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Taste bud development in chickens (Gallus gallus domesticus).

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THE ANATOMICAL RECORD 218:88-93 (1987)
Taste Bud Development in Chickens
(Gallus gallus domesticus)
Department of Oral Biology, The Hebrew University-Hadassah School of Dental Medicine,
Jerusalem 91010 (J.R. G.), and Department ofAnatomy and Anthropology, Sackler Faculty of
Medicine, Tel Aviv University, Tel-Aviv 69978 (D.G.), Israel
Oral epithelium in the anterior mandibular glands region was examined in embryonic, hatchling, and mature chickens to establish the timing of
morphologic events during taste bud ontogeny. Hematoxylin-and-eosin-stainedsections (10 pm) from 27 Anak (broiler breed) chickens were examined serially, and
buds were quantified at 16-20 days of incubation (E) and, posthatch days 1 and 5060. Taste buds were first recognized at the beginning of E17 as small clusters of cells
in the basal epithelium. Only spherical-shapedbuds were observed on E17 and E18,
and these spherical clusters never penetrated to the surface of the stratified epithelial layer. E19 marked a transitional stage when mature bud features began to
emerge: the buds assumed a more elongate shape, several kinds of cells comprising
the bud were distinguishable and the first taste pores were observed. During the
ensuing embryonic days, buds continued to elongate commensurate with the deepening oral epithelium and by hatching virtually all buds opened to the oral cavity.
No marked morphological changes in taste bud structure were observed on the day
of hatching and at 50-60 days posthatching. Taste bud numbers increased dramatically during E17 and E18, peaked on E19, and remained relatively constant thereafter. It is concluded that the morphological sequence of taste bud development in
chickens is similar to that in mammals. The timing of bud ontogeny, though initiated only during the third trimester in ovo, essentially is completed by hatching,
thus providing the precocial hatchling with the sensory apparatus essential for
gustatory experience.
The sequence of events in the development of taste
buds is relatively consistent across mammalian species
(cf. Bradley, 1972; Bradley and Mistretta, 1973; Bradley
and Stern, 1967; Bradley et al., 1980; Farbman, 1965;
Ferrell, 1984; Komatsu and Yamasaki, 1980; Stedman
et al., 1983; Zahm and Munger, 1983a,b).Initially, presumptive buds are recognized as small clusters of cells
in the basal epithelium. Early developing taste buds are
covered by superficial layers of epithelium, thereby remaining isolated from the environment of the oral cavity. Later in development the buds elongate as their
cells become oriented perpendicular to the basement
membrane epithelium. Bud maturity is usually defined
when a pore is formed as a channel communicating
between the apices of the taste bud cells and the oral
cavity. Marked increases in the number of taste buds
also occur during these progressive stages. To what extent this morphogenetic sequencing during mammalian
bud ontogeny is generally applicable to that in other
vertebrates is not known. For example, the evolution of
avian and mammalian forms from different reptilian
ancestors (Romer, 1941) argues for elaborating and comparing the developmental bud sequence in these vertebrate species.
Unlike the uniform sequencing of events in bud development, the time of appearance of the first buds in
mammals varies with time in utero. Ferrell (1984) suggested that the longer the gestational period, the earlier
0 1987 ALAN R. LISS, INC.
in fetal life the taste receptors begin to develop. Thus,
for humans (280 days gestation) and macaque monkeys
(168 days gestation), taste buds begin to develop by the
end of the first trimester (Bradley, 1972; Bradley and
Stern, 1967; Zahm and Munger, 1983a); in sheep (147
days gestation) bud development is initiated early in the
second trimester (Bradley and Mistretta, 1973);for puppies (Ferrell, 1984) and kittens (Stedman et al., 1983)
(62-63 days gestation) bud development commences near
the middle of the third trimester; the first signs of immature buds in rats (21 days gestation) and rabbits (30
days gestation) appear only at the end of the third
trimester (Hermann, 1884; Lustig, 1884; Mistretta,
The data above might imply that bud development in
chicks (21 days in OVO) should originate close to the time
of hatching. However, though rats and chicks have the
same length of gestation, their maturational state at
birth and hatching differs. Rats are altricial mammals,
and isolated, mature taste buds are not apparent until
several days after birth followed by a great increase in
numbers of buds during the suckling period (Mistretta,
1972). In contrast, newly hatched chicks are precocial
avians and hatchlings already possess a considerable
array of mature buds located in the oral epithelium of
Received July 7, 1986; accepted October 22,1986.
the upper beak (palate), anterior mandibular glands region of the lower beak, posteroventrolateral region of
the anterior tongue, and oral epithelium posterior to the
lingual spines (Ganchrow and Ganchrow, 1985; Saito,
1966). Taste discrimination tests show that these buds
are indeed functional at hatching (Braun-Bartena et al.,
1986) as well as during the last embryonic day Wince,
1977). These data suggest that the onset of taste bud
development might be initiated well before hatching
within the relatively short gestational period.
The present study provides quantitative and descriptive light microscopic data on the morphogenetic sequence and timing of anterior mandibular taste bud
development in the domestic chicken. Anterior mandibular buds are concentrated in the sublingual region of
the lower beak oral epithelium. Their viability is dependent upon the integrity of the chorda tympani branch of
the facial nerve (Ganchrow et al., 1986b), which transmits primary afferent gustatory information from these
buds to somata of the geniculate ganglion (Gentle, 1983,
1984; personal communication), and further centrally,
to subnuclei related to the solitary tract in the brainstem (Ganchrow et al., 1986a; Gentle, 1979).
animal. Several transitional morphologic stages occur
in the developing taste bud, and these stages are clearly
differentiable from the epithelial surround by the organization and staining characteristics of the bud. However, during quantification of taste buds, morphological
differences were disregarded. Each bud was traced serially through its entire extent and counted only once.
Occasionally the base of one bud appeared to be continuous with the base of an adjacent one; these were
counted as two separate buds since they approached the
superficial epithelial layers independently. Number of
gland duct openings was also noted. Results are expressed as averages plus or minus the standard error of
the mean unless stated otherwise.
Quantitative Considerations
Gustatory receptor development in the chicken is
characterized by a rapid establishment of the bud population during the last trimester before hatching, which
is substantially maintained over the ensuing 8 posthatching weeks. In the region of the anterior mandibular glands, no clear taste bud primordia were observed
until after the onset of the 16th embryonic day (E16).
By the beginning of E17, the initial sign of taste buds
Observations were made on 27 Anak strain (broiler (mean = 16 f 4) appeared. Numbers of buds increased
breed) chickens supplied by the Kibbutz Tzuba Hatchery through E18 (mean = 36 f 8) and E19 (mean = 83 f 2)
(Jerusalem). Either eggs prior to incubation (i.e., “day and ranged between 60 and 80 over the remaining ages
0”) or 1-day-old hatchlings were obtained. Eggs were examined (E20, 72 _+ 6; H1, 61 _+ 8; and H50-60, 57 _+
incubated at 99.6”F, saturated humidity, in a rotating, 8).
In the lower beak epithelium sampled, taste buds only
forced-draft incubator (Modern Equipment, Inc., Haifa),
while hatchlings were either utilized immediately or appeared adjacent to ducts of the anterior mandibular
maintained in the Hebrew University-Hadassah Medi- glands that opened into the floor of the mouth. However,
cal School Animal Facility. Light and electron micro- gland duct openings did not necessitate the presence of
scopic sampling of supplementary lower beak oral tissue a taste bud, especially in the lateral edge of oral epitheprior to this report established that there were no clear lium or posteriormost regions adjacent to the lingual
signs of buds throughout the first 15 days of incubation. frenulum. Mandibular salivary glands in the chicken
Toe and beak lengths also were measured to define the begin to develop on E8 as a series of solid ingrowths of
embryonic stage in the last trimester of development the mucosa, and by E16 the population of gland ducts
(Hamburger and Hamilton, 1951).While third toe length that open to the oral surface is well established (Hamilcompared favorably with the atlas developmental stages, ton, 1952; and personal observations).The average numupper beak length in our breed was at variance. Hence ber of anterior mandibular gland duct openings was
in our material, number of incubation days (E) was 27 f 1 in the anteroposterior extent of the bud region
considered preferable to staging as the embryonic index sampled across all the ages. The variation in the numbers of gland duct openings and taste buds correlated
of age.
The dissected beaks from 17 younger embryos (E16- positively (r = 0.74, P < .Ol) after the bud population
19) were immersion-fixed in 10% neutral buffered for- count had peaked (i.e., at E19 and older). When taste
malin. The remaining ten older animals-three at E20, buds were initially forming at E17-18, the bud-gland
three hatchlings (Hl), and four 50-60-day-old (H50-60) duct opening correlation approached significance (r =
chickens-were anesthetized with 6% pentobarbital so- 0.67; P = .05). Thus individual variability in the numdium (Hadassah), the blood was flushed transcardially ber of gland duct openings may partially account for the
with heparinized saline, and the chickens were perfused variability in the total number of buds observed. A more
transcardially with 10%neutral buffered formalin. Then accurate representation of taste bud development is
the lower beak was immediately placed in 10% neutral therefore a ratio of buds-to-glandduct openings. Figure
buffered formalin where it remained for at least a week. 1 shows that the number of taste buds per gland duct
Oral tissue extending from the beak tip to the lingual opening increased exponentially during the first portion
frenulum was dissected free and postfixed in the same of the last embryonic trimester (E16-18) and reached a
solution for several additional days. Subsequently, the plateau of about 2.5 buds per opening in the ensuing
tissue was decalcified (Rapid Bone Decalcifier, Du-Page prehatching (E19 and E20) and posthatching (H1 and
Kinetic Laboratories), dehydrated in increasing concen- H50-60) periods. This developmental index seems relitrations of ethanol, and embedded in paraffin. Frontal able since, independently, Kusuhara (personal commusections (10 pm) were stained with hematoxylin-and- nication) analyzed anterior mandibular buds in seven
mature chickens and obtained a similar ratio of 2.23
eosin for light microscopic examination.
Analyses of taste bud morphology, number, and den- budslgland duct opening.
Since the lower beak continued to grow throughout
sity were made unilaterally in each processed block of
bilateral tissue without foreknowledge of the age of the the ages examined, the density of buds decreased mark-
H 50-60
Fig. 1 . Mean (+SE.) number of taste buds per anterior mandibular
glands duct (AMQ opening as a function of embryonic age (E16-E20)
and posthatching(Hl-H60) age. The number of cases sampled at each
age appears in parentheses.
edly once the total population had been established. For
example, at E20, the bud region (2.83 k 0.07 mm anteroposterior extent) contained 25 f 1 buds/mm. At hatching, this density had decreased to 19 +_ 3 budslmm over
a distance of 3.16 f 0.14 mm, and by H50-60, 9 +_ 1
budslmm were distributed over 6.66 +_ 0.46 mm. The
region of the lower beak oral epithelium containing
taste buds generally constituted about the middle 75%
of the length of tissue examined.
Morphologic Considerations
Figure 2A illustrates oral epithelium and a gland duct
(*) at E16, the oldest age at which buds still were not
apparent. The epithelium consists of a single basal cell
layer covered by two to three strata of flattened cells.
The cuboidal cells lining the gland duct still extend
somewhat beyond the duct opening borders. Based on
previous data (Ganchrow and Ganchrow, 1985), at the
point where epithelium meets glandular tissue, one
might expect to find a taste bud. There are a few lighter
staining cells (curved arrows), which may represent the
taste bud Anlage in this region. Only two instances of
such possible precursor cells were observed at E16 within
the otherwise uniform oral epithelium.
Immature taste buds initially were identified at E17.
The course of bud maturation may be divided into two
main time frames based on bud shape: the spherical and
ovoid stages. The percentages of buds perceived to be in
the spherical stage were 94% at E17, 85% at E18, 32%
at E19, 13%at E20, and none thereafter.
Figure 2B-D illustrates three types of spherical-stage
buds characteristic of ages E17, E18, and E19. Spheres
varied in their size and depth within oral epithelium.
The earliest identified buds were spherical clusters of
cells located in the deepest epithelial layers (Fig. 2B,C).
Some bud cells appeared slender and elongated already
at E17, although their axial orientation could vary (Fig.
2B,C). The cytoplasm of some bud cells stained slightly
less intensely, and fewer still stained more intensely,
than that of the epithelial surround. Bud cell nuclei
were somewhat larger and as intensely stained as those
in basal epithelium. In some locations, the epithelium
at this stage had differentiated to include a third, intermediate layer whose cells contained more cytoplasm and
smaller, paler-staining round nuclei than those in adjacent basal and superficial layers. The surface layer of
flattened stratified epithelial cells was three to four cells
in height and sometimes appeared desquamate. By E18,
the basalmost deeper-staining layer had expanded to
about three cells deep, and the superficial stratified layer
was about eight to nine cells thick. Fine tubules penetrating the developing bud were already apparent at
this spherical bud stage (thick arrows Fig. 2C, D). Widediameter buds (Fig. 2D) multiply insinuated with fine
tubules were mainly noted at E18 and E19.
Embryonic day 19 represented the second transitional
phase in bud maturation. The spherical structures began to elongate to an ovoid shape that extended the
entire thickness of the oral epithelium, such that the
long axis of the bud was oriented perpendicular to the
basal and surface epithelial layers. Once the surface
epithelium was invaded by the bud, a taste pore became
apparent (fine arrow, Fig. 2E); occasionally, multiple
pores were observed (cf. in mammals: Bradley, 1972;
Ferrell, 1984; Heidenhain, 1914; Zahm and Munger,
1983b). At this stage, fine tubules still were a consistent
feature in the bud (thick arrow, Fig. 2E), and lighterstaining cells were more easily seen at the bud apex
than on earlier embryonic days.
As more buds elongated to the ovoid stage, characteristics of mature taste buds were expressed further (cf.
Figs. 2F, H1 and 2G, H50-60). The basal half of the bud
clearly contained lighter-staining cells with large, round,
medium-staining nuclei interspersed among darker cells
with lighter-staining nuclei. The basal half of the buds
was ensheathed by small cells with darker-staining nuclei. The pore region was flanked by long, narrow apical
bud cells oriented approximately perpendicular to the
epithelial surface in an orderly arrangement around the
pore (Figs. 2E and F). These slender cells contained slim,
dark-staining as well as lighter-staining round nuclei
located distal to the pore. Adult buds retained these
main features (Fig. 2G).
Neither pore opening nor other morphologic signs of
communication between the bud and oral cavity were
observed prior to E19. In contrast, from E19 and later,
three modes of pore opening were seen. The usual mature pore form was a narrow (1-2 pm), shallow channel
whose walls are composed of superficial epithelial cells
(Fig. 2E,F). Sometimes this channel appeared in a widened form (Fig. 2G) more closely resembling a pit (Fig.
2H). Rarely, the taste pore and the fine tubules of the
bud seemed to be continuous, as if a single channel had
penetrated through to the basal bud regions. Figure 21
is a montage of a bud from two adjacent sections, showing one such long channel directed toward a tubule in
the bud base. Since the tubule is cut in cross-section,it
appears as the hollow center of a cellular rosette. This
rosette-like configuration is a usual feature in mature
Fig. 2. Events in taste bud development. Asterisks in all photographs
indicate gland duct openings or the location at which the duct will
open in an adjacent section. A Oral epithelium 1 day prior (E16) to the
spheroidal stage of bud development. The curved arrows indicate a
collection of four cells (identified in several planes of focus) located at
the junction of glandular and epithelia1 cells. This configuration may
represent the taste bud primordium (10pm X 10 pm). E16. Magnification, x400. B: A small, spheroidal, presumptive bud (18 pm x 20 pm)
(curved arrow) in the basal oral epithelium. E17. Magnification, X 160.
C: Spherical bud (50 pm x 40 pm) with tubule (arrow). E17. Magnification, x 160. D: Large spherical bud (76 pm x 76 pm) with multiple
tubules seen in cross-section. Arrow points to one such tubule. E19.
Magnification, x200. E: Ovoid taste bud (width: 50 pm) with a pore
opening. Fine arrow indicates pore (2 pm). Note orientation of apical
bud cells toward the pore. Thick arrow points to tubule in cross-section.
E19. Magnification, x 160. F: Two taste buds (widths 50 pm, left; 35
pm, right) surrounding a salivary gland duct opening. Pores are marked
with arrows. Note the orientation of apical bud cells toward the pore
(widths, 1-2 pm). H1. Magnification, x 160. G: Mature taste bud with
pore (fine arrow). Pore width = 25 pm. Note the orientation of apical
bud cells toward the pore and ductule (thick arrow) cut in cross-section.
H50-60. Magnification, x 100.H: A taste pit opening (fine arrow). Pit
width = 21 pm. Thick arrow points to tubule in cross-section. H1.
Magnification, ~ 2 0 0 I:. Montage of two adjacent sections showing a
bud tubule directed toward a taste pore (fine arrow). The lowest portion
of the tubule is indicated by the thick arrow. E20. Magnification,
TABLE 1. Variability in the number of anterior mandibular taste buds in
the posthatch chicken: Light microscopic, serial section analyses
Anak (broiler)
White leghorn
Brown leghorn
Anak (broiler)
Present study
Saito (1966)
Ganchrow and Ganchrow (1985)
Gentle and Hunter (1983)
Present study
‘Unilateral bud counts were doubled to derive an estimate of buds in the entire anterior
mandibular bud region.
taste buds (Berkhoudt, 1985; Ganchrow and Ganchrow, generating elements. Moreover, perhaps by chance the
1985; Ganchrow et al., 198613; Gentle, 1971; Kurosawa sample of E19 chick embryos utilized was biased toward
animals with more salivary duct openings in the anteet al., 1983; Saito, 1966).
rior mandibular bud region than the sample of animals
at the other ages. Since a significant correlation beWithin the last trimester of a relatively short gesta- tween the number of buds and duct openings was obtion period (21 days), chick embryos display a rapid served in the present study, the latter variable could
development of taste buds. Specifically, anterior man- parsimoniously account for the large number of buds
dibular taste bud development begins around E17, pro- observed at E19.
Intra- and interstrain variability exists in the numceeds through a morphological sequence of events similar to that described for mammals, and by H1 the full bers of chicken taste buds. Table 1summarizes the light
population of buds with mature features has been estab- microscopic bud counts in the anterior mandibular
lished. Thus, unlike the delayed onset of bud develop- glands region in different strains of posthatch chickens.
ment observed in altricial mammals with similarly Clearly, the ranges in bud numbers and the means are
short, gestational periods (rats: Mistretta, 1972;rabbits: quite variable. The method of bud counting could acLustig, 1884; Hermann, 1884), chicken taste buds de- count for some of this variability, but even in the same
velop sufficiently early in the embryo to provide a taste laboratory and using the same observers and counting
receptor population commensurate with the hatchling’s methods, 1-day-oldbroilers (Anak strain) displayed more
precocial maturational state. Active ingestion of am- than twice as many buds as lighter-weight chicks bred
niotic fluids commences during the week preceding the for egg laying (Yarkon-tinted). Assuming that higher
onset of taste bud development, and thus, the forming anterior mandibular bud counts in the Anak strain rebuds are potentially stimulated by the increasingly con- flect a greater density of taste buds throughout the oral
centrated egg fluids during the final embryonic week cavity and that the number of buds is related to taste
(Romanoff, 1960).
sensitivity, these results would be compatible with reBud counts in the chick increased rapidly compared to cent data showing that heavier-breed chickens have a
most mammalian species, such that within 3 days bud greater overall taste sensitivity than do lighter breeds
numbers reached a unilateral total of 83 f 2 buds. This (Barbato et al., 1982).
total at E19 was somewhat high compared to all other
ages analyzed suggesting an embryonic “overshoot” in
This research was supported by a grant from the
the pool of gustatory receptors produced prior to bud
maturation, with subsequent bud degeneration until a United States-Israel Binational Science Foundation
stable taste bud population evolved. Cell death in the (BSF), Jerusalem, Israel. A preliminary report of these
developing nervous system is a well documented phe- findings was presented at the IX International Symponomenon (e.g., Barnett, 1985; Rubel et al., 1976). In the sium on Olfaction and Taste, Snowmass, Colorado, July
striped dolphin, the entire perinatal taste bud popula- 1986. We would like to thank Ilana Frank and Dr. Ron
tion disappears before adulthood (Komatsu and Yama- Goldstein for their technical assistance, Eva Salomon
saki, 1980),which represents a kind of phylogenetic cell for her photographic expertise, Shula Konig for typing
death. If the pattern of bud innervation in embryonic the manuscript, and Kibbutz Tzuba for supplying the
chickens is similar to that in adult mammals with sev- eggs.
eral nerve fibers innervating an individual bud (e.g.,
Beidler, 1969; Miller, 1971), and since the integrity of Barbato, G.F., P.B. Siegel, and J.A. Cherry (1982) Genetic analyses of
gustation in the fowl. Physiol. Behav., 29:29-33.
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