium by
primary groove (PG, inset); meanwhile the two papillae were separated from each other by a secondary groove (SG, inset). (b–d) Taste buds were
observed in the two side epithelium of secondary groove (c), and in the medial wall only of the primary groove (b, d) a: 92.5; b–d: 920.
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secondary groove and within the epithelial lining of deep
sinuses in the lateral papillary wall, which has not been
reported before. In contrast, Doughbag (1988) and Salehi
et al. (2010) found taste buds on the dorsal surface of the
vallate papillae of the embryonic tongue. It is not clear
whether the taste buds also exist or not in the papillary
side epithelium. It seems likely that taste buds appear first
in the surface epithelium then in the papillary wall in the
embryonic period. Mbiene and Roberts (2003) reported
that a drastic shortfall occurs in taste buds in the surface
epithelium and only the taste buds in the side wall epi-
thelium which remain in the adult vallate papilla of rat.
Vallate papillae of camel continue development after
birth?
In this study, we demonstrated several profiles of vallate
papillae apparently at different stages of development in
the tongue of camel. Definitive papillae are flattened, cen-
trally concave and surrounded by a continuous groove
and a distinctly prominent annular pad. Up to this stage,
there were three stages: (1) Prominent small rounded
papilla surrounded by a shallow groove and prominent
annular pad, which had few taste buds. (2) Small flat-
tened papilla projected beyond the annular pad. (3) Cen-
trally concave papilla with peripheral edges at the same
level with annular pad. Doughbag (1988) examined the
prenatal development of vallate papillae in camel and
reported that the papillae develop gradually in a caudo-
rostral direction forming one column on each side of the
lingual torus. We also found in older specimens of camel
tongue, various degrees of fusion of two papillae and lay
down of small or accessory papillae arranged constantly
medial to the larger or main papillae. This formation has
not been recorded in other animals including ruminants
and may be characteristic only for camel. It seems that
the camel vallate papillae may have a degree of develop-
ment and growth during life, which seems to be corre-
lated with seasonal variations or feeding habits.
Immunoreactivity of taste buds and gustatory functions
of camel vallate papillae
In this study, we used a-gustducin to estimate the matu-
ration of taste buds (i.e. presence of �IR type II cells).
We did not demonstrate a-gustducin in the taste buds in
the small-sized and accessory papillae. The taste buds in
these papillae are apparently immature. Meanwhile, taste
buds in the medium-sized and larger papillae showed a-
gustducin-IR. The demonstrated �IR cells are typically
similar to those observed in cattle and referred as mature
type II cells (Tabata et al., 2003).
Finally, the present results of the vallate papillae in
camel exhibited some different characteristics from other
domestic ruminants. This supports the hypothesis of
Kubota (1988) that morphology of the vallate papillae have
evolved in correlation with the habitat and feeding behav-
iour. These unique morphological characteristics assist the
camel in the prehension and manipulating of inorganic
stiff plants that grow in its favourable environment.
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Fig. 7. Immunoreactivity (IR) of a-gustducin in the vallate papillae of camel. The IR for a-gustducin was recognised only within the taste buds, and
the -IR cells were spindled-shaped, longitudinally oriented, having ovoid nuclei and a smooth regular outline. a, b: 920.
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