Skip to main content
Log in

Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus) — light and scanning electron microscopy

  • Published:
Biologia Aims and scope Submit manuscript

Abstract

The aim of this study was to identify the lingual surface and posterior lingual glands in the red kangaroo (Macropus rufus) using light and scanning electron microscopy (SEM). Haematoxylin and eosin (H&E), Masson-Goldner trichrome and Azan trichrome stainings were used for the histological examinations of both the papillae and concomitant glands, located beneath the body of the papillae. The samples were stained also with Alcian blue pH 2.5 and periodic acid-Schiff for histochemical observations. A scanning electron microscope (Tesla BS–300) was used to examine the lingual surface. Small, giant and elongated filiform mechanical papillae and fungiform, vallate and foliate gustatory papillae were recognized. No typical conical or lenticular papillae were found on the lingual surface. The distribution of each group of papillae varied on the whole surface of the tongue. The majority of the fungiform papillae resembled “bud-like” shapes, and rotund taste buds were present within the fungiform papillae epithelium. The SEM study showed that the apical part of the vallate papilla was oval with an irregular surface. Additionally, the internal wall of this papilla had many intraepithelial cylindrical or rod-shaped taste buds. The papillary leaves did not have any typical appearance, however, the histological study showed the presence of intra-epithelial taste buds in the wall of the foliate papillae area. Furthermore, two types of posterior mixed mucoserous and serous lingual glands were observed. In conclusion, the morphology of the lingual surface as well as the structure of the lingual glands facilitates the consumption of particular foods in the red kangaroo. Additionally, there are typical microstructural features of the red kangaroo tongue, which are different than in other marsupials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abd-Elnaeim M.M.M., Zayed A.E. & Leiser R. 2002. Morphological characteristics of the tongue and its papillae in the donkey (Equus asinus): a light and scanning electron microscopy study. Ann. Anat. 184 5: 473–480. DOI: https://doi.org/10.1016/S0940-9602(02)80081-4

    Article  PubMed  Google Scholar 

  • Abd Murad N. & Hassan N.H. 2010. Anatomical study of the tongue in adult rams. Kufa J. Vet. Med. Sci. 1 2: 48–57.

    Google Scholar 

  • Abe T., Koizumi K. & Kobayashi K. 2001. Comparative morphological studies on the lingual papillae and their connective tissue cores in the Swamp wallaby Wallabia bicolor. Jpn. J. Oral Biol. 43 3: 292–309.

    Article  Google Scholar 

  • Abumandour M.M.A. & El-Bakary R.M.A. 2013a. Morphological and scanning microscopic studies of the tongue of the Egyptian fruit bat (Rousettus aegyptiacus) and their lingual adaptation for its feeding habits. Vet. Res. Commun. 37 3: 229–238. DOI: https://doi.org/10.1007/s11259-013-9567-9

    Article  PubMed  Google Scholar 

  • Abumandour M.M.A. & El-Bakary R.M.A. 2013b. Anatomic reference for morphological and scanning electron microscopic studies of the New Zealand white rabbits tongue (Orycotolagus cuniculus) and their lingual adaptation for its feeding habits. J. Morphol. Sci. 30 4: 254–265.

    Google Scholar 

  • Agungpriyono S., Yamada J., Kitamura N., Nisa C., Sigit K. & Yamamoto Y. 1995. Morphology of the dorsal lingua papillae in the lesser mouse deer, Tragulus javanicus. J. Anat. 187 (Pt 3): 635–640. PMID: 8586562

    PubMed  PubMed Central  Google Scholar 

  • Chamorro C.A., Fernandez J.G., de Paz P., Pelaez B. & Anel L. 1994. Scanning electron microscopy of the wild boar and pig lingual papillae. Histol. Histopathol. 9 4: 657–667. PMID: 7894137

    CAS  PubMed  Google Scholar 

  • Cheng S.J., Huang C.F., Chen Y.C., Lee J.J., Chang H.H., Chen H.M., Chiang M.L., Kuo M.Y., Kok S.H. & Tseng C.Y. 2009. Ultrastructural changes of posterior lingual glands after hypoglossal denervation in hamsters. J. Anat. 214 1: 163–170. DOI: https://doi.org/10.1111/j.1469-7580.2008.01019.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson T.J., Blaney C.E., Munn A.J., Krockenberger A. & Maloney S.K. 2000. Thermoregulation by kangaroos from mesic and arid habitats: influence of temperature on routes of heat loss in eastern grey kangaroos (Macropus giganteus) and red kangaroos (Macropus rufus). Physiol. Biochem. Zool. 73 3: 374–381. PMID: 10893177

    Article  CAS  PubMed  Google Scholar 

  • Docherty B.A., Alpart L.J., Bhatnagar K.P., Burrows A.M. & Smith T.D. 2010. Tongue morphology in infant and adult bushbabies (Otolemur spp.), pp. 257–260. DOI: https://doi.org/10.1007/978-1-4419-6661-2_13. In: Burrows A.M. & Nash L.T. (eds), The Evolution of Exudativory in Primates, Springer, 306 pp. ISBN: 978-1-4419-6660-5. DOI: https://doi.org/10.1007/978-1-4419-6661-2

    Chapter  Google Scholar 

  • 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 3: 147–151. DOI: https://doi.org/10.1111/j.1439-0264.2001.t01-1-0317.x

    Article  PubMed  Google Scholar 

  • El Sharaby A.A., El-Gendy S.A., Alsafy M.A., Nomir A.G. & Wakisaka S. 2014. Morphological variations of the vallate papillae in some mammalian species. Anat. Sci. Int. 89 3: 161–170. DOI: https://doi.org/10.1007/s12565-013-0215-9

    Article  PubMed  Google Scholar 

  • Emura S., Hayakawa D., Chen H. & Shoumura S. 2004. SEM and gross study on the lingual surface of the red kangaroo, Macropus rufus. Acta Scholae Medicinalis Universitatis in Gifu 52 2: 30–35.

    Google Scholar 

  • Emura S., Hayakawa A., Chen H., Shoumura S., Atoji Y. & Agungpriyono S. 2001. SEM study on the dorsal lingual surface of the lesser dog-faced fruit bat (Cynopterus brachyotis). Okajimas Folia Anat. Jpn. 78 4: 123–128. DOI: http://doi.org/https://doi.org/10.2535/ofaj1936.78.4123

    Article  CAS  PubMed  Google Scholar 

  • Emura S., Tamada A., Hayakawa D., Chen H. & Shoumura S. 2000a. Morphology of the dorsal lingual papillae in the black rhinoceros (Diceros bicornis). Anat. Histol. Embryol. 29 6: 371–374. DOI: https://doi.org/10.1046/j.1439-0264.2000.00283.x

    Article  CAS  PubMed  Google Scholar 

  • Emura S., Tamada A., Hayakawa D., Chen H. & Shoumura S. 2000b. Morphology of the dorsal lingual papillae in the Barbary sheep, Ammotragus lervia. Okajimas Folia Anat. Jpn. 77 (2–3): 39–45. DOI: https://doi.org/10.2535/ofaj1936.77.2-339

    Article  Google Scholar 

  • Erdoğan S., Arias S.V. & Pérez W. 2015. Morphology of the lingual surface of South American fur seal (Arctocephalus australis) and sea lion (Otaria flavescens). Microsc. Res. Tech. 78 2: 140–147. DOI: https://doi.org/10.1002/jemt.22456

    Article  PubMed  Google Scholar 

  • Erdoğan S., Arias S.V. & Pérez W. 2016a. Morphofunctional structure of the lingual papillae in three species of South American Camelids: alpaca, guanaco, and llama. Microsc. Res. Tech. 79 2: 61–71. DOI: https://doi.org/10.1002/jemt.22604

    Article  PubMed  Google Scholar 

  • Erdoğan S., Lima M. & Pérez W. 2016b. Anatomical and scanning electron microscopic study of the tongue in the meerkat (Suricata suricatta, Schreber, 1776). Anat. Histol. Embryol. 45 1: 51–59. DOI: https://doi.org/10.1111/ahe.12170.

    Article  PubMed  Google Scholar 

  • Goździewska-Harłajczuk K., Klećkowska-Nawrot J., Janeczek M. & Zawadzki M. 2015. Morphology of the lingual and buccal papillae in alpaca (Vicugna pacos) — light and scanning electron microscopy. Anat. Histol. Embryol. 44 5: 345–360. DOI: https://doi.org/10.1111/ahe.12147

    Article  PubMed  Google Scholar 

  • Gregorin R. 2003. Comparative morphology of the tongue in freetailed bats (Chiroptera, Molosoide). Iheringia Ser. Zool. 93 2: 213–221. DOI: doi:https://doi.org/10.1590/S0073-47212003000200014

    Article  Google Scholar 

  • Harem M.K., Harem I.S., Sari E.K. & Aydin M.F. 2011. Light and scanning electron microscopic study of the dorsal lingual papillae of the Goitered gazelle (Gazelle subgutturosa). J. Anim. Vet. Adv. 10 15: 1906–1913. DOI: https://doi.org/10.3923/javaa.2011.1906.1913

    Article  Google Scholar 

  • Ibira Y., Yokosuka H., Haga-Tsujimura M. & Yoshie S. 2013. Occurrence of gustducin-immunoreactive cells in von Ebner’s glands of guinea pigs. Histochem. Cell Biol. 140 5: 567–574. DOI: https://doi.org/10.1007/s00418-013-1094-9

    CAS  Google Scholar 

  • Inatomi M. & Kobayashi K. 1999. Comparative morphological studies on the tongue and lingual papillae of the Japanese black bear (Carnivora) and the mountain goat (Atriodactyla). Odontology 87 3: 313–328. [in Japanese]

    Google Scholar 

  • Iwasaki S. 2002. Evolution of the structure and function on the vertebrate tongue. J. Anat. 201 1: 1–13. DOI: https://doi.org/10.1046/j.1469-7580.2002.00073.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Iwasaki S., Asami T., Wanichanon 1996. Ultrastructural study of the dorsal lingual epithelium of the soft-shell turtle, Trionix cartilaginous (Cehlonia, Trionychidae). Anat. Rec. 246 3: 305–316. PMID: 8915452

    Article  CAS  PubMed  Google Scholar 

  • Jabbar A.I. 2014. Macroscopical and microscopical observations of the tongue in the Iraqi goat (Capra hircus). Int. J. Adv. Res. 2 6: 642–648.

    Google Scholar 

  • K. Goździewska-Harłajczuk et al. Jackowiak H. & Godynicki S. 2007. Light and scanning electron microscopic study on the structure of the lingual papillae of the feathertail glider (Acrobates pygmeus, Burramyidae, Marsupialia). Anat. Rec. 290 11: 1355–1365. DOI: https://doi.org/10.1002/ar.20606

    Article  Google Scholar 

  • Jackowiak H., Trzcieli´nska-Lorych J., Godynicki S. 2009. The microstructure of lingual papillae in the Egyptian fruit bat (Rousettus aegyptiacus) as observed by light microscopy and scanning electron microscopy. Arch. Histol. Cytol. 72 1: 13–21. DOI: https://doi.org/10.1679/aohc.72.13

    Article  PubMed  Google Scholar 

  • Kobayashi K., Jackowiak H., Frąckowiak H., Yoshimura K., Kumakura M. & Kobayashi K. 2005. Comparative morphological study on the tongue and lingual papillae of horses (Perissodactyla) and selected ruminantia (Atriodactyla). Ital. J. Anat. Embryol. 110 (Suppl. 1, n. 2): 55–63.

    CAS  PubMed  Google Scholar 

  • Kobayashi K., Kumakura M., Yoshimura K., Nonaka K., Murayama T. & Henneberg M. 2003. Comparative morphological study of the lingual papillae and their connective tissue cores of the koala. Anat. Embryol. (Berl.) 206 4: 247–254. DOI: https://doi.org/10.1007/s00429-002-0296-z

    Article  Google Scholar 

  • Kubota K., Kubota J., Fukuda N., Asakura S., Nakagava S. & Masui M. 1963. Comparative anatomical and neurohistological observations on the tongue of the marsupials. Anat. Rec. 147 3: 337–353. DOI: https://doi.org/10.1002/ar.1091470305

    Article  CAS  PubMed  Google Scholar 

  • Kumar P., Kumar S. & Singh Y, 1998. Tongue papillae in goat: a scanning electron microscopic study. Anat. Histol. Embryol. 27 6: 355–357. DOI: https://doi.org/10.1111/j.1439-0264.1998.tb00207.x

    Article  CAS  PubMed  Google Scholar 

  • Kurtul I. & Atalgin S.H. 2008. Scanning electron microscopy study of the lingual papillae of the Saanen goat. Small Rumin. Res. 80 1: 52–56. DOI: https://doi.org/10.1016/j.smallrumres.2008.09.003

    Article  Google Scholar 

  • Mançanares C.A., Santos A.C., Piemonte M.V., Vasconcelos B.G., Carvalho A.F., Miglino M.A., Ambrosio C.E. & Assis Neto A.C. 2012. Macroscopic and microscopic analysis of the tongue of the common opossum (Didelphis marsupialis). Microsc. Res. Tech. 75 10: 1329–1333. DOI: https://doi.org/10.1002/jemt.22070.

    Article  PubMed  Google Scholar 

  • Martinez M., Martinez F.E., Pinheiro P.F.F., Almeida C.C.D., Guida H.L. & Watanabe I. 1998. Light and scanning electron microscopic study of the vallate papillae of the opossum (Didelphis albiventris). Rev. Chil. Anat. 16 1: 67–73. DOI: https://doi.org/10.4067/S0716-98681998000100009

    Article  Google Scholar 

  • Mohebinia S. & Ghassemi F. 2013. Histological study of tongue in insectivore bat (Rhinopoma hardwickii). Adv. Environ. Biol. 7 14: 4643–4648.

    Google Scholar 

  • Munn A.J. & Dawson T.J. 2006. Forage fibre digestion, rates of feed passage and gut fill in juvenile and adult red kangaroos Macropus rufus Desmarest: why body size matters. J. Exp. Biol. 209: 1535–1647. DOI: https://doi.org/10.1242/jeb.02137

    Article  PubMed  Google Scholar 

  • Murtey M. D. & Ramasamy P. 2016. Sample preparations for scanning electron microscopy — life sciences. Chapter 8, pp. 161–185. DOI: https://doi.org/10.5772/61720. In: Janecek M. & Kral R. (eds), Modern Electron Microscopy in Physical and Life Sciences, InTech, CC BY 3.0 license, 298 pp. ISBN: 978-953-51- 2252-4

  • Nonaka K., Zheng J.H. & Kobayashi K. 2008. Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits. Okajimas Folia Anat. Jpn. 85 2: 57–66. DOI: http://doi.org/https://doi.org/10.2535/ofaj.85.57

    Article  PubMed  Google Scholar 

  • Okada S. & Schraufnagel D.E. 2005. Microvasculature of the lingual papillae of the common opossum (Didelphis marsupialis). Microsc. Microanal. 11 (Suppl. S02): 319–332. DOI: doi:https://doi.org/10.1017/S1431927605503660

    Article  CAS  PubMed  Google Scholar 

  • Pastor J.F., Barbosa M. & de Paz F.J. 2008. Morphological study of the lingual papillae of the giant panda (Ailuropoda melanoleuca) by scanning electron microscopy. J. Anat. 212 2: 99–105. DOI: https://doi.org/10.1111/j.1469-7580.2008.00850.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parliament of the Republic of Poland: Ustawa z dnia 21 sierpnia 1997 o ochronie zwierzat. Dziennik Ustaw 1997 Nr 111 poz. 724 z pozn. zmianami. 2012. pp. 3445–3453. http://isap.sejm.gov.pl/DetailsServlet?id=WDU19971110 724

    Google Scholar 

  • Spicer S.C. & Henson J.G. 1967. Methods for localizing mucosubstances in epithelial and connective tissue, pp. 78–112. In: Bajusz E. & Jasmin G. (eds), Series on Methods and Achievements in Experimental Pathology, Vol. 2. Investigative Techniques, S. Karger AG, Basel, Switzerland, 290 pp. ISBN: 978-3-8055-0522-2, 3-8055-0522-1

    Google Scholar 

  • Staker L. 2006. The complete guide to the care of Macropods. Matilda’s Publishing, 437 pp. ISBN: 0977575101, 978097757 5107

    Google Scholar 

  • Trzcieli´nska-Lorych J., Jackowiak H., Skieresz-Szewczyk K. & Godynicki S. 2009. Morphology and morphometry of lingual papillae in adult and newborn egyptian fruit bats (Rousettus aegyptiacus). Anat. Histol. Embryol. 38 5: 370–376. DOI: https://doi.org/10.1111/j.1439-0264.2009.00956.x

    Article  Google Scholar 

  • Ünsaldi E. 2010. Macroscopic and light microscopic structure of fungiform papillae on the tongue of squirrels (Sciurus vulgaris). Kafkas Univ. Vet. Fak. Derg. 16 1: 115–118. DOI: https://doi.org/10.9775/kvfd.2009.530

    Google Scholar 

  • Watanabe I.S., Dos Santos Haemmerle C.A., Dias F.J., Cury D.P., Da Silva M.C., Sosthines M.C., Dos Santos T.C., Guimaraes J.P. & Milino M.A. 2013. Structural characterization of the capybara (Hydrochaeris hydrochaeris) tongue by light, scanning and transmission electron microscopy. Microsc. Tes. Tech. 76 2: 141–155. DOI: https://doi.org/10.1002/jemt.22145

    Article  Google Scholar 

  • Windle B.C.A. & Parsons F.G. 1897. On the anatomy of Macropus rufus. J. Anat. Physiol. 32 (Pt 1): 119–134. PMCID: PMC1327962

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimura K., Natsuki H., Shindoh J., Kobayashi K. & Kageyama I. 2009a. Light and scanning electron microscopic study on the tongue and lingual papillae of the hippopotamus, Hippopotamus amphibious amphibious. Anat. Rec. (Hoboken) 292: 921–934. DOI: https://doi.org/10.1002/ar.20915.

    Article  Google Scholar 

  • Yoshimura K., Shindoh J. & Kageyama I. 2013. Comparative morphology of the papillae linguales and their connective tissue cores in the tongue of the greater Japanese shrew-mole, Urotrichus talpoides. Anat. Histol. Embryol. 42 1: 21–29. DOI: https://doi.org/10.1111/j.1439-0264.2012.01159.x

    Article  CAS  PubMed  Google Scholar 

  • Yoshimura K., Shindoh J. & Kobayashi K. 2009b. Scanning electron microscopic study of the tongue and lingual papillae of the California sea lion, (Zalophus californianus californianus) Anat. Rec. 267 2: 146–153. DOI: https://doi.org/10.1002/ar.10093

    Article  Google Scholar 

  • Zheng J.H. & Kobayashi K. 2006. Comparative morphological study on the lingual papillae and their connective tissue cores (CTC) in revees’ Muntjac deer (Muntiacus reevesi). Ann. Anat. 188 6: 555–564. DOI: https://doi.org/10.1016/j.aanat.2006.05.014

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karolina Goździewska-Harłajczuk.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Goździewska-Harłajczuk, K., Klećkowska-Nawrot, J., Nowaczyk, R. et al. Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus) — light and scanning electron microscopy. Biologia 71, 701–716 (2016). https://doi.org/10.1515/biolog-2016-0082

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/biolog-2016-0082

Key words

Navigation