Published December 4, 2014
Morphological adaptations of yak (Bos grunniens) tongue
to the foraging environment of the Qinghai-Tibetan Plateau1
B. Shao,*† R. Long,*‡2 Y. Ding,§ J. Wang,† L. Ding,*‡ and H. Wang‡#
*Key Laboratory of Arid and Grassland Ecology (Lanzhou University), Ministry of Education, Lanzhou 730000,
China; †Institute of Zoology, School of Life Science, Lanzhou University, Lanzhou 730000, China;
‡International Centre for Tibetan Plateau Ecosystem Management, and §School of Life Science,
Northwest Normal University, Lanzhou 730070, China; and #College of Pastoral Agriculture Science
and Technology, Lanzhou University, Lanzhou 730020, China
ABSTRACT: Using light and scanning electron microscopy, the morphological adaptations of the yak (Bos
grunniens) tongue to its foraging environment in the
Qinghai-Tibetan Plateau were studied. The tongue of
the yak was compared with that of cattle (Bos taurus).
Compared with cattle, yak tongues are on average 4 cm
shorter (P < 0.001), and yak consume forages using the
labia oris, rather than by extending the tongue into the
harsh environment. The lingual prominence of yak is
greater (P < 0.001) and more developed than in cattle.
The conical papillae on the prominence surface of yak
are slightly larger (diameter: P = 0.068 and height: P =
0.761) and more numerous (P < 0.001) than in cattle.
The lenticular papillae on the prominence surface of
yak are larger (diameter: P = 0.002 and height: P =
0.115) and more numerous (P = 0.007) than in cattle.
Such characteristics may improve the digestibility of
forage by the grinding of food between the tongue and
the upper palate. Filiform, conical, lenticular, fungiform, and vallate papillae were observed on the dorsal
surface of the tongues studied; no foliate papillae were
observed. The papillae were covered by keratinized
epithelium, which was thicker (P < 0.001) in the yak
than in cattle. It is suggested that the development
of characteristic filiform papillae, and more numerous
lingual gland ducts and mucus-secreting pores in the
lenticular, fungiform and vallate papillae, fungiform
papillae, probably having mechanical functions, are all
morphological adaptations by yak to diets with greater
fiber and DM content as provided by the plants within
the Qinghai-Tibetan Plateau environment. On average,
yak has 26 vallate papillae and cattle have 28. In the
vallate papillae of the yak, the taste buds are arranged
in a monolayer within the epithelium, whereas they are
multilayered (2 to 4) in those papillae in cattle. The
number of taste buds in each vallate papillae was less
(P < 0.001) in the yak than in cattle. Therefore, the
gustatory function of the yak was weaker than in cattle. Yaks graze throughout the year on diverse natural
grasslands and have evolved morphological characteristics enabling them to consume a wide variety of plant
species, thereby better adapting them to the typically
harsh characteristics of their pastures.
Key words: lingual papillae, morphological adaptation, Qinghai-Tibetan Plateau, yak tongue
©2010 American Society of Animal Science. All rights reserved.
J. Anim. Sci. 2010. 88:2594–2603
doi:10.2527/jas.2009-2398
INTRODUCTION
1
This work was supported by grants from the Open Foundation of
the Chinese Educational Department Key Laboratory of Arid Agroecology and National Natural Science Foundation of China project:
30730069. The authors thank Tom Stewart of the School of Animal
Biology at the University of Western Australia (Perth) for his comments and suggestions on the preparation of this manuscript. The
authors express their appreciation to Malcolm Gibb (formerly Environment and Grassland Research Institute, North Wyke, UK) for
revision of the manuscript. The authors thank W. Ye and C. Yang
(School of Life Science, Lanzhou University, Lanzhou, China) for
assistance with sample collection.
2
Corresponding author: [email protected]
Received August 14, 2009.
Accepted April 3, 2010.
The yak (Bos grunniens), as a year-round grazing
animal, is a key species for maintaining alpine rangeland ecosystems in the Qinghai-Tibetan Plateau. There
are more than 14 million yak on the plateau, which
represents more than 90% of the world yak population. These yaks provide >90% of the milk and 50% of
the meat consumed by the local population (Long et
al., 1999a). The various rangelands of the plateau are
characterized by their high altitude, very low annual
average temperature (from −1 to −5°C), short growing
season (from June to September), and great seasonal
variation in feed supply (Long et al., 2004, 2005).
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Yak tongue adaptations
Feeding mechanisms are clearly an important factor
in determining the success and survival of vertebrate
species within their environment (Roth and Wake,
1989). During feeding, the tongue plays a principal role,
together with other organs within and near the oral
cavity, particularly in tetrapods in which the tongue
has a characteristic form (Iwasaki, 2002). Fish have
a slight elevation of the mucosa on the floor of the
mouth, but this structure does not contain any voluntary muscles, unlike the tongues of land vertebrates
(Kent, 1978). Most adult amphibians have a tongue,
as do reptiles, birds, and mammals. It is likely that
the tongue appeared during the evolution of tetrapods,
and this structure appears to be related to some extent
to the terrestrial lifestyle (Helff, 1929). Comparative
morphology of the tongues of vertebrates has revealed
how variations in the morphology and function of the
organ might be related to evolutionary events (Iwasaki,
2002). Therefore, it was predicted that the yak tongue
may have evolved specific morphological and structural
characteristics in response to the unique living environment and dietary habits imposed on the Qinghai-Tibetan Plateau. The objective of the present study was
to investigate the co-evolutionary relationship between
the morphological features of yak tongue and its foraging environment.
MATERIALS AND METHODS
All research protocols used in the current experiments were approved by the Animal Ethics Committee
of the Gansu province, China.
The tongues of 8 healthy yak (4 castrated and 2 entire males and 2 females, 3 to 6 yr old) with a mean
BW of 265 kg (SD ± 20 kg) were collected immediately
after slaughter from the Youyi slaughter house, Tianzhu Tibetan Autonomous County (>3,000 m above sea
level), Gansu Province, China. For comparison, the
tongues of 8 healthy cattle (Bos taurus; 4 castrated and
4 female, 3 to 4 yr old) of similar BW (275 kg, SD ±
25 kg) were collected immediately after slaughter from
the Xiaoxihu slaughter house, Lanzhou City (<1,500 m
above sea level), Gansu Province, China. The tongues
were fixed with 10% formalin, and shortly afterward,
blocks were cut from various parts of the tongue.
For light microscopy, specimens were dehydrated
through a graded series of alcohol, cleared and embedded in paraffin wax, and sectioned at 4 μm. Sections
were stained with hematoxylin-eosin and the slides observed using bright field light microscopy (BH-2, Olympus, Nagano, Japan).
For scanning electron microscopy, samples were taken
of the lingual surface from different areas and fixed in a
1% solution of osmium tetroxide in a phosphate buffer
for 4 h at room temperature. Subsequently, these were
immersed in a solution of 3.5 N HCl for 3 wk at room
temperature (22 to 25°C) to remove mucus and sloughed
cells (Evan et al., 1976). The samples were then washed
thoroughly in water and dehydrated through a graded
series of ethanol to 100%. The dehydrated tissues were
freeze-dried in a hyperbaric chamber (FreeZone 6 Plus,
Labconco, Kansas City, MO) of CO2 and coated with
gold in an argon (18 mV) vacuum chamber for 3 min.
The samples were observed using a scanning electron
microscope (JSM-6380 LV, JEOL, Tokyo, Japan) with
a 20-kV acceleration voltage. Descriptions of morphology refer to methods as described by Guo (1978) and
Hunan Research Group (1984). All statistical analyses
were performed using the independent samples t-test
(SPSS Inc., Chicago, IL), and significance was declared
at P < 0.05.
RESULTS
Mean values and ranges of measurements made of
yak and cattle tongues are presented in Table 1. In both
yak and cattle, the lingual prominence was observable
on the lingual body, but the yak lingual prominence was
greater (P < 0.001; Table 1) and more developed than
in cattle (Figures 1A and 2A). The transverse sulcus of
the yak tongue was visible at the anterior of the lingual
prominence (Figure 1A: d), but no median sulcus was
observed in the midline of the tongue. However, neither sulci were observed in the tongues of cattle (Figure
2A). The yak tongue on average measured (from the
tip to the glosso-epiglottic fold) 28.0 cm in total length,
8.0 cm in the length of the free portion (lingual apex),
and 8.5 cm at its maximum width. The tongue of cattle
was on average 32.0 cm in total length, 12.0 cm in the
length of the free portion, and 8.0 cm at its maximum
width. In both species, papillae were distributed not
only on the dorsal surface of the tongue, but also on
the anterior and ventral surfaces. Except for foliate papillae, 5 types of papillae, conical, lenticular, filiform,
fungiform, and vallate, were clearly identifiable on the
tongue surface of both species.
Conical Papillae
In the yak, the conical papillae (Figures 1A and 1D)
were distributed on the dorsal surface of the lingual
prominence, and there were 2 subtypes of these papillae
present at the prominence and directed centro-caudally.
One type of conical papillae had a broad base and a
tapering apex (Figure 3B), whereas the other type had
a blunt apex (Figure 3B′). The shape and distribution
of the conical papillae in yak (Figures 4B and 4B′) were
similar to those in cattle, but had a slightly greater
base diameter (P = 0.068) and were more (P < 0.001)
numerous than in cattle (Table 1). In both species, the
central papillae were larger (P < 0.001) than the peripheral papillae, and the surface of the papillae showed
scales of cornified epithelial cells (Figures 3D, 3D′, and
4D). On the surface of cattle conical papillae (Figure
4D′), the taste pores lie at the bottom of crater-like
depressions surrounded by squamous epithelial cells.
However, the taste pore was not found on the yak conical papillae (Figures 3D and 3D′).
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Shao et al.
Table 1. Gross measurements of tongues of the yak and cattle (n = 8)
Range
(minimum to maximum)
Item
Total length of tongue, cm
Maximum width of tongue, cm
Maximum thickness of tongue, cm
(maximum thickness of lingual prominence)
Length of lingual apex, cm
Maximum width of lingual apex, cm
Conical papillae
Total number
Diameter, mm
Height, mm
Thickness of keratinized epithelium, μm (papilla surface)
Lenticular papillae
Total number
Diameter, mm
Height, mm
Filiform papillae
Total number
Diameter, mm
Height, mm
Number per cm2 (anterior dorsal surface)
Fungiform papillae
Total number
Diameter, mm
Height, mm
Number per cm2 (anterior dorsal surface)
Vallate papillae
Total number
Diameter, mm
Height, mm
Thickness of epithelium, μm (papilla surface)
Number of taste bud per papilla
For both yak and cattle, the top of the conical papillae was covered by keratinized epithelium, which
was thicker (P < 0.001; Table 1) in the yak (Figures
3A and 4A). No taste buds were identified in the epithelium of the conical papillae of yak, but in cattle,
some taste buds were distributed within the epithelium
(Figure 4A). In the 2 species, the serous-rich mixed
lingual glands, as seen in some other ungulates, were
not found in the lamina propria, although some lingual
gland ducts (GD) were identified (Figures 3A and 4A).
There were, however, no obvious histological differences
between the 2 types of papillae in the 2 species.
Mean ± SD
Yak
Cattle
Yak
Cattle
P-value
26.5 to 30.0
7.0 to 9.5
1.8 to 3.0
29.5 to 34.0
7.0 to 8.6
3.0 to 4.2
28.0 ± 1.1
8.5 ± 0.8
2.0 ± 0.4
32.0 ± 1.4
8.0 ± 0.5
3.8 ± 0.4
<0.001
0.166
<0.001
7.0 to 9.5
7.0 to 9.5
190 to 240
0.5 to 2.0
1.0 to 3.0
210 to 270
180 to 210
1.5 to 3.0
1.0 to 2.0
10.0 to 14.5
7.0 to 8.6
140 to 160
0.5 to 1.5
1.5 to 3.5
34 to 73
200 to 240
0.8 to 2.2
1.0 to 3.0
8.0 ± 0.9
8.5 ± 0.8
200 ± 18
1.6 ± 0.5
2.3 ± 0.6
250 ± 16
200 ± 11
2.5 ± 0.5
1.8 ± 0.3
12.0 ± 1.3
8.0 ± 0.6
150 ± 8
1.2 ± 0.3
2.2 ± 0.7
50 ± 7
220 ± 14
1.6 ± 0.5
2.2 ± 0.6
<0.001
0.170
<0.001
0.068
0.761
<0.001
0.007
0.002
0.115
—
0.2 to 1.0
0.5 to 3.5
—
270 to 300
0.5 to 1.5
0.4 to 1.2
—
22 to 28
1.0 to 2.5
0.5 to 2.0
280 to 520
20 to 45
—
0.2 to 0.5
0.4 to 2.0
—
230 to 290
0.8 to 2.0
0.5 to 1.8
—
22 to 32
1.5 to 3.0
0.6 to 1.6
120 to 240
70 to 120
—
—
—
12 ±
290 ±
1.2 ±
0.8 ±
2.5 ±
26 ±
2.0 ±
1.0 ±
420 ±
26 ±
—
—
—
40 ±
260 ±
1.2 ±
1.0 ±
0.7 ±
28 ±
2.2 ±
1.2 ±
180 ±
82 ±
—
—
—
<0.001
0.002
1.000
0.238
<0.001
0.133
0.400
0.324
<0.001
<0.001
2
11
0.3
0.2
0.3
2
0.5
0.5
38
5
6
19
0.4
0.4
0.1
3
0.5
0.3
32
16
(Figures 1A and 2A), and the papillae had a distinctive encircling groove separated by the conical papillae
and their dorsal surface was slightly convex (Figures 5B
and 6D). In addition, many lingual gland pores were
Lenticular Papillae
Lenticular papillae for both yak and cattle were distributed on the dorsal surface of the lingual prominence
and were circular to oval in shape. Examples for yak
appear in Figures 1A, 1D, and 5B; and for cattle in
Figures 2A, 2D, and 6D, which were similar in both yak
and cattle. Although in yak, the papillae had a greater
average base diameter (P = 0.002), they were shorter
(P = 0.115) and less numerous (P = 0.007) than in
cattle (Table 1). In both species, the central papillae
were larger (P < 0.001) than the peripheral papillae
Figure 1. The tongue of the yak: (A) a, lingual root; b, lingual
body; c, lingual apex; d, lingual transverse sulcus. (B) 1, vallate papillae. (C) 2, fungiform papillae; 3, filiform papillae. (D) 4, 5, conical
papillae; 6, lenticular papillae. Color version available in the online
PDF.
Yak tongue adaptations
2597
yak (about 20% the length of the papillae), the main
protrusion was covered by a regular, continuous, and
tough aculeate-serrate keratinized epithelium (Figures
7D and 7E). The central region of the papillae (about
60% the length of the papillae) was flat, and the surface
showed scales of cornified epithelial cells (Figures 7B
and 7C). On the remaining basal region (about 20%
the length of the papillae), there were 5 to 8 secondary
papillae and pseudo-papillae, which emerged as delicate
projections from the surface of the central papillary
body and which adhered to the central papillae. However, in cattle, the whole surface of the filiform papillae
was covered by irregular aculeate-serrate keratinized
epithelium, and there were 2 to 4 secondary papillae at
the papillary (Figures 8A and 8B). In light microscopy
observations, there was no obvious morphological difference between the 2 species.
Figure 2. The tongue of cattle: (A) a, lingual root; b, lingual body;
c, lingual apex. (B) 1, vallate papillae; 2, conical papillae; 3, lenticular
papillae. (C) 4, fungiform papillae; 5, filiform papillae. (D) 2, conical
papillae; 3, lenticular papillae; (E) 4, fungiform papillae; 5, filiform
papillae. Color version available in the online PDF.
observed on the dorsal surface of each papilla in the 2
species (Figures 5C and 6C: arrows). On the surface of
cattle lenticular papillae, the taste pores lie at the bottom of crater-like depressions surrounded by squamous
epithelial cells (Figure 6D: star). However, the taste
pore was not found on the yak conical papillae (Figures
5A and 5D).
In yak, the tops of the lenticular papillae were covered by thin keratinized epithelium (Figure 5A), unlike
those of cattle, which were not keratinized (Figures 6A
and 6B). No taste buds (TB) were identified in the
epithelium of the lenticular papillae of yak (Figure 5A:
TB), but in cattle some were multilayered (2- or 3-layered; Figure 6A: TB) in the lateral epithelium.
Filiform Papillae
In both yak and cattle, most of the filiform papillae
(Figures 1A and 2A) were found on the dorsal surface
of the anterior tongue, with the remainder being distributed on the anterior ventral region of the lingual
apex, from the tip to the margin of the vallate papillae
on the 2 lateral regions of the lingual prominences. All
of the filiform papillae were cylindrical with a short
convex point in shape (Figures 1C, 2C, 2E, 7B, and
8A), and all lay pointing in the direction of the lingual
root (Figures 1C, 2C, and 2E). Compared with cattle,
in yak these papillae were more variable both in their
base diameter and height, but there were fewer per unit
area of the anterior dorsal surface of the lingual apex (P
< 0.001; Table 1). In both species, the filiform papillae
on the dorsal surface gradually increased in size from
the lingual body to the apex, whereas on the ventral
surface they were smaller (P < 0.001) and fewer (P <
0.001) in number. On the filiform papillary apex of the
Figure 3. Conical papillae of the yak: (A) light micrograph of a
sagittal section of the conical papillae, the top of the papillae is covered by keratinized epithelium and the lingual gland ducts (GD) are
found on the lamina propria, scale bar = 500 μm; (B), (C), and (D)
scanning electron microscope (ScEM) micrograph of the external surface of the conical-like apex papilla. Scale bar = 500 μm (B), scale bar
= 10 μm (C), and scale bar = 2 μm (D); (B′), (C′), and (D′) ScEM
micrograph of the external surface of the blunt-like apex papilla, scale
bar = 500 μm (B′), scale bar = 100 μm (C′), and scale bar = 10 μm
(D′). Color version available in the online PDF.
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Shao et al.
Figure 4. Conical papillae of cattle: (A) light micrograph of a sagittal section of the conical papillae. There are some lingual gland ducts
(GD) and taste buds (TB). Scale bar = 200 μm. (B) Scanning electron microscope (ScEM) micrograph of the external surface of conical
papilla present on the dorsal surface of the lingual prominence. The
conical papilla is tapering, cone-like in shape. Scale bar = 500 μm. (B′)
ScEM micrograph of the external surface of conical papilla present on
the dorsal surface of the lingual prominence. The conical papillae are
blunt, cone-like in shape. Scale bar = 200 μm. (C), (C′), (D), and (D′)
ScEM micrograph of the external surface of the conical papilla (large
arrow: mucus-secreting pore; small arrow: taste pore). Scale bar = 50
μm (C), scale bar = 10 μm (C′), scale bar = 5 μm (D), and scale bar
= 2 μm (D′). Color version available in the online PDF.
Fungiform Papillae
The fungiform papillae (Figures 1A and 1C) were
distributed within the central area occupied by the
filiform papillae and were intermixed with them, but
their periphery was protected by a marginal band of
the longer filiform papillae. The distribution of fungiform papillae in cattle (Figures 2A, 2C, and 2E) was
similar to that of the yak. In the yak and cattle, the
fungiform papillae had the same average base diameter
(P > 0.95), but were more numerous in the yak (P =
0.002; Table 1). In both species, the number of papillae
gradually diminished from the lingual body to the apex
(Figures 1A and 2A). In the yak, there were 2 types of
fungiform papillae, bud-shaped (Figure 9B) and dome-
shaped (Figure 9E), and numbered approximately 290
in total (Table 1). In contrast, only dome-shaped fungiform papillae were found in cattle (Figure 10A), and the
total number was approximately 260 (Table 1). In both
species, each fungiform papilla had a distinctive encircling groove separated by the filiform papillae (Figures
9B, 9E, and 10A). In yak, the filiform papillae lay over
the fungiform papillae, either in contact with them or
in the area immediately above (Figures 1C, 9B, and
9E). However, this feature was not observed in cattle
(Figure 10A). Some taste pores were observed on the
surface of the dome-shaped fungiform papillae of yak;
the surface of the bud-shaped papillae was convex and
there were 5 to 12 mucus-secreting and taste pores. The
mucus-secreting pores of the bud-shaped papillae were
smaller (P < 0.001) than those of the dome-shaped
papillae (Figures 9D and 9F: arrow). In addition, the
bud-shaped papillae had several small bud-shaped protrusions arranged on the rim of the primary protrusion
(Figures 9B and 9C). However, the papillary surface of
cattle was flat except for the presence of some mucussecreting and taste pores (Figure 10A).
In the yak, some taste buds were distributed in the
epithelium of the fungiform papillae, the surfaces of
which were covered by thin keratinized epithelium
(Figure 9A), although in cattle the epithelium was not
keratinized (Figure 10A). In neither species were serous-rich, mixed lingual glands observed in the lamina
propria; however, some lingual GD (Figure 9A) were
identified. There was no obvious morphological difference between the bud-shaped and the dome-shaped papillae in the yak based on the histological examination,
except for the epithelial surface.
Vallate Papillae
In yak, the vallate papillae were arranged in a V pattern on the posterolateral surface of the lingual prominence (the posterior one-third of the tongue) with the
apex of the V pointed anteriorly (Figures 1A and 1B).
Each papilla was a cylindrical central body, surrounded
by a deep groove and a circular raised area of tough
epithelial tissue (Figure 11A). Vallate papillary distribution and structure in cattle (Figures 2A and 2B)
were similar to that of the yak, but in cattle the papillae were the shape of a truncated cone (Figure 12A).
In both species, the papillae appeared alone or in pairs
with smaller papillae (Figures 1B and 2B), and some
mucus-secreting and taste pores were observed on the
surface of each papilla (Figures 11C, 11D, 12B, 12C,
and 12F: arrow and star).
In the vallate papillae of yak, the taste buds were arranged in the epithelium as a monolayer (Figures 11A
and 11B: TB) and serous-rich mixed lingual glands
(Figure 11A), and their ducts (Figure 11A: GD), as
in other ungulates, were observed in the lamina propria. However, in cattle, the taste buds were arranged
in the lateral epithelium and were multilayered (2 to 4
layers; Figure 12A: TB). The number of taste buds in
Yak tongue adaptations
Figure 5. Lenticular papillae of the yak: (A) light micrograph of a
sagittal section of the lenticular papillae. The taste buds are found on
the dorsal surface of the epithelium, the lingual glands ducts (GD) are
found on the lamina propria, and the surface of the papillae is covered
by thin keratinized epithelium. Scale bar = 500 μm. (B) Scanning
electron microscope (ScEM) micrograph of the external surface of the
lenticular papilla. Scale bar = 200 μm. (C) ScEM magnified micrograph of the external surface of the lenticular papilla (arrow: mucussecreting pore). Scale bar = 20 μm. (D) ScEM magnified micrograph
of the small pores in between keratinized epithelium. Scale bar = 2
μm. Color version available in the online PDF.
each vallate papillae was less (P < 0.001; Table 1) in
the yak than in cattle. The epithelium of the vallate
papillae of the yak was thicker than that of cattle (P
< 0.001; Table 1), but only in the yak was it covered
by a thin keratinized epithelium (Figures 11B and 12A,
respectively).
2599
ticatory requirements and functions of those species in
which they occur.
In contrast, in cattle, the lingual prominence was not
as well-developed because the transverse sulcus of the
tongue was not present. In the anterior border of the
lingual prominence, the number of the conical papillae
was less than in yak, and the lenticular papillae appear to have a limited mechanical function due to the
surface of the papillae not being covered with keratinized epithelium. Although the tongues of the yak were
generally shorter than those of cattle, the difference (4
cm) was attributable to the difference in length of the
lingual apex between the 2 species. The yak possesses
an unusual foraging behavior in that grass is pulled
into the mouth by the labia oris, and the tongue is not
extended into the environment. Yak living in the Qinghai-Tibetan Plateau and its peripheral plateau areas
can feed on grasslands normally when the temperatures
are as cold as −30 to −40°C, or even colder in a harsh
winter. If the foraging behavior of the yak were similar
to that of cattle, which pull grass into the mouth using
the tongue, the lingual tissue would be injured by frost,
with loss of heat and water.
The conical papillae are included by various authors
in the group of filiform papillae (Barone, 1976; Scala et
al., 1993; Emura et al., 2000c, 2008a,b; Yoshimura et
al., 2002, 2008; Nonaka et al., 2008). However, in the
present study, in agreement with other authors (Sonntag, 1920; Chamorro et al., 1987; de Paz et al., 1988;
Yoshimura et al., 2002; Pastor et al., 2008), we consider
that because of their size, shape, structure, and other
DISCUSSION
This study showed that the tongues of yak and cattle
can be divided into 3 areas. The lingual prominence,
which can be observed on the lingual body, corresponds
with those of other domestic animals, such as the dog
(Singh et al., 1980), pig (Kumar and Bate, 2004), sheep
(Emura et al., 2000a), goat (Kumar et al., 1998), cow
(Steflik et al., 1983; de Paz et al., 1988; Scala et al.,
1995), buffalo (Scala et al., 1993), horse (de Paz et al.,
1988; Pfeiffer et al., 2000; Kobayashi et al., 2005), and
camel (Qayyum et al., 1988; Eerdunchaolu et al., 2001).
Both the species studied in the current study have a
conspicuous lingual prominence with conical and lenticular papillae on the dorsal surface, filiform papillae
on the anterior-lateral edge, and vallate papillae on the
posterior-lateral area of the prominence. However, the
lingual prominence of the yak was greater and more
developed than in cattle. The presence of a lingual
prominence is regarded as a characteristic structure of
herbivores, and this muscle-rich prominence with filiform, conical and lenticular papillae allows herbivores
to grind food by crushing it between the tongue and the
upper palate. The morphology and structure of conical
and lenticular papillae have evolved fulfilling the mas-
Figure 6. The lenticular papillae of cattle: (A) light micrograph of
a sagittal section of the lenticular papillae. The taste buds (TB) are
found on the dorsal surface of the epithelium, and the lingual glands
ducts (GD) are found on the lamina propria. Scale bar = 500 μm. (B)
Light micrograph of a sagittal section of the TB, which is distributed
in the epithelium of the grooved side of the lenticular papillae. Scale
bar = 20 μm. (C) Scanning electron microscope (ScEM) micrograph
of the external surface of the lenticular papilla (arrow: mucus-secreting
pore). Scale bar = 200 μm. (D) ScEM magnified micrograph of the
external surface of the lenticular papilla (star: taste pore). Scale bar =
2 μm. Color version available in the online PDF.
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Figure 7. Filiform papillae situated on the lingual apex of the
yak: (A) light micrograph of a sagittal section of the base of filiform
papillae distributed on the anterior part of the tongue. The top of
the papillae is covered by thick keratinized epithelium, and the lingual glands ducts (GD) are found on the lamina propria. Scale bar =
200 μm. (B) Scanning electron microscope (ScEM) micrograph of the
external surface of filiform papilla present on the anterior part of the
tongue. The filiform papilla is spearhead-like in shape. Scale bar = 100
μm. (C) ScEM micrograph of the external surface of the postmedian
region of the papillae, which is covered with microgrooves and pores
(an intricate mesh-work of microplicae). Scale bar = 5 μm. (D) ScEM
micrograph of the external surface of the papillae apex. The main protrusion is surrounded by the concinnous, continuous, and developed
aculeate-serrate keratinized epithelium. Scale bar = 50 μm. (E) ScEM
magnification micrograph of the aculeate-serrate keratinized epithelium. Scale bar = 10 μm. Color version available in the online PDF.
characteristics, they are worthy of being considered a
separate group of papilla. In some species of carnivores
and in giant panda, the conical papillae have a smooth
surface and are not very prominent (Chamorro et al.,
1987; Iwasaki et al., 1987a; Emura et al., 2000c; Pastor et al., 2008), whereas those of the yak are longer,
flattened, and directed posteriorly. The size, morphology, and position of these papillae are similar to those
described by Yoshimura et al. (2002) in the sea lion
(Zalophus californianus), by Pastor et al. (2008) in the
giant panda, and by other authors (Steflik et al., 1983;
de Paz et al., 1988; Qayyum et al., 1988; Scala et al.,
1993, 1995; Kumar et al., 1998; Emura et al., 2000b;
Pfeiffer et al., 2000; Eerdunchaolu et al., 2001; Kumar
and Bate, 2004; Kobayashi et al., 2005) in various herbivores. In yak and cattle, the conical papillae possess
mucus-secreting pores and lingual GD, the tops of the
papillae are covered with keratinized epithelium, and
the mucus-secreting pores and microfolds distributed
Figure 8. The filiform papillae situated on the lingual apex of
cattle: (A) scanning electron microscope micrograph of the external
surface of filiform papilla present on the anterior part of the tongue.
The filiform papilla is cylindrical in shape. Scale bar = 100 μm. (B)
Scanning electron microscope micrograph of the external surface of
the papilla apex. The main protrusion is surrounded by the regular,
continuous, and tough aculeate-serrate keratinized epithelium. Scale
bar = 50 μm. (C) Scanning electron microscope micrograph of the
aculeate-serrate keratinized epithelium. Scale bar = 5 μm.
Figure 9. Fungiform papillae of the yak: (A) light micrograph of
a sagittal section of the fungiform papillae. The top of the papillae is
covered by thin keratinized epithelium and there are some taste buds
(TB) in the epithelium, and the lingual gland ducts (GD) are found
on the lamina propria. Scale bar = 500 μm. (B) Scanning electron microscope micrograph of the external surface of the bud-shaped papilla.
The surface of the bud-shaped papillae is convex and there are some
mucus-secreting pores. Scale bar = 200 μm. (C) Scanning electron
microscope micrograph of the external surface of the small bud-shaped
protrusions on the bud-shaped fungiform papilla (arrow: mucus-secreting pore). Scale bar = 20 μm. (D) Scanning electron microscope
micrograph of mucus-secreting pores in the bud-shaped fungiform papilla (arrow: mucus-secreting pore). Scale bar = 10 μm. (E) Scanning
electron microscope micrograph of the external surface of the domeshaped papilla. The dorsal surface is smooth, and the mucus-secreting
pores are observed (arrow: mucus-secreting pore). Scale bar = 500 μm.
(F) Scanning electron microscope micrograph of the mucus-secreting
pores in the dome-shaped fungiform papilla (arrow: mucus-secreting
pore). Scale bar = 10 μm. Color version available in the online PDF.
on the papillary surfaces resemble those of some carnivores and the giant panda (Chamorro et al., 1987;
Iwasaki et al., 1987b; Emura et al., 2000c; Pastor et
al., 2008). However, the keratinized epithelium of the
Figure 10. The fungiform papilla of cattle: (A) and (B) scanning
electron microscope micrograph of surface view of the round fungiform
papilla showing several mucus-secreting pores (arrow: mucus-secreting
pore). Scale bar = 200 μm (A) and scale bar = 5 μm (B).
Yak tongue adaptations
Figure 11. The vallate papilla of the yak: (A) light micrograph of
a sagittal section of the vallate papilla. The taste buds (TB) are found
on the dorsal surface of the epithelium, and serous-rich mixed lingual
glands (SR) and their ducts (GD) are found on the lamina propria.
Scale bar = 500 μm (a). (B) Light micrograph of a sagittal section of
the TB, which is distributed in the epithelium of the grooved side of
the vallate papillae. Scale bar = 20 μm. (C) and (D) Scanning electron
microscope micrograph of the surface view of the vallate papilla showing several taste and mucus-secreting pores (arrow: mucus-secreting
pore; star: taste pore); the flat scale-like peeling of the epithelium is a
characteristic feature of the taste pores. Scale bar = 200 μm (C) and
scale bar = 2 μm (D). Color version available in the online PDF.
conical papillae of the yak was thicker than that of
cattle and the papillae are larger and more numerous,
indicating an enhanced mechanical function for the yak
conical papillae compared with cattle.
In both yak and cattle, the lenticular papillae were
situated on the lingual prominence and the centrally situated papillae were larger in size compared with those
situated peripherally. The papillae had a distinctive circular groove separated by the conical papillae. No taste
buds were identified in the epithelium of the lenticular
papillae of yak, but in cattle some were multilayered
in the lateral epithelium. The papillary dorsal surface
in the yak was convex and covered by a thin keratinized epithelium, which was not the case for cattle. It
is suggested that the lenticular papillae may only have
mechanical function in the yak, whereas in cattle they
only possess a gustatory function. No reports describing the lenticular papillae in the other mammals have
been published, excepted for some artiodactyls (Nickel
et al., 1979).
According to published data, filiform papillae of most
mammals are similar to that of the yak in shape and
structure (Chamorro et al., 1987; Kobayashi et al.,
1988a,b, Kobayashi and Wanichanon, 1992; Inatomi
and Kobayashi, 1999; Emura et al., 2004; Jackowiak
et al., 2004), except for variations in size and number
per unit area of the main and secondary papilla. In this
study, on the basis of the characteristics of shape and
structure, it was concluded that this papilla type had
the purely mechanical functions of grasping food and
grooming in yak and cattle. Furthermore, on the basis
their distribution, we conclude that these papillae may
2601
also serve to protect fungiform papillae and fulfill a
mechanical cleaning function in the interdental spaces
of the lower jaw in the yak and cattle, similar to that
which occurs in other mammals such as prosimians,
tupaias, and the giant panda (Hofer et al., 1993; Pastor
et al., 2008). As is the case among all mammals, these
were the most numerous mechanical papillae on the
tongue and were distributed along the entire surface
of the lingual dorsum, as well as the ventral surface
close to the tip (Davis, 1964). However, in yak and
cattle, the conical and lenticular papillae were distributed on the dorsal surface of the lingual prominence
and only a few small filiform papillae were distributed
on the anterior-lateral edge of the lingual prominence.
The filiform papillae of the yak were larger than those
in cattle, but their frequency on the dorsal surface of
the anterior tongue of yak was less than in cattle. In
the filiform papillary apex of yak, the main protrusion
was surrounded by the regular, continuous, and tough
aculeate-serrate keratinized epithelium, which enhances
the papillary mechanical function.
The fungiform papillae were in all ways similar to
those found in other mammals; their base was rounded
and encircled by filiform papillae, which gave the appearance of providing protection for them. In the yak
these papillae possessed 2 shapes, bud and dome. It
is noteworthy that several small bud-shaped secondary
papillae were distributed on the dorsal surface of the
bud-shaped fungiform papillae, and no reports have yet
been published describing these uniquely shaped papillae in other mammals. In the yak, the fungiform papil-
Figure 12. The vallate papilla of cattle: (A) light micrograph of
a sagittal section of the vallate papillae. The taste buds (TB) were
found on the dorsal surface of the epithelium and serous-rich mixed
lingual glands (SR), and the lingual gland ducts (GD) were found on
the lamina propria. Scale bar = 500 μm. (B) Scanning electron microscope micrograph of the vallate papilla showing vallum, moat, and
pseudo-papillae on its surface. There are mucus-secreting pores (arrow:
mucus-secreting pore). Scale bar = 500 μm. (C) and (D) Scanning
electron microscope micrograph showing the honeycomb-like surface
of the body of the vallate papilla (arrow: mucus-secreting pore; star:
taste pore). Scale bar = 5 μm (C) and scale bar = 1 μm (D). Color
version available in the online PDF.
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Shao et al.
lae appear to possess dual mechanical and gustatory
functions because in these papillae there are many taste
buds and taste pores in the epithelium, and the surface
of the papillae is covered with keratinized epithelium.
This was especially evident in the bud-shaped papillae
where there were some small bud-shaped protrusions
arranged on the dorsal surface of the papillae. Fungiform papillae of the yak were more abundant per unit
area on the anterior dorsal surface of the tongue than in
cattle. The distinct structure of the fungiform papillae
strengthens the gustatory function of the lingual apex,
and the protection of the papillae by the filiform papillae is beneficial.
Vallate papillae in other mammals may have 2 principal morphologies, simple or compound. The simple
type has a not-very-prominent uniform central part
and is surrounded by a deep groove, whereas the compound papillae have a central part divided by secondary grooves. The number of secondary papillae can be
quite variable even within the same species. Occasionally double or triple papillae are present, sharing a primary groove. In the yak and cattle, the papillae are
compound, as in perissodactyls (Chamorro et al., 1986;
Emura et al., 2000b), certain artiodactyls (Chamorro et
al., 1986; Emura et al., 1999) and in carnivores, such as
the cat (Chamorro et al., 1987), Asian black bear (Inatomi and Kobayashi, 1999; Emura et al., 2001), silver
fox (Jackowiak et al., 2004), sea lion (Yoshimura et al.,
2002), and in the giant panda (Pastor et al., 2008). On
average, yak and cattle had 26 and 28 vallate papillae,
respectively, compared with animals such as goat, deer,
and sheep (artiodactyla; Asami et al., 1995; Inatomi
and Kobayashi, 1999; Yamaguchi et al., 2002; Zheng
and Kobayashi, 2006), which have on average 10 to 20
or more. In addition, in the yak there were fewer taste
buds in each vallate papillae than in cattle. It is suggested that an increase in the number of vallate papillae provides greater sensitivity in the sense of taste. It
is concluded that, compared with cattle, the gustatory
function of the yak tongue is weaker and this may be an
advantage for an animal needing to consume a broad
diet across a variety of rangelands where there are
more than 100 edible plant species, including grasses,
legumes, sedges, forbs, and many shrub species, most of
which contain secondary compounds, such as tannins,
in the fresh material (Long et al., 1999a). However, further investigation of this possible association is needed.
Compared with cattle, the vallate papillary epithelium
of the yak was thicker and the surface was covered with
a thin keratinized epithelium, suggesting that the vallate papillae of yak may function as a grinding organ
against the palate.
Within each mammalian clade, the morphology of
lingual papillae has unique characteristics reflecting
the evolutionary taxonomic position and dietary niche
of the animal (Yoshimura et al., 2008). Adaptation to
the pressures of the environment and available diet
may also affect the morphology of the lingual mucosa
(Yoshimura et al., 2002). Given the extremely harsh
environment and the seasonal changes in diet quantity and quality, the yak suffers considerable malnutrition during the long cold season (Long et al., 1999b).
The distinctive morphology of the filiform papillae, the
lingual GD, and the more numerous mucus-secreting
pores in the lenticular, fungiform, and vallate papillae,
and the probable mechanical function of the fungiform
papillae, lead us to suggest that they represent morphological adaptations by the yak to foraging in the highlands of the Qinghai-Tibetan Plateau environment.
In conclusion, it is suggested that the morphological
features of the yak tongue, namely, the strengthened
and well-developed stratification and keratinization of
the epithelium and an enhanced mechanical function of
the lingual surface, are adaptations to a varied environment. The environment provides diets rich in the secondary compounds in the warm season and fiber in the
cold season and is characterized by low-temperature climatic characteristics, as found on the Qinghai-Tibetan
Plateau. Further investigations regarding this species
are needed.
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