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Morphogenesis of lingual papillae of one‐humped camel (Camelus dromedarius) during prenatal life: A light and scanning electron microscopic study

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Abstract

This study was made on 24 camel fetuses of crown-rump vertebral length (CVRL) ranging from 10.5 cm to 105 cm CVRL (94–352 days old). These camel fetuses were classified into three groups representing the three trimesters of prenatal life. During the first trimester (94–142 days), lingual papillae (circumvallate and lentiform papillae) were demonstrated on the lingual root, but lingual body and the apex were almost free of papillae except for some scattered epithelial projections especially near the lateral borders of the body. In the second trimester (152–229 days), the lentiform papillae covered the entire root of the tongue except for areas occupied by the circumvallate papillae. Taste buds with clear pores were observed for the first time in areas between the circumvallate gustatory furrow and surface epithelium of the tongue. In addition, short numerous filiform papillae were observed on the rostral part of the lingual body and the lateral parts of the apex. Fungiform papillae, however, were demonstrated amidst the filiform papillae. In this trimester, taste buds were also seen on the top of the fungiform papillae. In the third trimester (256–352 days), all lingual papillae were clearly demonstrated on the dorsum of the root, body and apex of the tongue. Both types of gustatory papillae (circumvallate and fungiform) had well-developed taste buds. Mechanical papillae (filiform and lentiform) were well developed. Lentiform papillae occupied most of the dorsal aspect of the Torus linguae; they were larger in size with semicircular apices. Filiform papillae, however, were numerous and demonstrated heavily on the lateral and rostral parts of the body as well as on the apex of the tongue.
Anat Histol Embryol. 2017;1–8. wileyonlinelibrary.com/journal/ahe  
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© 2017 Blackwell Verlag GmbH
Received:18November2016 
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  Accepted:10October2017
DOI:10.1111/ahe.12321
ORIGINAL ARTICLE
Morphogenesis of lingual papillae of one- humped camel
(Camelus dromedarius) during prenatal life: A light and scanning
electron microscopic study
A. S. Abou-Elhamd1,2| M. Abd-Elkareem1| A. El-Zuhry Zayed1,2
1DepartmentofAnatomy,Histology
andEmbryology,FacultyofVeterinary
Medicine,UniversityofAssiut,Assiut,Egypt
2DepartmentofMedicalBiology,Jazan
University,Jazan,SaudiArabia
Correspondence
AlaaSayedAbou-Elhamd,Departmentof
AnatomyandHistology,FacultyofVeterinary
Medicine,AssiutUniversity,Assiut,Egypt.
Email: alaa88@yahoo.com
Summary
This study was made on 24 camel fetuses of crown-rump vertebral length (CVRL)
rangingfrom10.5cmto105cmCVRL(94–352daysold).Thesecamelfetuseswere
classifiedintothreegroupsrepresentingthethreetrimestersofprenatal life.During
thefirsttrimester(94–142days),lingualpapillae(circumvallateandlentiformpapillae)
weredemonstratedonthelingualroot,butlingualbodyandtheapexwerealmostfree
ofpapillaeexceptforsomescatteredepithelialprojectionsespeciallynearthelateral
bordersofthebody.Inthe second trimester (152–229days), the lentiform papillae
coveredtheentirerootofthetongueexceptforareasoccupiedbythecircumvallate
papillae.Tastebudswithclearporeswereobservedforthefirsttimeinareasbetween
thecircumvallategustatoryfurrowandsurfaceepitheliumofthetongue.Inaddition,
shortnumerousfiliformpapillaewereobservedontherostralpartofthelingualbody
andthe lateral partsof the apex. Fungiform papillae,however, were demonstrated
amidstthefiliformpapillae.Inthistrimester,tastebudswerealsoseenonthetopof
thefungiformpapillae.Inthethirdtrimester(256–352days),alllingualpapillaewere
clearlydemonstratedonthedorsumoftheroot,bodyandapexofthetongue. Both
types of gustatory papillae (circumvallate and fungiform) had well-developed taste
buds.Mechanicalpapillae(filiformandlentiform)werewelldeveloped.Lentiformpa-
pillaeoccupiedmostofthedorsalaspectoftheTorus linguae;theywerelargerinsize
withsemicircularapices.Filiformpapillae,however,werenumerousanddemonstrated
heavilyonthelateralandrostralpartsofthebodyaswellasontheapexofthetongue.
1 | INTRODUCTION
Camelus dromedarius(one-humpedcamel) isamongthelargestmam-
malianspecies,livesinregionswithhightemperatureanddryclimate
and fed on thorny plants with rough and hard stems (Bello etal.,
2012,2015).The camel’smouthisverysturdyandhasdevelopeda
specialfeaturetomaintainefficient feedingontheseplants (Sui,Su,
&Chen,1983).Thetongueis a muscular organ coveredbymucous
membranewithanumberofsalivaryglandsandnervesembeddedin
betweenthemuscletissues.Onthedorsalsurfaceofthetongue,the
lingualmucosawas thrown into projections called thelingual papil-
lae (Dyce, Sack, & Wensing, 1996; Sisson & Grossman, 1975). The
lingual papillae fulfil diverse functions during food intake,transport
andswallowing(Abbateetal.,2008;Skieresz-Szewczyk&Jackowiak,
2017).Thelingual papillae in camels,likeothermammalian species,
were classified into mechanical and gustatory papillae. Mechanical
papillae, as previously described, include filiform, lentiform, conical
andwart-likepapillae (Qayyum, Fatani,&Mohajir,1988).Gustatory
papillaewithtastebudsarefungiformandcircumvallate(Erdunchaolu
etal.,2001; Qayyum etal., 1988; Salehietal., 2010). Foliategusta-
torypapillaedemonstratedinothervertebrates(Abbateetal.,2009,
2010;Abd-Elnaeim, Zayed,&Leiser,2002)have notbeendescribed
in the one-humped camel (Dyce etal., 1996).Themorphogenesis of
thetongueanditspapillaewasinvestigatedinvariousmammalssuch
asmouse(Iwasaki,Okumura,&Kumakura,1999;Iwasaki,Yoshizawa,
&Kawahara,1996),goats(Shawulu,Kwari, &Abgyal,2012),human
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   ABOU- ELHAMD Et AL.
(Bradley& Stern,1967),rabbit(Elnasharty, Sharaby,& El-Din,2013)
andsheep (Hejazi & Baroughi, 2013). Mostpreviousstudies on the
prenatal development of the camel’s lingual papillae (Abd-Elnaeim,
Kelany,Dorreia,&Abdel-Moneim,2008; Bello,Alimi,Umaru,&Onu,
2015;Belloetal.,2014;Bello,Alimi,Sonfada,etal.,2015; Dougbag,
1987a,b;Salehi etal., 2010)describedindividuallingualpapillae and
havenotgivenageneraloutlineoftheirmorphogenesisandtimingof
theirdifferentiation.Inourpreviousreport(Gad-Allah,Abou-Elhamd,
Abdelmonem,& Zayed,2015),wediscussedtheveryearlystages of
development of the tongue ofone-humpedcamel. The aim of this
studywastocompleteourinvestigationaboutthemorphogenesisof
thecamel’stongueanditspapillaeduringprenatallifeusinglightand
scanningelectron microscopethatmayhelpinbetterunderstanding
the relationships between the lingual morphology and the feeding
habitsinthisuniquespecies.
2 | MATERIAL AND METHODS
This study was made on 24 camel fetuses of CVRL ranging from
10.5cmCVRLto105cmCVRL.Theageofthefetuseswascalcu-
latedusing the equation: Age=(CVRL+23.99)/0.366 accordingto
Elwishy,Hemeida,Omar,Mobarak,andElSayed(1981). Camel fe-
tuses were collected from Cairo Slaughter house; then, they were
classifiedintothreegroupsrepresentingthethreetrimestersofpre-
natal life; ten in the first, nine in the second and five in the third
trimester.Fetusesinthefirsttrimesterranged from 10.5 to 28cm
CVRL(94–142days),inthesecondtrimesterfrom32to60cmCVRL
(152–229days)while inthethird trimester theyrangedfrom 70to
105cmCVRL(256–352days).Afterinvestigation ofthegrossmor-
phologyofthewholetongue,smallpiecesofthelingualmucosaand
underlyinglingual tissue inthe root, bodyand apex of the tongue
weretakenandprocessedforlightandscanningelectronmicroscopy.
Forlightmicroscopy,smalltissueblockswerefixedinneutralbuffer
formalin, washed under tap water, dehydrated in graded ethanol,
clearedinmethylbenzoateandembeddedinparaffinwax.Three-to
five-micrometre-thickparaffinsectionsweremadeandstainedwith
haematoxylinandeosin,trichrome, PASandalcianbluestains,then
examinedand photographed microscopically. Forscanningelectron
microscopy, small tissue blocks with the covering lingual mucosa
werefixed inmixtureofparaformaldehyde solution(2.5%)and glu-
taraldehydesolution(2.5%)in phosphate buffer (pH 7.3) for 24hr.
Sampleswerethenwashedin0.1Mphosphatebuffer,dehydrated
inascending grades of ethanol,critical point-dried inliquid carbon
dioxideandthencoatedwithgoldpalladiusinsputteringdevice.The
sampleswerethenexaminedandphotographedusingJSM-5400LV
Scanningelectron microscopeoperatedat20 KV intheEM Center
ofAssiutUniversity.
Thestudywasconductedinaccordancewiththeapprovalandguide-
linessetoutbytheEthicsCommissionatAssiutUniversityinEgypt.
3 | RESULTS
Thedromedarylingualpapillaepresentspecificgrossanatomicaldur-
ingprenataldevelopment.
3.1 | First trimester (94–142 days)
The tongue appeared elongated with a flat surface and almost uni-
forminthicknessandwidththroughoutitslength(Figures1aand2b).
Lingualpapillae were demonstrated on the lingual root(2b). Lingual
bodyandtheapexwerealmostfreeofpapillaeexceptforsomescat-
teredepithelialprojectionsespeciallyonthelateralpartsofthedorsum
ofthe body. The earlyformed lingual groove appearedon the mid-
sagittallineoftheDorsum linguae(Figure2a,b).Thesurfaceepithelium
isformed of stratified cuboidal epithelium (Figure3a). Theprimordia
of circumvallate and lentiform papillae were clearly demonstrated
onthe lingual root (Figure3a). Thecircumvallatepapillaappearedas
smallprominencessurroundedbycirculargroovesandanannularpad
(Figure3b). The circular groove of circumvallate papilla was formed
asa resultofsequestering epithelial cells(3c).Some epithelial placo-
desappearedonthelingualbodyresultingfromdifferentialepithelial
growthrepresentingtheprimordiaoffungiformpapillae(Figure3d–f).
3.2 | Second trimester (152–229 days)
The tongue attained a more elongated form with tapering end
(Figure1b). The covering lingual epithelium displayed the features
of keratinized stratified squamous epithelium on both papillary and
interpapillarydorsallingualsurface. The circumvallate and lentiform
papillaeweredemonstratedonlyontherootofthetongue.Thelenti-
formpapillaeappearedcoveringalltherootofthetongueexceptthe
areaoccupied bythecircumvallate papillae,andtheywere arranged
laterallyintworows(4–5each)oneithersideofthelingualroot.They
appearedassmallprominencesurroundedbycirculargroovesandan-
nularpadsofthesurroundinglingualmucosa(Figure4a,c).Tastepores
wereobserved in the areabetweenthecircumvallategustatory fur-
rowandthesurroundingsurfaceepitheliumofthetongue(Figure4b).
FIGURE1 AGrossphotographshowingfetalcameltongues
atdifferentstagesofdevelopment:(a)(firsttrimester),(b)(second
trimester)and(c)(thirdtrimester).Abbreviations:A;apex,B;body,R;
root.NotetheprominentTorus linguaeintherootregioninthethird
trimester
(a)
(b)
(c)
    
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ABOU- ELHAMD Et AL.
Inthisstage,shortnumerousfiliformpapillae,whichappearedas
dome-like elevations, wereobserved laterally on the rostral part of
thebodyandtheapexandofthetongue.Manythread-likeepithelial
projectionswereseenamongthem(Figure4f,g).Thefungiformpapil-
laeweredemonstratedamidstthefiliformpapillae.Inthisstage,taste
budswerefirstseenonthetopofthesepapillaewithwell-demarcated
tastepores(Figure4e,h).
3.3 | Third trimester (256–352 days)
Inthisstage,thetonguewaswelldevelopedandattainedtheform
of adult tongue with prominent Torus linguae. All lingual papil-
lae were clearly demonstrated on the dorsum of the root, body
and apex of the tongue (Figure1c). The gustatory papillae (cir-
cumvallateand fungiform) had well-developed taste buds, which
showed basal, supporting and neuroepithelial cells. The taste
poresweredemonstratedonthefreeand lateral surfaces of the
papillae (Figure5a,c,e). Axons of neuroepithelial cells were seen
penetratingthesubepithelial connective tissue (Figure5c). In ad-
dition,Ebner’s glands were well developed and theirducts were
seenpenetratingthegustatoryfurrow(DataS1).Theseglandswere
negativetoPASandalcianbluereactions(DataS2).Thefungiform
papillaewere roundedandeach onewassurroundedby apromi-
nentgroove;tasteporesweredemonstratedontheirfreesurfaces.
Lentiform papillae were numerous and larger in size with semi-
circularapices(Figure5g),andtheycoveralmost all of the Torus
linguae except areas occupied by circumvallate papillae. Filiform
papillae, however, were more numerous and larger in size; they
weredemonstrated heavilyonthelateral androstralpartsof the
bodyaswellasontheapex(Figure5f).
4 | DISCUSSION
Thepresentstudywascarriedouton24camelfetuses(94–352days)
toinvestigatethedevelopmentalchangesinthetongueanditspapil-
laeduringthethreetrimestersoftheprenatallife.
In agreement with Saidu etal. (2015) and Bello,Alimi, Sonfada,
etal.(2015),thetongueappearedelongatedwithflatsurfaceandal-
mostuniform thicknessandwidth throughoutits length inallstages
ofdevelopment.
Thecamellingualepithelium,asdemonstratedinthecurrentstudy,
experiencedthefirstappearanceofpapillaewhenthisepitheliumat-
tainedastratifiedform.SimilarconclusionhasbeenreportedbyHejazi
andBaroughi(2013),whomentionedthatthetimeofemergenceand
growthof the lingual papillae accompanytheformationofstratified
squamousepithelium.Ina studyonthe Geomyid & Heteromyidro-
dents(Frederick,Stangl,&Russell,1994)statedthatmechanicalpapil-
laearethefirstdifferentiatedlingual papillae and gustatorypapillae
withtaste budcellsarethelastto appearandtheyemergenearthe
delivery.Thelaststatementdisagreeswithourcurrentfindingswhere
thetiming of emergenceoflingual papillae is a regionalissuewhere
bothmechanical and gustatorypapillaeappearedfirst on the lingual
rootwhilethoseonthe bodyand apexappearedlateron.Moreover,
thefungiform papillae (gustatory papillae) preceded the appearance
offiliformpapillae(mechanicalpapillae)onthe bodyandapexofthe
cameltonguefetuses.
In agreement with previous studies (Erdunchaolu etal., 2001;
Qayyum,Fatani,Mehta,Shaad, & Mustafa, 1991; Saidu etal., 2015;
Salehietal.,2010),thelingualpapillaeinadultcamelsincludefiliform,
lentiform as mechanical papillae and fungiform and circumvallate
asgustatorypapillae.Qayyumetal. (1991) described a specialtype
(wart-like)papillaeincloserelationshipwithcircumvallatepapillae. In
addition,Ramayyaetal.(Ramayya,Babu,Rao,Lakshmi,&Patki,2012)
reportedconicalpapillaeontheperipheryofthedorsalsurfaceofthe
tongue especially on the Torus linguae. According to Qayyum etal.
(1988),the wart-like papillae seen ontherootof the tonguecanbe
classifiedintotwomajortypes:withpointedandbluntends,respec-
tively.Itisclearthatthereisacontroversyinthetypesofmechanical
papillaedemonstratedonthelingualrootofthecamel.Inouropinion
andaccordingto the currentfindings,thecamelhasonly two types
ofmechanical papillae: one onthebodyand apex(filiform) and one
onthe root(lentiformtype)whichsometimeshas apointedend and
describedaswart-likeorbluntendanddescribedasconicalpapillaby
someauthors. Itseemsthatthese aresubtypesoflentiformpapillae
whichmaydeveloppostnatallyastheyhavenotbeendemonstratedin
thecurrentprenatalstudy.
Thepresentstudyshowedthatthecircumvallatepapillaeappeared
earlyinthefirsttrimesterassmallprominencessurroundedbycircular
grooves.Theywerearrangedintworows(4–5ineachraw)oneither
sideoftheTorus linguaeinbetweenthedevelopinglentiformpapillae.
Thenumberofthiskindofgustatorypapillaediffersgreatlyamongspe-
cies(Agungpriyonoetal.,1995;Ateş,Bozkurt,Kozlu,Alan,& DÜzler,
2013; Chamorro, De Paz, Sandoval, & Fernandez, 1986; Chamorro,
Fernandez, De Paz, Pelaez,& Anel, 1994; Erdunchaolu etal., 2001;
FIGURE2 Lightmicrograph(a)andscanningelectronmicrograph
(b)offetalcameltonguesinthefirsttrimestershowinglingual
papillae(arrows)onthelingualroot(R).Lingualbody(B)andapex
(A)arealmostfreeofpapillaeexceptforsomescatteredepithelial
projectionsespeciallyonthelateralaspectsofthebody.The
earlyformedlingualgrooveappearsonthemid-sagittallinein(b)
(asterisks).Noticetheintrinsiclingualmuscle(ILM)andextrinsic
lingualmuscle(ELM)in(a).(a)Isstainedwithhaematoxylinandeosin
(a)
(b)
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   ABOU- ELHAMD Et AL.
Fredericketal.,1994).Itcanbepostulatedthatanimalswithoutfoliate
gustatorypapillaelikecamel havenumerouscircumvallatepapillaein
comparisonwiththosewhichhavefoliatepapillaelikeequines.
Inthe second trimester, taste buds were first observed opening
inthelateralwallofthecircumvallatepapillae.Bythethirdtrimester,
tastebuds wereseen opening onbothdorsaland lateralsurfacesof
thepapillae.Inthesamecontext,Erdunchaoluetal.(2001)andBello,
Alimi,Sonfada, etal.(2015)foundtaste budsonthelateral papillary
surface while (Doughbag, 1988; Salehi etal., 2010) observed taste
budsonthedorsalsurfaceofthecircumvallatepapillaeofdeveloping
cameltongue.Inadultcamel,ElSharapy(ElSharaby,2006;ElSharaby,
Alsafy,El-Gendy,&Wakisaka,2012)mentionedthatthefreesurface
ofthe circumvallatepapillae isfreeoftasteporeandmost of them
werelocatedalongthemedialwallepitheliumandoccasionallyinthe
lateralwall.Thelastresultsinadultcamelsmaybeduetoapostnatal
modulationofthepapillaryepitheliumasaresultofcellularinvolution
thatmayaccompanyincreasingdepthsofthepapillarycirculargrooves
duringpostnataldevelopment.
PrematureEbner’sglandswereobservedin thethirdtrimesterin
thedeeperpartsofthecircumvallatepapillaeandtheywereopening
intothegustatoryfurrow.TheyshowednegativereactivitytoPASand
alcianbluereactionindicatingthattheirsecretionsaremainlyserous
andfree from mucus contents. Sbarbati, Crescimanno,andOsculati
(1999)statedthattheseglandsaremainlyinvolvedinthewashingof
thevallumaroundthe circumvallatepapillae.Thelastauthorsadded
that both circumvallate papillae and Ebner’s glands form a single
functionalunitywhichseemstorepresentanimportantenzyme-and
pheromone-producing system composed of a sensitive (taste buds)
and an effectory (Ebner’sgland) branch linked by feedback mecha-
nismsofcontrol.Theyhypothesizedthatthetastebudslocatedinthe
FIGURE3 Lightandscanningelectron
micrographsoffetalcameltonguesatthe
firsttrimestershowingthedeveloping
circumvallate(a,b,c)andfungiformpapillae
(e,d,f,longarrows).Thesurfaceepithelium
isformedofstratifiedcuboidalepithelium.
Theprimordiumofcircumvallatepapilla
(bluearrow)andlentiformpapillae(blue
arrowhead)isclearlydemonstratedonthe
root(a)whiletheprimordiaoffungiform
papillaeappearonthebody(d)inthe
formofepithelialplacodes(blackarrows).
Noticethatthecircumvallatepapilla
appearsassmallprominencesurrounded
bycirculargroove(arrowheads)andan
annularpad(asterisks).(c)Demonstrates
ahighermagnificationoftheforming
circulargrooveofcircumvallatepapillaby
sequesteringepithelialcells(redarrows).
(f)Demonstratesahighermagnification
ofthedevelopingfungiformpapillainthe
formofepithelialplacodethatresultsfrom
differentialepithelialgrowth.(a,d)Are
stainedwithhaematoxylinandeosin
(a) (d)
(b) (e)
(c) (f)
    
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ABOU- ELHAMD Et AL.
distalportion oftheEbner’sglandsductalsystem canbeconsidered
similartothechemoreceptorcellslocatedinotherportionsofthedi-
gestiveapparatussuchaspancreaticandbileducts.
Inagreementwith thatreportedbyGad-Allah etal. (2015), at
94days of pregnancy, the primordia of the fungi papillae firstly
appeared on the apex ofthe camel tongue and the circumvallate
and lentiform papillae on the root, however, filiform papillae ap-
pearedlater.Thepresentfindings revealedthat fungiformpapillae
appeared as epithelial placodes in the first trimester and became
differentiatedgraduallyinthesecondtothethirdtrimester.Similar
tothatobservedincattle(Chamorroetal.,1986),thebactriancamel
(Erdunchaolu etal., 2001), Akkaraman sheep (Ünsal, Aktumsek,
Celik,& Sur,2003)andreeves’muntjac deer(Zheng&Kobayashi,
2006), dromedary camel (Sharifabad and Salehi, 2014), the taste
buds with taste pores weredemonstrated on the free surface of
thefungiformpapillae.Unlikely,fungiformpapillaeofgoat(Kumar,
Kumar,& Singh,1998; Kurtula & Atalgınb, 2008; Qayyum & Beg,
1975),Japaneseweasels(Furubayashi,Sato,&Ishibashi,1989)and
FIGURE4 Lightandscanningelectron
micrographsoffetalcameltonguesatthe
secondtrimestershowingthepapillaeon
theroot(circumvallate;a,c,dandlentiform
papillae;b)andpapillaeonthebody
(Fungiform;e,handfiliformpapillaef,g).
(d)Demonstratesahighermagnification
oftheareabetweenthecircumvallate
gustatoryfurrowandsurfaceepithelium
ofthetongue.Abbreviations:AP(Annular
pad),F(filiformpapillae),arrowheads(taste
pores),asterisks(gustatoryfurrow).Note
thekeratinizedcoveringepitheliumofthe
lingualpapillae.(a,b,e,f)Arestainedwith
haematoxylinandeosin
(a) (e)
(b) (f)
(c) (g)
(d) (h)
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   ABOU- ELHAMD Et AL.
Egyptiancamel(Korans& Bachir,2004)werewithouttaste buds.
The last finding that fungiform papillae in Egyptian camel lack
tastebuds maybe attributed to amisleading finding due to non-
representingtissuematerials.
Thepresentstudy revealedthat the lentiform papillaewerethe
firstmechanicalpapillaeseen on the lingual surface of camel in the
firsttrimester.InaccordancewithErdunchaoluetal.(2001),onlysim-
pletype of lentiformpapillaewas observedonthedorsalsurface of
thetongueofcamel. However,simpleandcompoundtypeofthese
papillaewasreportedincaprine(Kumaretal.,1998).
Inthe present study,the filiform papillae becameclearlyvisible
in the second trimester of prenatal life then they became heavily
demonstratedon thelateraland rostralpartsofthe bodyas wellas
ontheapex.InaccordancewithQayyumetal.(1988),therewereno
secondary papillaryprojections in the filiform papillae of the camel
tongue.
In agreementwith Hejazi and Baroughi (2013), keratinization of
papillaryepitheliumwasdemonstratedduringembryoniclifeandthat
thereisnorelationshipbetweentheirkeratinizationandthedietofthe
animalafterthebirth.
FIGURE5 Lightandscanningelectron
micrographsoffetalcameltongues
atthethirdtrimestershowingthe
gustatory(circumvallatepapillaea-dand
fungiforme,f)andmechanicalpapillae
(filiformpapillae;e,fandlentiform;g).(d)
Demonstratestastepores(asterisks)in
thegustatoryfurrow(blackarrows)ofthe
circumvallatepapillae.Insetin(a)showsa
highermagnificationofthemarkedarea
withthetastebudsofthecircumvallate
papilla.Noticethetastebudswiththe
axonsofneuroepithelialcellspenetrating
inthesubepithelialconnectivetissuein
(c)(blackarrowheads).Abbreviationsand
shapes:annularpad(AP),Ebner’sgland
(Eg),fungiformpapilla(redarrow),filiform
papillae(F),lentiformpapillae(L),taste
buds(bluearrowheads).(a,e)Arestained
withhaematoxylinandeosin,while(c)is
stainedwithtrichromestain
(a) (e)
(b) (f)
(c)
(d)
(g)
    
|
 7
ABOU- ELHAMD Et AL.
ACKNOWLEDGEMENTS
We are grateful to the technician staffs of the Department of
Anatomy,HistologyandEmbryology,FacultyofveterinaryMedicine,
AssiutUniversity,fortheirhelpandvaluabletechnicalassistance.The
projectisfundedbyAssiutUniversity,Egypt.
CONFLICT OF INTEREST
Theauthorsdeclarenoconflictofinterest.
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How to cite this article:Abou-ElhamdAS,Abd-ElkareemM,
El-ZuhryZayedA.Morphogenesisoflingualpapillaeof
one-humpedcamel(Camelus dromedarius)duringprenatallife:
Alightandscanningelectronmicroscopicstudy.Anat Histol
Embryol. 2017;00:1–8. https://doi.org/10.1111/ahe.12321
... Fungiform, vallate and foliate papillae are related to gustatory function [5] . Morphological and histological structures of lingual papillae are species-specific and regions specific in the same animal to be consistent with the masticatory and gustatory needs [1,6,7] . ...
... One-humped or Arabian camels (Mammalia: Artiodactyla) lives in regions of dry climate with high temperature and feed on thorny plants with rough hard stems. Thus, the camel's oral cavity is so sturdy with special characteristics for ease feeding and taste functions [6] . Moreover, rabbit (Mammalia: Lagomorpha) exhibits modified tongue and teeth as an adaptation to herbivorous diet. ...
... In the current study, only fungiform and circumvallate papillae were detected in camels, while the three gustatory papillae including foliate papillae were observed in rabbits. Some reports [6,[29][30][31] displayed parallel results in camels that exhibited a huge size of lingual papillae dissimilar to some vertebrates including rabbits [32] . Concurrently, others [33,34] proposed that the broad top of fungiform papillae designated to increase the surface areas and serve for the sensory taste organs. ...
... 6c LM of sagittal and 6d LM of horizontal sections of rabbit's tongue apex at 2 months showing multiple and elongated secondary papillae (arrows), H&E staining Oakley 1987), in mice (Toprak and Yilmaz 2016), in hamster (Whitehead and Kachele 1994) and in cat (Haddad et al. 2019). While in animals having a long gestational period, most of their developmental differentiations occurred during the prenatal life, and complete their maturation postnatal as in camel (Abou-Elhamd et al. 2018). ...
... Moreover, the serous acini increased forming lobulations at 1-2 months. Similar results were recorded in rabbits (Kulawik et al. 2013), in rat (Asar et al. 1996), in hamster (Paliwal et al. 2006) and in camel (Abou-Elhamd et al. 2018). Moreover, the acini of von Ebner's glands are serous. ...
... They have similar shapes but differ in their number and pattern of distribution according to the type of gustatory papilla. They developed on the dorsal surface of the fungiform papillae in hamster (Whitehead and Kachele 1994) and in camel (Abou-Elhamd et al. 2018), on lateral and medial sides of the foliate and vallate papillae in rabbit (Elnasharty et al. 2013) and in rat (Asar et al. 1996). Sometimes apical taste buds were observed in rabbit vallate papillae (Elnasharty et al. 2013). ...
Article
This study aimed to investigate the postnatal morphological features of rabbit’s lingual gustatory papillae using histological, histochemical, morphometrical and scanning electron microscopical studies. A total of 48 New Zealand rabbits (1, 7, 15, 23, 30, 60 days postnatal) were used as the material. Tongue consisted of an apex, body and root with three types of gustatory papillae fungiform, vallate and foliate. Rounded to oval fungiform papillae were distributed on lingual apex among filiform papillae. Two foliate papillae on lateroposterior side have parallel folia increased progressively in number (14–20) with age advancement. Two oval vallate papillae on lingual root surrounded by annular grooves. Histologically, the gustatory papillary epithelium was thin at birth then increased in stratification and cornification from third to fourth week. Vallate and foliate grooves were shallow in newborns then grew deeply by desquamation of their lining epithelium which completely opened and connected with lingual excretory ducts at 23 days. Developing serous von Ebner’s glands appeared at 23 days and became lobulated form 1–2 months. They gave a negative reaction with Periodic Acid Schiff–Alcian blue stain, while mucous Weber's glands showed Alcian blue positive reaction. Taste buds were firstly seen at 15 days old, increased in number and size and became mature with taste pores from third to fourth week. They distributed dorsally on fungiform and on lateral sides of vallate and foliate. This structural adaptation and maturity of gustatory papillae to meet the functional demands of food ingestion during the transition from suckling to dry matter feeding.
... Generally, the vallate papillae are classified as gustatory papillae with taste buds (Abou-Elhamd et al., 2018). Each papilla is encircled by a papillary groove and an annular pad of the surrounding lingual mucosa (Qayyum et al., 1988). ...
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The present study aimed at investigating the histological structures of the vallate papillae of the tongue of the dromedary camel. Samples were taken from the tongues of 5 healthy adult dromedary camels, then processed by standard routine histological technique. The vallate papillae were broad, encircled by a distinctive sulcus, and exhibited concave dorsal surfaces. The papillae were covered with stratified squamous epithelium which was made up of several layers of cells arranged from the basement membrane to the outer surface as follows: basal layer; spinosum layer; squamous layer; corneum layer. The lamina propria sub mucosa showed two well-defined layers. The first one was located beneath the epithelium and characterized by loose connective tissue. The second layer was much thicker and composed mainly of dense irregular collagenous fibres. Deep to the circumvallate papilla was a group of prominent tubulo-acinar glands (von Ebner’s glands). The main ducts of the glands opened directly into the surrounding sulcus at different levels. In general, the histological structures of the vallate papillae of the dromedary camel were similar to those of other domestic mammals. The well-developed von Ebner’s glands suggested their abundant serous secretion that reflected on the high capability of gustation.
... All specimens were mounted on aluminum stubs covered with carbon tabs, sputtered with gold. The prepared specimens were examined and photographed using JEOL scanning electron microscopy (JSM-5400) at an accelerating voltage of 15kv in the electron microscope unit of Assiut University 26 . The nomenclature used in the present study was coped with the (Nomina Anatomica Avium) as well as that was synonymized and homologized with names in previous and recent studies of the chicken and other avian species by different authors. ...
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To understand the development of the mucous preglottal salivary gland in Coturnix japonica (Japanese quail), morphological and histochemical studies were performed on 20 healthy Japanese quail embryos (aging from 10 th to 17 th incubation days) and 25 healthy quail chicks (aging from 0 th to 60 th days). The primordia of preglottal salivary gland was observed as an epithelial bud at the early embryonic stage, which then elongated and differentiated into secretory units by the end of this stage. In Japanese quails, the preglottal salivary gland was a mucous polystomatic tubulo-alveolar unpaired gland composed of two lateral portions and a middle one embedded into submucosa of the lingual root. The gland openings accompanied taste pore (8.17 μm) of taste buds associated salivary glands type; some skeletal muscle fibers embedded among secretory lobules extended from muscle cricohyoideus at 14 th day old quail chick. Also, both herbts corpuscles and secretory motor plexus could be detected among secretory lobules. Based on our investigations, the development of preglottal salivary gland could clearly be distinguished in the embryonic stage into prebud and bud stages at 10 th day old, cord and branching stages ended by cavitation at 11 th day old, canalization stage at 13 th day old, lobulation and secretory stages by the 17 th day old. This mucous secretion showed different histochemical reactions ended with highly alcinophilic mucous indicated highly sialomucin (acidic) content. Myoepithelial cells could be demonstrated at 17-day old quail embryo and there after, surrounded the secretory endpieces of the preglottal salivary gland.
Article
To understand the development of the mucous preglottal salivary gland in Coturnix japonica (Japanese quail), morphological and histochemical studies were performed on 20 healthy Japanese quail embryos (aging from 10th to 17th incubation days) and 25 healthy quail chicks (aging from 0th to 60th days). The primordia of preglottal salivary gland were observed as an epithelial bud at the early embryonic stage, which then elongated and differentiated into secretory units by the end of this stage. In Japanese quails, the preglottal salivary gland was a mucous polystomatic tubuloalveolar unpaired gland composed of two lateral portions and a middle one embedded into the submucosa of the lingual root. The gland openings accompanied taste pore (8.17 μm) of taste buds associated salivary glands type; some skeletal muscle fibers embedded among secretory lobules extended from muscle cricohyoideus at 14th day-old quail chick. Also, both herbts corpuscles and secretory motor plexus could be detected among secretory lobules. Based on our investigations, the development of the preglottal salivary gland could clearly be distinguished in the embryonic stage into pre bud and bud stages at 10th day old, cord and branching stages ended by cavitation at 11th day old, canalization stage at 13th day old, lobulation and secretory stages by the 17th day old. The secretory materials showed different histochemical reactions ended with highly alcinophilic mucous indicated highly sialomucin (acidic) content. Myoepithelial cells could be demonstrated at a 17-day old quail embryo and thereafter surrounded the secretory endpieces of the preglottal salivary gland.
Article
The current study was designed to describe the prenatal developmental stages of the rabbit tongue. Thirty‐five embryos of prenatal ages (E16, E19, E23, E25, E28, and Postnatal) were obtained from New Zealand white (NZW) rabbit. The primordia of the tongue were observed on the foundation as early as day 16 prenatal age (E16). The first primordia of lingual papillae were observed that including the primordia of circumvallate papillae at day 19 prenatal (E19). Thickenings of lingual epithelium developed at 19 day prenatal of embryo. At day 23–25 pc, the presence of primordia of foliate papillae was shown in addition to primordia of the fungiform and filiform papillae were found. The development of the final shape of the tongue is a longstanding process that occurs during the prenatal and postnatal life. The first primordia of gustatory papillae appear, and only later primordia of mechanical papillae are formed. In conclusion, the morphogenesis of the tongue and its lingual papillae discussed its herbivorous nature of feeding. The primordia of the tongue observed early at day 16 prenatal age (E16). The first primordia of lingual papillae were observed, which primordia of circumvallate papillae were at day 19 prenatal (E19). Thickenings of lingual epithelium developed at 19 day prenatal of embryo. At day 23–25 pc, primordia of foliate papillae with primordia of fungiform and filiform papillae were found. The development of final lingual shape is a longstanding process and occurs both during the prenatal and postnatal life. The first primordia of gustatory papillae appear, and only later primordia of mechanical papillae are formed.
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A histomorphological study was conducted on the prenatal development of camel fungiform papillae using standard histomorphological methods. In the research, fifteen Camelus dromedarius foetuses obtained from Sokoto metropolitan abattoir at different gestational ages were used for the study. The fetuses were weighed and grouped according to their gestational ages which were estimated using their crown-vertebral-rump length. Grossly, in all the stages of development, the tongues were observed to be elongated, with flat surfaces and rounded at the apices. At first trimester, the tongues were seen as smooth muscle mass, with almost uniform width and thickness throughout the length. They were uniformly pinkish, no pigmentation and no visual evidence of lingual papillae. At second trimester, the tongues were observed to have taken the normal shape of an adult tongue with variable size and shape of lingual papillae; tapering rostrally from the root to the apex. Biometrically, all the values of weight of the foetuses, the crown – vertebral – rump – length, weight of the head and weight of the tongues were found to be increasing progressively with advancement of gestational from first to third trimester. Histological observations showed that the fungiform papillae were generally lined with keratinised stratified squamous epithelium, which was composed by basal, spinosum, granulosum and corneum layers. Lingual glands located in the deeper parts of the papillae, and they opened into a groove. The surface epithelium was less keratinised compared to that of the surrounding area except the peripheral parts of the papilla. Dermal inter-digitations of variable sizes into the epidermis were observed along the whole surface. Few developing taste buds were observed along the medial papillary wall epithelium of the small-sized papillae at third trimester of age.
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A histomorphological study was conducted on the prenatal development of camel filiform papillae using standard histomorphological methods. In the experiment, fifteen Camelus dromedarius foetuses obtained from Sokoto metropolitan abattoir at different gestational ages were used for the study. The fetuses were weighed and grouped according to their gestational ages which were estimated using their crown-vertebral-rump length. From the fifteen (15) samples used for the study, five (5) belongs to the first trimester, five (5) from the second trimester and five (5) belongs to the third trimester. A total of ten (10) foetuses were males and five (5) were females. Grossly, in all the stages of development, the tongues were observed to be elongated, with flat surfaces and rounded at the apices. At first trimester, the tongues were seen as smooth muscle mass, with almost uniform width and thickness throughout the length. They were uniformly pinkish, no pigmentation and no visual evidence of lingual papillae. At second trimester, the tongues were observed to have taken the normal shape of an adult tongue with variable size and shape of lingual papillae; tapering rostrally from the root to the apex. Biometrically, the weight of the foetuses were found to be 0.18±0.05 to 21.70±7.28kg from the first trimester to third trimester, the crown – vertebral – rump – length were found to be 15.75±4.42 to 94.00±2.83cm from the first trimester to the third trimester, weight of the head were found to be 25.05±15.17 to 1120.00±14.14g and weight of the tongues were found to be 0.79±0.22 to 116.25±11.49g from first trimester to third trimester of age. Histological observations showed that the filiform papillae were generally lined with keratinised stratified squamous epithelium, which was composed by basal, spinosum, granulosum and corneum layers. There was no evidence of lingual glands in all the stages of development.
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Three types of mechanical papillae, i.e., conical, filiform, and hair-like papillae, are present on the tongue in the domestic goose. Within conical papillae, we distinguish three categories: large and small conical papillae on the body and conical papillae on the lingual prominence. The arrangement of mechanical papillae on the tongue in Anseriformes is connected functionally with different feeding mechanisms such as grazing and filter-feeding. The present work aims to determine whether morphology of three types of mechanical papillae in goose at the time of hatching is the same as in an adult bird and if the tongue is prepared to fulfill feeding function. Our results revealed that the primordia of the large conical papillae start to develop during the differentiation stage. The primordia of the small conical papillae and conical papillae of the lingual papillae start to develop during the growth stage. At the end of the growth stage, only large conical papillae, three pairs of small conical papillae, and conical papillae of the lingual prominence have similar arrangement as in an adult bird. The shape and arrangement of the remaining small conical papillae probably will be changed after hatching. During embryonic period, the filiform papillae and hair-like papillae are not formed. The embryonic epithelium that covered the mechanical papillae undergoes transformation leading to the formation of multilayered epithelium. During prehatching stage, epithelium becomes orthokeratinized epithelium. In conclusion, the tongue of the domestic goose after hatching is well prepared only for grazing. The filtration of food from water is limited due to the lack of filiform papillae.
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Gross morphology and morphometry of apparently normal tongues of forty antenatal and ten adult dromedaries (Camelus dromedarius) of both sexes, procured from the Maiduguri Metropolitan abattoir, were studied. This was with the aim of documenting information on these aspects. The thirteen months dromedary gestation period was divided into four quarters for the purpose of the foetal tongue morphometric study, with ten foetuses per quarter. The prenatal and postnatal tongues were grossly observed to be flat apically and oval basally. They were highly flexible, like other ruminants' tongues, and relatively small to the overall sizes of the study animals. The highest lingual weight percentage of the body weight of 0.39% was attained at the second prenatal growth phase of the dromedary while the least, 0.16%, was attained in the adult. The foetal tongues showed levels of significant increases in sizes and weights throughout the prenatal growth phases. It was concluded that the dromedary tongue is similar to other ruminant tongues and most of the salient gross features, like gustatory and non-gustatory papillae, of the dromedary tongue were already obvious as early as the first prenatal growth phase (2 – 3 months) and the remaining three periods were associated with size increases. In the prenatal dromedary tongues studied, the salient gross features of the tongue were fully evident right from the first quarter of gestation (first three months of prenatal life), but were relatively small in size. Likewise; the mean dimensions and the weights obtained in the present study, showed significant increments across the four-quarters gestation. This is not unrelated with the structural developments of the overall body size and weights.
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The early prenatal development of the tongue of the dromedary resemble in general outline that previously described in other mammals, however species specific differences have not been recognized yet. So the aim of this study to describe the early stages of tongue development in camel by using light and scanning electron microscopes. The current study was carried out on camel embryos ranging from 1.9cm to 10.5cm CVRL (71-94 days of pregnancy). In 1.9cm CVRL embryo, four prominent pharyngeal swellings appeared protruding in the primitive oral cavity representing the four branchial arches. The oral part of the tongue (anterior two thirds) developed from the first branchial arch as the latter gradually overgrew the second one, while the pharyngeal part (caudal third) of the tongue developed from the rostral part of the third branchial arch as demonstrated in 2.4cm CVRL embryos. The first sign of lingual papillae was demonstrated on the surface of the lingual root at 4.7cm CVRL and then after visualized on the body and apex of the tongue at 8.2cm CVRL. Up to 10.4cm CVRL, the investigated lingual papillae included lentiform and vallate papillae on the Torus linguae and fungiform papillae on the body and apex of the tongue, but filiform papillae were not yet developed as visualized by light and scanning electron microscopy. In conclusion, the present work presents the first report regarding the very early prenatal development of the tongue of camel.
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This study aimed at investigating the prenatal development of camel circumvallate papillae using standard histomorphometric methods. In the experiment, fifteen Camelus dromedarius foetuses obtained from Sokoto metropolitan abattoir at different gestational ages were used for the study. The fetuses were weighed and grouped according to their gestational ages which were estimated using their crown-vertebral-rump length. From the fifteen tongues used for the study, five belonged to the foetuses being in the first trimester of prenatal development, five came from the second trimester and the next five from the third trimester. A total of ten foetuses were males and five were females. In all stages of development, the tongues were elongated, with flattened and rounded apex .At the first trimester, the tongues were almost uniform width and thickness throughout the length. They were uniformly pinkish, withoutpigmentation and no visiblelingual papillae. At the second trimester, the tongues were observed to have taken the normal shape of an adult tongue with variable size and shape of lingual papillae; tapering rostrally from the root to the apex. Biometrically, the weight of the foetuses were found to be 0.18±0.05 to 21.70±7.28 kg from the first to the second trimester, the crown – vertebral – rump – length were found to be 15.75±4.42 to 94.00±2.83cm from the first trimester to the third trimester, weight of the head were found to be 25.05±15.17 to 1120.00±14.14g and weight of the tongues were found to be 0.79±0.22 to 116.25±11.49g from first trimester to third trimester. Histological observations showed that the circumvallate papillae were coveredwith keratinized stratified squamous epithelium, which was composed by basal, spinosum, granulosum and corneum layers. Lingual glands were located in the deeper parts of the papillae. The surface of the epithelium was less keratinised compared to that of the surrounding surface except the peripheral parts of the papilla. Dermal inter-digitations of variable sizes into the epidermis were observed along the whole surface. Few taste buds were observed along the medial papillary wall epithelium of the small-sized papillae.
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This study aimed at investigating the prenatal development of camel circumvallates papillae using standard histomorphometric methods. In the experiment, fifteen Camelus dromedarius foetuses obtained from Sokoto metropolitan abattoir at different gestational ages were used for the study. The fetuses were weighed and grouped according to their gestational ages, which were estimated using their crown-vertebral-rump length. From the fifteen (15) samples used for the study, five (5) belongs to the first trimester, five (5) from the second trimester and five (5) belongs to the third trimester. A total of ten (10) foetuses were males and five (5) were females. Grossly, in all the stages of development, the tongues were observed to be elongated, with flat surfaces and rounded at the apices. At first trimester, the tongues were seen as smooth muscle mass, with almost uniform width and thickness throughout the length. They were uniformly pinkish, no pigmentation and no visual evidence of lingual papillae. At second trimester, the tongues were observed to have taken the normal shape of an adult tongue with variable size and shape of lingual papillae; tapering rostrally from the root to the apex. Biometrically, the weight of the foetuses were found to be 0.18±0.05 to 21.70±7.28 kg from the first trimester to second trimester, the crown – vertebral – rump – length were found to be 15.75±4.42 to 94.00±2.83 cm from the first trimester to the third trimester, weight of the head were found to be 25.05±15.17 to 1120.00±14.14 g and weight of the tongues were found to be 0.79±0.22 to 116.25±11.4 9g from first trimester to third trimester. Histological observations showed that the circumvallate papillae were generally lined with keratinised stratified squamous epithelium, which was composed by basal, spinosum, granulosum and corneum layers. Lingual glands are located in the deeper parts of the papillae. The surface epithelium was less keratinised compared to that of the surrounding surface except the peripheral parts of the papilla. Dermal interdigitations of variable sizes into the epidermis were observed along the whole surface. Few taste buds were observed along the medial papillary wall epithelium of the small-sized papillae
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A Histomorphological study was conducted on the oesophagus of 35 foetuses of the one-humped camel collected from the Sokoto metropolitan abattoir, over a period of five months at different gestational ages. The approximate age of the foetuses was estimated from the crown vertebral rump length (CVRL) and samples were categorised into first, second and third trimester. At the first trimester, only three layers were identified, ie; Tunica mucosa, Tunica muscularis and Tunica adventitia. At the second trimester, the orientation of fibres changed, resembling that of the adult with all the four layers prominent i.e. Tunica mucosa, Tunica sub-mucosa, Tunica muscularis and Tunica adventitia. At the third trimester, the Oesophageal gland appeared prominently in the tunica sub-mucosa resembling that of the adult camel. The Tunica mucosa epithelium was simple squamous epithelium at first trimester and began to change at second trimester to stratified squamous epithelium. At third trimester, the epithelium was keratinized stratified squamous epithelium with the oesophageal (sub-mucosal) glands appearing to be prominent and abundant. The tunica muscularis showed clearly a single layer at second trimester while at third trimester; both inner circular and outer longitudinal layers appeared. The tunica adventitia 101 was typical. Blood vessels and nerve fibres became very visible at the tunica sub-mucosa and muscularis in third trimester fetuses. Based on the above findings, it showed that development of the camels' oesophagus (based on embryonic stages) was morphological in succession. Presence of keretinised stratified squamous epithelium throughout the length of the oesophagus showed adaptive features of the animal to its environment and mode of feeding. Base on histological differentiation, camels' oesophagus had little/few similarities with true ruminants embryologically.
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The purpose of this study was to investigate quantitatively the relation between the loss of taste sense and the aging in mammals. Various parameters such as the numbers and topographic distributions of fungiform papillae, the numbers and morphology of their taste buds, were studied comparatively for the tongues of young (6-9 months old) and aged (5-6 years old), female and male Akkaraman sheep. Also the lenght and area of the tongues were determined. There was no significant difference between young and old animals in respect to the density and the bud numbers of the fungiform papillae. However, the diameters of the fungiform papillae and their taste buds, and the length and surface area of the tongues of old animals were statistically different from those of the young ones. No significant difference was observed in the numbers of gustatory papillae and taste buds between the aged and the young animals. It is concluded that there is no relation between the loss of the sense of taste and the decrease in the number of papillae and their taste buds with age.
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The tongue of camel consisted of apex, body and the root. The total length of the tongue was 40 cm and the maximum width was noticed at the level of torus linguae. The fossa linguae was absent. Dorsal surface of the tongue showed filiform, fungiform, lenticular and circumvallate papillae. The number of circumvallate papillae was observed to be 4 on right side and 5 on left side on caudolateral aspect of the tongue. Foliate papillae were absent in the tongue of the camel.