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Submitted: 2021-02-19
Accepted: 2021-03-28
Published online: 2021-04-28
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Structural and Functional adaptation of the lingual papillae of the Egyptian fruit bat (Rousettus aegyptiacus): Specific Adaptive feeding Strategies

R. M. Kandyel1, M. M.A. Abumandour2, S. F. Mahmoud3, M. Shukry4, N. Madkour2, A. El-Mansi56, F. A. Farrag7
DOI: 10.5603/FM.a2021.0042
·
Pubmed: 33954957
Affiliations
  1. Tanta University Faculty of Science, Department of Zoology, Faculty of Science, Tanta University, Egypt., Tanta, Egypt
  2. Anatomy and Embryology Department, Faculty of Veterinary Medicine, Alexandria University, Alexandria, Egypt
  3. Department of Biotechnology, College of Science, Taif University,, Department of Biotechnology, College of Science, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia, Taif, Saudi Arabia
  4. Faculty of Veterinary Medicine, Kafrelsheikh University, Department of Physiology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33511 Kafrelsheikh, Egypt., Kafrelsheikh, Egypt
  5. Biology Department, Faculty of Science, King Khalid University, Abha, Saudi Arabia
  6. Zoology Department, Faculty of Science, Mansoura University, Mansoura, Egypt
  7. Faculty of Veterinary Medicine, Kafrelsheikh University, Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, 33511 Kafrelsheikh, Egypt., Kafrelsheikh, Egypt

open access

Ahead of Print
ORIGINAL ARTICLES
Submitted: 2021-02-19
Accepted: 2021-03-28
Published online: 2021-04-28

Abstract

The current investigation was directed to clarify the correlations between the feeding strategy and lingual structure of the Egyptian fruit bat captured from the Egyptian east desert. The current work depends on twelve adult Egyptian fruit bats that observed grossly and with the help of the stereo, light, and scanning electron microscope. There were three types of the lingual papillae; one mechanical filiform and two gustatory (fungiform and circumvallate). There were seven subtypes of filiform papillae were recognized on the seven lingual regions. There were scanty numbers of fungiform papillae distributed among the filiform papillae on the lingual tip and two lateral parts of apex and body while fungiform papillae completely absent in the median part. There were three circumvallate papillae. The central bulb of circumvallate papillae surrounded by one layer of two segmented circular annular bad. The lingual tip had cornflower-like and diamond-shaped filiform papillae. Histochemical results revealed that the lingual glands were a stronger AB-positive reaction and gave dark blue color, while the reaction for the PAS-stain was negative. Also, the glands exhibited a blue color as an indication of positive AB reactivity with combined AB-PAS staining.

Abstract

The current investigation was directed to clarify the correlations between the feeding strategy and lingual structure of the Egyptian fruit bat captured from the Egyptian east desert. The current work depends on twelve adult Egyptian fruit bats that observed grossly and with the help of the stereo, light, and scanning electron microscope. There were three types of the lingual papillae; one mechanical filiform and two gustatory (fungiform and circumvallate). There were seven subtypes of filiform papillae were recognized on the seven lingual regions. There were scanty numbers of fungiform papillae distributed among the filiform papillae on the lingual tip and two lateral parts of apex and body while fungiform papillae completely absent in the median part. There were three circumvallate papillae. The central bulb of circumvallate papillae surrounded by one layer of two segmented circular annular bad. The lingual tip had cornflower-like and diamond-shaped filiform papillae. Histochemical results revealed that the lingual glands were a stronger AB-positive reaction and gave dark blue color, while the reaction for the PAS-stain was negative. Also, the glands exhibited a blue color as an indication of positive AB reactivity with combined AB-PAS staining.

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Keywords

Egyptian fruit bat, lingual papillae, scanning electron microscope (SEM), histology, histochemical examination

About this article
Title

Structural and Functional adaptation of the lingual papillae of the Egyptian fruit bat (Rousettus aegyptiacus): Specific Adaptive feeding Strategies

Journal

Folia Morphologica

Issue

Ahead of Print

Article type

Original article

Published online

2021-04-28

Page views

622

Article views/downloads

430

DOI

10.5603/FM.a2021.0042

Pubmed

33954957

Keywords

Egyptian fruit bat
lingual papillae
scanning electron microscope (SEM)
histology
histochemical examination

Authors

R. M. Kandyel
M. M.A. Abumandour
S. F. Mahmoud
M. Shukry
N. Madkour
A. El-Mansi
F. A. Farrag

References (64)
  1. Aboelnour A, Noreldin AE, Massoud D, et al. Retinal characterization in the eyes of two bats endemic in the Egyptian fauna, the Egyptian fruit bat (Rousettus aegyptiacus) and insectivorous bat (Pipistrellus kuhlii), using the light microscope and transmission electron microscope. Microsc Res Tech. 2020; 83(11): 1391–1400.
  2. Abumandour M. Morphological Comparison of the Filiform Papillae of New Zealand White Rabbits (Oryctolagus cuniculus) as Domestic Mammals and Egyptian Fruit Bat (Rousettus aegyptiacus) as Wild Mammals Using Scanning Electron Microscopic Specimens. Int J Morphol. 2014; 32(4): 1407–1417.
  3. Abumandour MMA, El-Bakary RMA. Anatomic reference for morphological and scanning electron microscopic studies of the New Zealand white rabbits tongue (Orycotolagus cuniculus) and their lingual adaptation for feeding habits. J Morphol Sci. 2013; 30(4): 1–12.
  4. Abumandour MMA, El-Bakary RMA. Morphological and scanning electron microscopic studies of the tongue of the Egyptian fruit bat (Rousettus aegyptiacus) and their lingual adaptation for its feeding habits. Vet Res Commun. 2013; 37(3): 229–238.
  5. Akbari G, Babaei M, Hassanzadeh B. Morphological study of the European hedgehog (Erinaceus europaeus) tongue by SEM and LM. Anat Sci Int. 2018; 93(2): 207–217.
  6. Altringham JD, McOwat T, Hammond L. Bats: biology and behaviour. Oxford University Press, Oxford 1996.
  7. Birt P, Hall L, Smith G. Ecomorphology of the Tongues of Australian Megachiroptera (Chiroptera: Pteropodidae). Austr J Zool. 1997; 45(4): 369–384.
  8. Boland DJ. Forest Trees of Australia. Thomas Nelson, Melbourne 1984.
  9. Chung YW, Kwun HS. A morphological study on the tongues of the vertebrates. I. Comparative macroscopic and microscopic observations. J Catholic Medical College (Korean). 1977; 30: 531–555.
  10. Ciuccio M, Estecondo S, Casanave EB. Scanning electron microscopy study of the dorsal surface of the tongue of dasypus hybridus (Mammalia, Xenarthra, Dasypodidae). Int J Morphol. 2010; 28(2).
  11. Dinç G, Girgin A, Yllmaz S. Ratlarda papilla fungiformis'in prenatal ve postnatal gelişimi. FFrat Üniv SağlFk Bil Derg. 1995; 9(2): 161–163.
  12. Eby P. Finger-winged night workers: managing forests to conserve the role of grey-headed flying foxes as pollinators and seed dispersers. In: Lunney D. (ed.). Conservation of Australias Forest Fauna. Royal Zoological Society of New South Wales, Mosman 1991: 91–100.
  13. Eby P. The biology and management of flying foxes in New South Wales. New South Wales National Parks and Wildlife Service, Report No. 18 1995.
  14. El-Bakary NER, Abumandour MMA. Morphological studies of the tongue of the egyptian water buffalo (bubalus bubalis) and their lingual papillae adaptation for its feeding habits. Anat Histol Embryol. 2017; 46(5): 474–486.
  15. El-Mansi A, Al-Kahtani MA, Abumandour M. Comparative phenotypic and structural adaptations of tongue and gastrointestinal tract in two bats having different feeding habits captured from Saudi Arabia: Egyptian fruit bat (Rousettus aegyptiacus) and Egyptian tomb bat (Taphozous perforatus). Zoologischer Anzeiger. 2019; 281: 24–38.
  16. El-Sharaby AA, El-Gendy SA, Alsafy MA, et al. Morphological variations of the vallate papillae in some mammalian species. Anat Sci Int. 2014; 89(3): 161–170.
  17. Emura S, Tamada A, Hayakawa D, et al. SEM study on the dorsal lingual surface of the flying squirrel, Petaurista leucogenys. Ann Anat - Anatomischer Anzeiger. 1999; 181(5): 495–498.
  18. Emura S, Hayakawa D, Chen H, et al. SEM study on the dorsal lingual surface of the large flying fox, Pteropus vampyrus. Okajimas Folia Anat Jpn. 2002; 79(4): 113–119.
  19. Emura S, Hayakawa D, Chen H, et al. SEM study on the dorsal lingual surface of the lesser dog-faced fruit bat, Cynopterus brachyotis. Okajimas Folia Anat Jpn. 2001; 78(4): 123–128.
  20. Emura S, Okumura T, Chen H. Morphology of the lingual papillae in the Egyptian rousette bat (Rousettus aegyptiacus). Okajimas Folia Anat Jpn. 2012; 89(3): 61–66.
  21. Gewily DI, Mahmoud FA, Saber SA, et al. Ultrastructural comparison between the tongue of two reptilian species endemic in Egyptian fauna; Bosc's fringe-toed lizard Acanthodactylus boskianus and Sinai fan-fingered gecko Ptyodactylus guttatus. Microsc Res Tech. 2021; 84(9): 1977–1991.
  22. 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. 2016; 71(6): 174–178.
  23. Goździewska-Harłajczuk K, Klećkowska-Nawrot J, Barszcz K, et al. Biological aspects of the tongue morphology of wild-captive WWCPS rats: a histological, histochemical and ultrastructural study. Anat Sci Int. 2018; 93(4): 514–532.
  24. Grandi D, Arcari ML, Azalli G. Ultrastructural aspects of the lingual papillae in the gerbil (Meriones unguiculatus). Ital J Anat Embryol. 1994; 99: 201–217.
  25. Greenbaum IF, Phillips CJ. Comparative anatomy and general histology of tongues of long-nosed bats (Leptonycteris sanborni and L. nivalis) with reference to infestation of oral mites. J Mammal. 1974; 55(3): 489–504.
  26. Gregorin R. Comparative morphology of the tongue in free-tailed bats (Chiroptera, Molossidae). Iheringia. Série Zoologia. 2003; 93(2): 213–221.
  27. Humason GL. Animal tissue techniques. Animal tissue techniques, 1962.
  28. Iwasaki Si. Evolution of the structure and function of the vertebrate tongue. J Anat. 2002; 201(1): 1–13.
  29. Iwasaki S, Yoshizawa H, Kawahara I. Study by scanning electron microscopy of the morphogenesis of three types of lingual papilla in the mouse. Acta Anat (Basel). 1996; 157(1): 41–52.
  30. Iwasaki S, Yoshizawa H, Kawahara I. Study by scanning electron microscopy of the morphogenesis of three types of lingual papilla in the rat. Anat Rec. 1997; 247(4): 528–541, doi: 10.1002/(SICI)1097-0185(199704)247:4<528::AID-AR12>3.0.CO;2-R.
  31. Jackowiak H, Godynicki S. The distribution and structure of the lingual papillae on the tongue of the bank vole Clethrinomys glareolus. Folia Morphol. 2005; 64(4): 326–333.
  32. Jackowiak H, Godynicki S. The scanning electron microscopic study of lingual papillae in the silver fox (Vulpes vulpes fulva, Desmarest, 1820). Ann Anat. 2004; 186(2): 179–183.
  33. Jackowiak H, Ludwig M. Light and scanning electron microscopic study of the structure of the ostrich (Strutio camelus) tongue. Zoolog Sci. 2008; 25(2): 188–194.
  34. Jackowiak H, Trzcielińska-Lorych J, Godynicki S. The microstructure of lingual papillae in the Egyptian fruit bat (Rousettus aegyptiacus) as observed by light microscopy and scanning electron microscopy. Arch Histol Cytol. 2009; 72(1): 13–21.
  35. Jarrar BM, Taib N. Histochemical characterization and distribution of mucosubstances and enzyme activity in the lingual salivary glands of the one-humped camel (Camelus dromedarius). Revue d’élevage et de médecine vétérinaire des pays tropicaux. 1989; 41(1): 63–71.
  36. Kobayashi K, Kumakura M, Yoshimura K, et al. Comparative morphological studies on the stereo structure of the lingual papillae of selected primates using scanning electron microscopy. Ann Anat. 2004; 186(5-6): 525–530.
  37. Kobayashi S, Shimamura A. Comparative anatomical observations of the tongue of the Japanese long-fingered bats, Miniopterus schreibersi fuliginosus. Okajimas Folia Anat Jpn. 1982; 58(4-6): 923–932.
  38. Kurtul I, Atalgın SH. Scanning electron microscopic study on the structure of the lingual papillae of the Saanen goat. Small Ruminant Res. 2008; 80(1-3): 52–56.
  39. Luna LG. Routine staining procedures. Manual of histologic staining methods of the Armed Forces Institute of Pathology. Blakiston Division, McGraw-Hill, New York 1968: 33–46.
  40. Mahmoud MMAE, Ahmed EZ, Rudolf L, et al. Morphological characteristics of the tongue and its papillae in the donkey (Equus asinus): a light and scanning electron microscopical study. Ann Anat - Anatomischer Anzeiger. 2002; 184(5): 473–480.
  41. Massoud D, Abumandour MMA. Anatomical features of the tongue of two chiropterans endemic in the Egyptian fauna; the Egyptian fruit bat (Rousettus aegyptiacus) and insectivorous bat (Pipistrellus kuhlii). Acta Histochem. 2020; 122(2): 151503.
  42. Massoud D, Abumandour MMA. Descriptive studies on the tongue of two micro-mammals inhabiting the Egyptian fauna; the Nile grass rat (Arvicanthis niloticus) and the Egyptian long-eared hedgehog (Hemiechinus auritus). Microsc Res Tech. 2019; 82(9): 1584–1592.
  43. Masuko TS, et al. Comparative Scanning Electron Microscopic Study of the Lingual Papillae in Three Species of Bats (Carollia perspicillata, Glossophaga soricina and Desmodus rotundus). Microsc Microanal. 2007; 13(Suppl 2): 280–281.
  44. Morrison DW. Efficiency of food utilization by fruit bats. Oecologia. 1980; 45(2): 270–273.
  45. Mowry RW. Alcian blue technics for the histochemical study of Alcian carbohydrates. J Histochem Cytochem. 1956; 4: 407–411.
  46. Mqokeli BR, Downs CT. Palatal and lingual adaptations for frugivory and nectarivory in the Wahlberg’s epauletted fruit bat (Epomophorus wahlbergi). Zoomorphology. 2012; 132(1): 111–119.
  47. Nomina Anatomica Veterinaria N. International Committee on Veterinary Gross Anatomical Nomenclature and authorized by the general assembly of the world Association of veterinary Anatomist. Knoxville, 3rd Ed. Ghent. Published by the Editorial Committee Hanover (Germany), Ghent (Belgium), Columbia, MO (USA), Rio de Janeiro (Brazil). 2017.
  48. Park H, Hall E. The gross anatomy of the tongues and stomachs of eight new world bats. Trans Kans Acad Sci (1903-). 1951; 54(1): 64–72.
  49. Park J, Lee JH. Comparative Morphology of the Tongue of Miniopterus schreibersi fuliginosus and Pipistrellus savii. Applied Microscopy. 2009; 39(3): 267–276.
  50. Park J, Lee JH. Morphological Study on the Dorsal Lingual Papillae of Sorex caecutiens Laxmann. Korean J Microscopy. 2009; 39(2): 106–106.
  51. Pastor JF, Moro JA, Verona JA, et al. Morphological study by scanning electron microscopy of the lingual papillae in the common European bat (Pipistrellus pipistrellus). Arch Oral Biol. 1993; 38(7): 597–599.
  52. Prothero DR. The Princeton field guide to prehistoric mammals. Vol. 112. Princeton University Press 2016.
  53. 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. 2018; 93(1): 58–68.
  54. Schwenk K. Morphology of the tongue in the tuatara, Sphenodon punctatus (Reptilia: Lepidosauria), with comments on function and phylogeny. J Morphol. 1986; 188(2): 129–156.
  55. Sharma R, Vidyadaran MK, Zulkifli I, et al. Ecomorphological implications of the microstructures on the tongue of the fawn roundleaf bat, Hipposideros cervinus (Chiroptera: Hipposideridae). Austr J Zool. 1999; 47(4): 405.
  56. Son SW, Lee HJ, Lee JH. Ultrastructural observations of the lingual papillae of the Korean greater horseshoe bat, Rhinolophus ferrumequinum korai. Kyungnam Univ J Basic Sci Res Int (Korean). 2000; 14: 65–72.
  57. Spicer SS, Meyer DB. Histochemical differentiation of acid mucopolysaccharides by means of combined aldehyde fuchsin-alcian blue staining. Am J Clin Pathol. 1960; 33(5_ts): 453–460.
  58. Suvarna SK, Layton C, Bancroft JD. Bancroft's Theory and Practice of Histological Techniques,Expert Consult: Online and Print,7: Bancroft's Theory and Practice of Histological Techniques. Churchill Livingstone Elsevier, Churchill Livingstone 2013.
  59. Tandler B, Toyoshima K, Seta Y, et al. Ultrastructure of the salivary glands in the midtongue of the common vampire bat, Desmodus rotundus. Anat Rec. 1997; 249(2): 196–205, doi: 10.1002/(SICI)1097-0185(199710)249:2<196::AID-AR6>3.0.CO;2-W.
  60. Wilson DE, Reeder DM. Mammal Species of the World. A Taxanomis and Geographic Reference. 2nd Ed. Smithsonium Institution Press, Washington 1993.
  61. Winokur RM. The buccopharyngeal mucosa of the turtles (Testudines). J Morphol. 1988; 196(1): 33–52.
  62. Yoshimura K, Hama N, Shindo J, et al. Light and scanning electron microscopic study on the lingual papillae and their connective tissue cores of the Cape hyrax Procavia capensis. J Anat. 2008; 213(5): 573–582.
  63. Yoshimura K, Shindoh J, Kobayashi K. Scanning electron microscopy study of the tongue and lingual papillae of the California sea lion (Zalophus californianus californianus). Anat Rec. 2002; 267(2): 146–153.
  64. Zheng J, Kobayashi K. Comparative morphological study on the lingual papillae and their connective tissue cores (CTC) in reeves' muntjac deer (Muntiacus reevesi). Ann Anat - Anatomischer Anzeiger. 2006; 188(6): 555–564.

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