Abstract
This study was carried out to describe the anatomical, histological and mucinous histochemical characteristics of the tongue in the Persian squirrel. This species is a rodent distributed all over the Middle East and recently has been considered a companion animal. Anatomical observations showed the median sulcus on the apex and absence of a lingual prominence in the body. Light and scanning electron microscopy showed that the filiform papillae cover the entire dorsal surface of the tongue, and their sizes increased approaching the root. The fungiform papillae, which contained 1–4 taste buds, were scattered on the apex, margin, body and root of the tongue. Three vallate papillae were observed on the root, each one surrounded by a groove and crescent pad with taste buds on its lateral walls. The foliate papillae on both margins of the tongue contained several laminae with taste buds. The core of the tongue was composed of lingual glands, skeletal muscles and connective tissues. These glands were confined to the body and root, which were composed of serous cells located anteriorly and mucosal and seromucosal cells placed posteriorly. The mucin histochemistry using the periodic acid-Schiff (PAS), alcian blue (AB) (pH 1.0 and 2.5), PAS–AB (pH 2.5) and aldehyde fuchsin-AB (pH 2.5) techniques showed that the mucosal content included both carboxylated and sulfated acidic mucins with neutral mucins. The results of this study could contribute to the knowledge of the morphological characteristics of the wild animal tongue and provide data for comparison with other rodents.
Similar content being viewed by others
References
Abumandour MM, El-Bakary RM (2013) Morphological and scanning electron microscopic studies of the tongue of the Egyptian fruit bat (Rousettusaegyptiacus) and their lingual adaptation for its feeding habits. Vet Res Commun 37:229–238
Amr ZS, Eid E, Qarqaz MA, Abu Baker MA (2006) The status and distribution of the Persian Squirrel, Sciurus anomalus (Mammalia: Rodentia: Sciuridae), in Dibbeen Nature Reserve. Jordan Zool Abhand 55:199–207
Atalar O, Karan Meryem (2011) The light and scanning electron microscopic structure of the papila vallate in the porpucine (Hystric cristata). J Anim Vet Adv 10:3069–3073
Bancroft JD, Cook HC (1994) Manual of histological techniques and their diagnostic application. Churchill Livingstone, London
Banks WJ (1993) Applied veterinary histology. Mosby-Year book, London
Carvalho ADV, Nogueira JC (1967) Alguns aspectos morfologicos e estuuo histoquimico dos polissacarideos nas glandulas salivares linguais posteriores de mammalia. I. Rodentia (Rattus norvegicus albinus, Mus musculus, Cavia porcellus e Cricetus auratus). Arq Cent Est Fac Qdont 4:95–112
Cheng SJ, Huang CF, Chen YC, Lee JJ, Chang HH, Chen HM, Chiang ML, Kuo MY, Kok SH, Tseng CY (2009) Ultrastructural changes of posterior lingual glands after hypoglossal denervation in hamsters. J Anat 214:163–170
Ciena AP, de Sousa Bolina C, de Almeida SR, Rici RE, de Oliveira MF, da Silva MC, Miglino MA, Watanabe IS (2013) Structural and ultrastructural features of the agouti tongue (Dasyprocta aguti Linnaeus, 1766). J Anat 223:152–158
Cizek P, Hamouzova P, Jekl V, Kvapil P, Tichy F (2016) Light and scanning electron microscopy of the tongue of a degu (Octodon degus). Anat Sci Int. doi:10.1007/s12565-016-0346-x
Eerdunchaolu Takehana K, Yamamoto E, Kobayashi A, Cao G, Baiyin Ueda H, Tangkawattana P (2001) Characteristics of dorsal lingual papillae of the Bactrian camel (Camelus bactrianus). Anat Histol Embryol 30:147–151
El-Bakary RM (1989) Comparative morphological studies on the tongue of some breeds of rabbits; Balady, Giant vlander and Bouscate rabbits. Zagazig Vet J 17:49–61
Emura S, Tamada A, Hayakawa D, Chen H, Jamali M, Taguchi H, Shoumura S (1999) SEM study on the dorsal lingual surface of the flying squirrel, Petaurista leucogenys. Ann Anat 181:495–498
Emura S, Tamada A, Hayakawa D, Chen H, Shoumura S (2001) SEM study on the dorsal lingual surface of the nutria, Myocastor coypus. Acta Anat Nipp 76:233–238
Emura S, Okumura T, Chen H (2011) Morphology of the lingual papillae in the Patagonian cavy. Okajimas Folia Anat Jpn 88:121–125
Goodarzi N (2014) Electron microscope structure of dorsal lingual epithelium of Persian squirrel Sciurus anomalus. Online J Vet Res 18:132–144
Grandi D, Arcari ML, Azalli G (1994) Ultrastructural aspects of the lingual papillae in the gerbil (Meriones unguiculatus). Ital J Anat Embryol 99:201–217
Hellstrand E (1980) Morphological and histochemical properties of tongue muscles in cat. Acta Physiol Scand 110:187–198
Iino T, Kobayashi K (1988) Morphological studies on the lingual papillae and their connective tissue papillae of rat. Shigaku 75:1039–1060
Iwasaki S (2002) Evolution of the structure and function of the vertebrate tongue. J Anat 201:1–13
Iwasaki S, Miyata K (1985) Studies on the lingual dorsal epithelium of the guinea pig by scanning electron microscopy. Okajimas Folia Anat Jpn 61:423–436
Iwasaki S, Miyata K, Mori H, Sakata K, Kobayashi K (1984) Fine structure of the lingual dorsal surface of rats. Kaibogaku Zasshi. J Anat 59:18–27
Iwasaki S, Miyata K, Kobayashi K (1987) The surface structure of the dorsal epithelium of tongue in the mouse. Acta Anat Nippon 62:69–76
Iwasaki S, Yoshizawa H, Kawahara I (1996) Study by scanning electron microscopy of the morphogenesis of three types of lingual papilla in the mouse. Acta Anat 157:41–52
Iwasaki S, Yoshizawa H, Kawahara I (1997) Study by scanning electron microscopy of the morphogenesis of the three types of lingual papilla in the rat. Anat Rec 247:528–554
Jackowiak H, Godynicki S (2004) The scanning electron microscopic study of lingual papillae in the silver fox (Vulpes vulpes fulva, Desmarest, 1820). Ann Anat 186:179–183
Jackowiak H, Godynicki S (2005) The distribution and structure of the lingual papillae on the tongue of the bank vole Clethrinomys glareolus. Folia Morphol (Warsz) 64:326–333
Jackowiak H, Godynicki S, Skieresz-Szewczyk K, Trzcielińska-Lorych J (2009) Scanning electron microscopic study of the lingual papillae in the arctic fox (Alopex lagopus L., 1758). Anat Histol Embryol 38:377–381
Kilinc M, Erdogan S, Ketani S, Ketani MA (2010) Morphological study by scanning electron microscopy of the lingual papillae in the Middle East blind mole rat (Spalax ehrenbergi, Nehring, 1898). Anat Histol Embryol 39:509–515
Kobayashi K (1990) Three-dimensional architecture of the connective tissue core of the lingual papillae in the guinea pig. Anat Embryol 182:205–213
Kobayashi S, Shimamura A (1982) Comparative anatomical observations of the tongue of the Japanese long-fingered bats, Miniopterus schreibersi fulginosus. Okajimas Fol Anat Jpn 58:923–932
Kobayashi K, Miyata K, Takahashi K, Iwasaki S (1989a) Three-dimensional architecture of the connective tissue papillae of the mouse tongue as viewed by scanning electron microscopy. Kaibogaku Zasshi 64:523–538
Kobayashi K, Miyata K, Asami T, Kitajima K, Iwasaki S, Sasagawa I (1989b) Three-dimensional structure of the connective tissue core of the lingual papillae in the crab-eating macaque, (Macacafascicularis). Shigaku (Odontology) 77:1308–1317
Konig HE, Leibich HG (2004) Veterinary anatomy of domestic mammals text book and colour atlas. Schattauer, New York
Kubota K, Togawa S (1966) Comparative anatomical and neurohistological observations on the tongue of Japanese dormouse (Glirus japonicus). Anat Rec 154:545–552
Kubota K, Fukuda N, Asakura S (1966) Comparative anatomical and neurohistological observations on the tongue of the porcupine (Hystrix cristata). Anat Rec 155:261–268
Kulawik M, Godynicki S (2007) Vallate papillae in the domestic rabbit (Oryctolagus cuniculus f. domestica). Pol J Vet Sci 10:47–50
Kumara P, Kumara S, Singh S (1998) Tongue papillae in the goat: a scanning electron-microscopic study. Anat Histol Embryol 27:355–357
Levin MJ, Pfeiffer CJ (2002) Gross and microscopic observations on the lingual structure of the Florida Manatee Trichechus manatus latirostris. Anat Histol Embryol 31:278–285
Li XJ, Snyder SH (1995) Molecular cloning of Ebnerin, a von Ebner’s gland protein associated with taste buds. J Biol Chem 270:17674–17679
Lopes MG, Watanabe IS, Soares LE et al (2009) Ultrastructural aspects of female aging Wistar rat epithelium tongue: a HRSEM and TEM study. Gerontology 55:442–448
Matsuo R (2000) Role of Saliva in the Maintenance of Taste Sensitivity. Crit Rev Oral Biol Med 11(2):216–229
Melgarejo MP, Hellín MD, Melgarejo MC (1999) Histochemical study with lectins submucous glands of the hamster’s tongue. An Otorrinolaringol Ibero Am 26:249–255
Miller IJ, Preslar AJ (1974) Spatial distribution of rat fungiform papillae. Anat Rec 181:679–684
Miller IJ, Smith DV (1984) Quantitative taste bud distribution in the hamster. Physiol Behav 32:275–285
Mowry RW (1956) Observations on the use of sulphuric ether for the sulphation of hydroxyl groups in tissue sections. J Histochem Cytochem 4:407
Nagato T, Ren XZ, Toh H, Tandler B (1997) Ultrastructure of Weber’s salivary glands of the root of the tongue in the rat. Anat Rec 249:435–440
Nogueira JC, de Carvalho AD (1973) Histochemistry of the mucins in the posterior lingual salivary glands of some mammals. Rev Bras Pesqui Med Biol 6:267–274
Nomina Anatomica Veterinaria (NAV) (2012) International committee on veterinary gross anatomical nomenclature. World Association of Veterinary Anatomists
Nonaka K, Zheng JH, Kobayashi K (2008) Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits. Okajimas Folia Anat Jpn 85:57–66
Paliwal A, Srikantan S, De PK, Hand AR, Redman RS (2006) Histological and biochemical characterization of von Ebner’s glands in the Syrian hamster; comparison with ratvon Ebner’s glands. Biotech Histochem 81:139–149
Parks JD, Whitehead MC (1998) Scanning electron microscopy of denervated taste buds in hamster: morphology of fungiform taste pores. Anat Rec 25:230–239
Pinkstaff CA (1980) The cytology of the salivary glands. Int Rev Cytol 63:142–261
Qayyum MA, Fatani JA, Mohajir AM (1988) Scanning electron microscopic study of the lingual papillae of the one humped camel, Camelus dromedarius. J Anat 160:21–26
Reginato Gde S, Bolina Cde S, Watanabe IS, Ciena AP (2014) Three-dimensional aspects of the lingual papillae and their connective tissue cores in the tongue of rats: a scanning electron microscope study. Sci World J 2014:841879
Sadeghinezhad J, Tootian Z, Latorre R, Sorteni C, Chiocchetti R (2013) Intrinsic innervation of the Persian squirrel (Sciurus anomalus) ileum. Anat Histol Embryol 42:201–212
Sakr SMI, Taki-El-Deen FMA, Aboelwafa HR (2013) Comparative light and scanning electron microscopic study of the lingual papillae in three different mammalian animals; Hemiechinus auritus (Erinaceomorpha: Erinaceidae), Cavia porcellus (Rodentia: Caviidae) and Mustela nivalis vulgaris (Carnivora: Mustelidae). Life Sci J Acta Zhengzhou Univ Overseas Ed 10:3082–3093
Schumacher U, Duku M, Katoh M, Jurns J, Krause WJ (2004) Histochemical similarities of mucins produced by Brunner’s glands and pyloric glands: a comparative study. Anat Rec A 278A:540–550
Shindo J, Yoshimura K, Kobayashi K (2006) Comparative morphological study on the stereo-structure of the lingual papillae and their connective tissue cores of the American beaver (Castor canadensis). Okajimas Folia Anat Jpn 82:127–137
Spicer SS, Meyer DB (1960) Histochemical differentiation of acid mucopolysaccharides by means of combined aldehyde fuchsin–alcian blue staining. Am J Clin Pathol 33:453–460
Tandler B, Denning CR, Mandel JA, Kutschner A (1969) Ultrastructure of human labial salivary glands. I-Acinar secretory cells. J Morphol 127:338–408
Tandler B, Pinkstaff CA, Riva A (1994) Ultrastructure and histochemistry of human anterior lingual salivary glands (glands of Blandin-Nuhn). Anat Rec 240:167–177
Tandler B, Nagato T, Toyoshima K, Phillips CJ (1997) Ultrastructure of the parotid gland in the common vampire bat, Desmodus rotundus, with special emphasis on oncocytes. J Submicrosc Cytol Pathol 29:37–49
Thorington RW Jr, Darrow K (2000) Anatomy of the squirrel wrist: bones, ligaments, and muscles. J Morphol 246:85–102
Tootian Z, Sadeghinezhad J, Sheibani MT, Fazelipour S, De Sordi N, Chiocchetti R (2013) Histological and mucin histochemical study of the small intestine of the Persian squirrel (Sciurus anomalus). Anat Sci Int 88:38–45
Triantafyllou A, Fletcher D, Scott J (2002) Lipolytic and esterolytic activities in posterior lingual glands of rat: a histochemical study. Histochem J 34:529–533
Unsaldi E (2010) Macroscopic and light microscopic structure of fungiform papillae on the tongue of squirrels (Sciurus vulgaris). Kafkas Univ Vet Fak Derg 16:115–118
Watanabe I, Santos Haemmerle CA, Dias FJ, Cury DP, Silva MCP, Sosthines MCK, Santos TC, Guimaraes JP, Miglino MA (2013) Structural characterization of the capybara (Hydrochaeris hydrochaeris) tongue by light, scanning, and transmission electron microscopy. Microsc Res Tech 76:141–155
Yücel F, Akdoğan I, Güven G, Ortuğ G (2002) SEM examination of the dorsal lingual papillae of pregnant rats. Ann Anat 184:251–255
Zaccone G, Lo Cascio P (1979) Histochemical distribution of acid mucopolysaccharides and some active transport enzymes in the lingual glands of Jaculus jaculus L. (Dipodidae, Mammalia). Acta Histochem 65:116–131
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Rights and permissions
About this article
Cite this article
Sadeghinezhad, J., Tootian, Z. & Javadi, F. Anatomical and histological structure of the tongue and histochemical characteristics of the lingual salivary glands in the Persian squirrel (Sciurus anomalus). Anat Sci Int 93, 58–68 (2018). https://doi.org/10.1007/s12565-016-0367-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12565-016-0367-5