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Structural and Functional Characterization of the Tongue and Digestive Tract of Psammophis sibilans (Squamata, Lamprophiidae): Adaptive Strategies for Foraging and Feeding Behaviors

Part of: Micrographia Collection

Published online by Cambridge University Press:  12 May 2020

Ahmed A. El-Mansi Open the ORCID record for Ahmed A. El-Mansi [Opens in a new window] ,
Mohamed A. Al-Kahtani ,
Mohamed M. A. Abumandour  and
Ahmed E. Ahmed
Ahmed A. El-Mansi*
Affiliation:
Biology Department, Faculty of Science, King Khalid University, P.O. Box 641, Abha61421, Saudi Arabia Zoology Department, Faculty of Science, Mansoura University, Mansoura, Egypt
Mohamed A. Al-Kahtani
Affiliation:
Biology Department, Faculty of Science, King Khalid University, P.O. Box 641, Abha61421, Saudi Arabia
Mohamed M. A. Abumandour
Affiliation:
Anatomy and Embryology Department, Faculty of Veterinary Medicine, Alexandria University, Behera, Egypt
Ahmed E. Ahmed
Affiliation:
Biology Department, Faculty of Science, King Khalid University, P.O. Box 641, Abha61421, Saudi Arabia Department of Theriogenology, Faculty of Veterinary Medicine, South Valley University, Qena, Egypt
*
*Author for correspondence: Ahmed El-Mansi, E-mail: aelmansi@kku.edu.sa, elmansi@mans.edu.eg
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Abstract

We describe the morphological adaptations of the tongue and gastrointestinal tract of the striped sand snake Psammophis sibilans and discuss their functional importance. Using standard histological, histochemical, and scanning electron microscopy techniques, we analyzed 11 adult snakes of both sexes. Our findings showed that the bifurcated non-papillate tongue exhibited chemoreceptive adaptions to squamate foraging behavior. The lingual apex tapered terminally with sensory spines, and the body of the tongue possesses a characteristic central odor–receptor chamber that might serve to trap and retain scent molecules. Furthermore, the intrinsic musculature showed interwoven and well-developed transverse, vertical and longitudinal muscle fibers that control contraction and retraction during probing and flicking. The esophagus displayed highly folded mucosa lined with columnar epithelium with goblet cells. In contrast, the stomach mucosa formed finger-like gastric rugae, encompassing tubular glands with dorsal gastric pits. The intestine is distinct from other vertebrates in lacking the crypts of Lieberkühn in the tunica mucosa and submucosa. The intestine mucosa is mostly arranged in interdigitating villi oriented perpendicular to the luminal surface. We extrapolated subtle variations for both acid and neutral mucopolysaccharides and glycoproteins localization as well as collagen fibers using histochemical analyses. The elaborate histo-morphological and functional adaptation of the tongue and digestive tract plays a pivotal role in foraging and feeding behavior.

Keywords

digestive tracthistochemistryPsammophis sibilansscanning electron microscope (SEM)tongue
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 3 , June 2020 , pp. 524 - 541
Copyright
Copyright © Microscopy Society of America 2020

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References

Abbate, F, Guerrera, MC, Montalbano, G, Zichichi, R, Germanà, A & Ciriaco, E (2010). Morphology of the lingual dorsal surface and oral taste buds in Italian lizard (Podarcis sicula). Anat Histol Embryol 39, 167–171.CrossRefGoogle Scholar
Abo-Eleneen, RE, Bakry, AM & Abdeen, AM (2014). Ultrastructural study of the alimentary tract of two reptilian species the lizard Scincus scincus and the snake Natrix tessellata. J Cytol Histol. Doi:10.4172/2157-7099.S4-010.Google Scholar
Akani, GC, Eniang, EA, Ekpo, IJ, Angelici, FM & Luiselli, L (2003). Food habits of the snake psammophis phillipsi from the continuous rain-forest region of southern Nigeria (West Africa). J Herpetol 37, 208–211.CrossRefGoogle Scholar
Aylward, M, Beselaar, LC, Alagaili, AN, Amor, NMS, Mohammed, OB & Kotzé, SH (2019). A comparative morphological and histological study of the gastrointestinal tract of four insectivorous bat species: Asellia tridens, Chaerephon pumilus, Nycteris thebaica, Rhinopoma hardwickii. J Morphol 280, 1106–1117.Google ScholarPubMed
Baeckens, S, Herrel, A, Broeckhoven, C, Vasilopoulou-Kampitsi, M, Huyghe, K, Goyens, J & Van Damme, R (2017 a). Evolutionary morphology of the lizard chemosensory system. Sci Rep 7, 10141.CrossRefGoogle ScholarPubMed
Baeckens, S, Van Damme, R & Cooper, WE (2017 b). How phylogeny and foraging ecology drive the level of chemosensory exploration in lizards and snakes. J Evol Biol 30, 627–640.CrossRefGoogle ScholarPubMed
Bauer, AM & Branch, WR (1999). Field Guide to Snakes and Other Reptiles of Southern Africa. Copeia 1, 236–238.CrossRefGoogle Scholar
Bels, VL, Chardon, M & Kardong, KV (1994). Biomechanics of the Hyolingual System in Squamata. In: Bels, VL, Chardon, M & Vandewalle, P (eds) Biomechanics of Feeding in Vertebrates. Advances in Comparative and Environmental Physiology. Vol 18, pp. 147–240. Springer, Berlin, Heidelberg.CrossRefGoogle Scholar
Bels, VL & Kardong, KV (1995). Water drinking in snakes: Evidence for an esophageal sphincter. J Exp Zool 272, 235–239.CrossRefGoogle Scholar
Berkhoudt, H, Kardong, KV & Zweers, GA (1995). Mechanics of drinking in the brown tree snake, Boiga irregularis. Zoology 98, 92–103.Google Scholar
Bessler, SM & Secor, SM (2012). Effects of feeding on luminal pH and morphology of the gastroesophageal junction of snakes. Zoology (Jena) 115, 319–329.CrossRefGoogle ScholarPubMed
Boonyoung, P, Senarat, S, Kettratad, J, Jiraungkoorskul, W, Poolprasert, P, Wangkulangkul, S, Pengsakul, T, Yenchum, W & Sulieman, Y (2017). Esophagogastric region and liver tissue in dog-faced water snake Cerberus rynchops: Histology and histochemistry. Agric Nat Resour 51, 538–543.Google Scholar
Broadley, DG (2002). A review of the species of Psammophis Boie found south of latitude 12° S (Serpentes: Psammophiinae). J Herpetol Assoc Africa 51, 83–119.CrossRefGoogle Scholar
Clark, RW (2015). How snakes work: Structure, function, and behavior of the world's snakes. In The Quarterly Review of Biology, Lillywhite, Harvey B (Ed.), p. xiii+241. Oxford and New York: Oxford University Press. ISBN: 978-0-19-538037-8. 2014.Google Scholar
Cooper, WE (1994). Multiple functions of extraoral lingual behaviour in iguanian lizards: Prey capture, grooming and swallowing, but not prey detection. Anim Behav 47, 765–775.CrossRefGoogle Scholar
Cooper, WE (1996). Variation and evolution of forked tongues in squamate reptiles. Herpetol Nat Hist 4, 135–150.Google Scholar
Cooper, WE (1997). Independent evolution of squamate olfaction and vomerolfaction and correlated evolution of vomerolfaction and lingual structure. Amphib Reptilia 18, 85–115.CrossRefGoogle Scholar
Cooper, WE, Pérez-Mellado, V & Vitt, LJ (2002 a). Responses to major categories of food chemicals by the lizard Podarcis lilfordi. J Chem Ecol 28, 709–720.CrossRefGoogle ScholarPubMed
Cooper, WE, Pérez-Mellado, V, Vitt, LJ & Budzinsky, B (2002 b). Behavioral responses to plant toxins by two omnivorous lizard species. Physiol Behav 76, 297–303.CrossRefGoogle ScholarPubMed
Cox, CL & Secor, SM (2010). Integrated postprandial responses of the diamondback water snake, Nerodia rhombifer. Physiol Biochem Zool 83, 618–631.CrossRefGoogle ScholarPubMed
Cundall, D, Brainerd, EL, Constantino, J, Deufel, A, Grapski, D & Kley, NJ (2012). Drinking in snakes: Resolving a biomechanical puzzle. J Exp Zool A Ecol Genet Physiol 317, 152–172.CrossRefGoogle ScholarPubMed
Cundall, D, Tuttman, C & Close, M (2014). A model of the anterior esophagus in snakes, with functional and developmental implications. Anat Rec (Hoboken) 279, 586–598.CrossRefGoogle Scholar
De Groot, JH, Van Der Sluijs, I, Snelderwaard, PCh & Van Leeuwen, JL (2004). A three-dimensional kinematic analysis of tongue flicking in Python molurus. J Exp Biol 207, 827–839.CrossRefGoogle ScholarPubMed
de Haan, CC (2003). Extrabuccal infralabial secretion outlets in Dromophis, Mimophis and Psammophis species (Serpentes, Colubridae, Psammophiini). A propable substitute for ‘self-rubbing’ and cloacal scent gland functions, and a cue for a taxonomic account. C R Biol 326, 275–286.CrossRefGoogle Scholar
El-Taib, NT & Jarrar, B (1983). Morphology and histology of the alimentary canal of Mauremys caspica (Reptilia, Emydidae). Indian J Zool 1, 95–112.Google Scholar
Ferri, S, Junqueira, LC & Medeiros, LO (1976). Fine structure of the esophagus lining epithelials cells of the snake Xenodon merremii Wagler, 1824 (Ophidia). Anat Anz 139, 221–233.Google Scholar
Filoramo, NI & Schwenk, K (2009). The mechanism of chemical delivery to the vomeronasal organs in squamate reptiles: A comparative morphological approach. J Exp Zool A Ecol Genet Physiol 311, 20–34.CrossRefGoogle ScholarPubMed
Gabe, M & Saint Girons, H (1972). Rapport entre la position systematique des sauriens et les caracteristiques histochemiques de leurs cellules caliciformes duodenales. Bull Biol Fr Belg 106, 81–90.Google Scholar
Gadelha-Alves, R, Rozensztranch, AMDS & Rocha-Barbosa, O (2008). Comparative intestinal histomorphology of five species of phyllostomid bats (Phyllostomidae, Microchiroptera): Ecomorphological relations with alimentary habits. Int J Morphol 26, 591–602.CrossRefGoogle Scholar
Gillingham, JC & Clark, DL (1981). Snake tongue-flicking: transfer mechanics to Jacobson's organ. Can J Zool 59, 1651–1657.CrossRefGoogle Scholar
Gogone, ICVP, Carvalho, MPNd, Grego, KF, Sant'anna, SS, Hernandez-Blazquez, FJ & Catão-Dias, JL (2017). Histology of the gastrointestinal tract from Bothrops jararaca and Crotalus durissus. Braz J Vet Res Anim Sci 54, 253–263.CrossRefGoogle Scholar
Goosse, V & Bels, VL (1992). Kinematic analysis of tongue movements during chemosensory behaviour in the European green lizard, Lacerta viridis (Reptilia: Lacertidae). Can J Zool 70, 1886–1896.CrossRefGoogle Scholar
Gove, D (1979). A comparative study of snake and lizard tongue-flicking, with an evolutionary hypothesis. Z Tierpsychol 51, 58–76.CrossRefGoogle Scholar
Graves, BM (1993). Chemical delivery to the vomeronasal organs and functional domain of squamate chemoreception. Brain Behav Evol 41, 198–202.CrossRefGoogle ScholarPubMed
Halpern, M & Borghjid, S (1997). Sublingual plicae (anterior processes) are not necessary for garter snake vomeronasal function. J Comp Psychol 111, 302–306.CrossRefGoogle Scholar
Helmstetter, C, Pope, RK, T'Flachebba, M, Secor, SM & Lignot, JH (2009 a). The effects of feeding on cell morphology and proliferation of the gastrointestinal tract of juvenile Burmese pythons (Python molurus). Can J Zool 87, 1255–1267.CrossRefGoogle Scholar
Helmstetter, C, Reix, N, T'Flachebba, M, Pope, RK, Secor, SM, Le Maho, Y & Lignot, J-H (2009 b). Functional changes with feeding in the gastro-intestinal epithelia of the Burmese python (Python molurus). Zool Sci 26, 632–638.CrossRefGoogle Scholar
Herrel, A, Canbek, M, Özelmas, Ü, Uyanoǧlu, M & Karakaya, M (2005). Comparative functional analysis of the hyolingual anatomy in lacertid lizards. Anat Rec A Discov Mol Cell Evol Biol 284, 561–573.CrossRefGoogle ScholarPubMed
Iwasaki, SI (2002). Evolution of the structure and function of the vertebrate tongue. J Anat 201, 1–13.CrossRefGoogle ScholarPubMed
Iwasaki, SI & Kumakura, M (1994). An ultrastructural study of the dorsal lingual epithelium of the rat snake, Elaphe quadrivirgata. Ann Anat 176, 455–462.CrossRefGoogle ScholarPubMed
Iwasaki, SI & Yoshihara, M (2003). Histochemical and ultrastructural features of the lingual epithelium of the rat snake (Elaphe climacophora). Zoology (Jena) 106, 63–72.CrossRefGoogle Scholar
Iwasaki, SI, Yoshizawa, H & Kawahara, I (1996). Three-dimensional ultrastructure of the surface of the tongue of the rat snake, Elaphe climacophora. Anat Rec 245, 9–12.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Jacobson, ER (2007). Infectious Diseases and Pathology of Reptiles.1st edn, CRC Press.CrossRefGoogle Scholar
Jamniczky, HA, Russell, AP, Johnson, MK, Montuelle, SJ & Bels, VL (2009). Morphology and histology of the tongue and oral chamber of Eublepharis macularius (Squamata: Gekkonidae), with special reference to the foretongue and its role in fluid uptake and transport. Evol Biol 36, 397–406.CrossRefGoogle Scholar
Kaas, JH (2009). Evolutionary Neuroscience, 1st ed.Elsevier Science.Google Scholar
Keiser, ED (1975). Observations on tongue extension of vine snakes (genus Oxybelis) with suggested behavioral hypotheses. Herpetologica 1, 131–133.Google Scholar
Kelly, CMR, Barker, NP, Villet, MH, Broadley, DG & Branch, WR (2008). The snake family Psammophiidae (Reptilia: Serpentes): Phylogenetics and species delimitation in the African sand snakes (Psammophis Boie, 1825) and allied genera. Mol Phylogenet Evol 47, 1045–1060.CrossRefGoogle ScholarPubMed
Khamas, W & Reeves, R (2011). Morphological study of the oesophagus and stomach of the gopher snake Pituophis catenifer. Anat Histol Embryol 40, 307–313.CrossRefGoogle ScholarPubMed
Kier, WM & Smith, KK (1985). Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats. Zool J Linn Soc 83, 307–324.CrossRefGoogle Scholar
Mahler, DL & Kearney, M (2006). The palatal dentition in squamate reptiles: morphology, development, attachment, and replacement. Fieldiana Zool 108, 1–61.Google Scholar
Mao, S-H, Wang, J-J, Huang, S-C, Chao, C-F & Chen, C-C (1991). Ultrastructure of the tongue and anterior process of the sublingual plica in four species of venomous snakes. J Morphol 208, 279–292.CrossRefGoogle ScholarPubMed
Mcdowell, SB (1972). The Evolution of the Tongue of Snakes, and its Bearing on Snake Origins. In Dobzhansky, T., Hecht, M.K., Steere, W.C. (eds) Evolutionary Biology, PP. 191–273, Springer, New York, NY.CrossRefGoogle Scholar
Morgans, LF & Heidt, GA (1978). Comparative tongue histology and scanning electron microscopy of the diamondback water snake (Natrix rhombifera) and black rat snake (Elaphe obsoleta) (Reptilia, Serpentes, Colubridae). J Herpetol 12, 275–280.CrossRefGoogle Scholar
Nishida, Y, Yoshie, S & Fujita, T (2000). Oral sensory papillae, chemo- and mechano-receptors, in the snake, Elaphe quadrivirgata. A light and electron microscopic study. Arch Histol Cytol 63, 55–70.CrossRefGoogle ScholarPubMed
Parker, MR, Young, BA & Kardong, KV (2008). The forked tongue and edge detection in snakes (Crotalus oreganus): An experimental test. J Comp Psychol 122, 35–40.CrossRefGoogle Scholar
Rabinowitz, T & Tandler, B (1986). Papillary morphology of the tongue of the American chameleon: Anolis carolinensis. Anat Rec 216, 483–489.CrossRefGoogle ScholarPubMed
Roberton, AM & Wright, DP (1997). Bacterial glycosulphatases and sulphomucin degradation. Can J Gastroenterol 11, 361–366.CrossRefGoogle Scholar
Schumacher, U, Duku, M, Katoh, M, Jörns, J & Krause, WJ (2004). Histochemical similarities of mucins produced by Brunner's glands and pyloric glands: A comparative study. Anat Rec A Discov Mol Cell Evol Biol 278, 540–550.CrossRefGoogle ScholarPubMed
Schwenk, K (1985). Occurrence, Distribution and Functional Significance of Taste Buds in Lizards. Copeia 1985, 91–101.CrossRefGoogle Scholar
Schwenk, K (1993). The evolution of chemoreception in squamate reptiles: A phylogenetic approach. Brain Behav Evol 41, 124–137.CrossRefGoogle ScholarPubMed
Schwenk, K (1994 a). Why snakes have forked tongues. Science 263, 1573–1577.CrossRefGoogle ScholarPubMed
Schwenk, K (1994 b). Comparative biology and the importance of cladistic classification: a case study from the sensory biology of squamate reptiles. Biol J Linn Soc 52, 69–82.CrossRefGoogle Scholar
Schwenk, K (1995). Of tongues and noses: chemoreception in lizards and snakes. Trends Ecol Evol 10, 7–12.CrossRefGoogle ScholarPubMed
Schwenk, K (2000)). In Feeding in Lepidosaurs. In Form, Function and Evolution in Tetrapod Vertebrates.1st edn, Academic Press, Elsevier.Google Scholar
Scillitani, G, Mentino, D, Liquori, GE & Ferri, D (2012). Histochemical characterization of the mucins of the alimentary tract of the grass snake, Natrix natrix (Colubridae). Tissue Cell 44, 288–295.CrossRefGoogle Scholar
Secor, SM (2003). Gastric function and its contribution to the postprandial metabolic response of the Burmese python Python molurus. J. Exp Biol 206, 1621–1631.CrossRefGoogle ScholarPubMed
Sheehan, D & Hrapchak, B (1980). Theory and Practice Histotechnology, 2nd ed.St. Louis, MO: Mosby.Google Scholar
Sherbrooke, WC & Schwenk, K (2008). Horned lizards (Phrynosoma) incapacitate dangerous ant prey with mucus. J Exp Zool A Ecol Genet Physiol 309, 447–459.CrossRefGoogle ScholarPubMed
Shine, R, Branch, WR, Webb, JK, Harlow, PS & Shine, T (2006). Sexual dimorphism, reproductive biology, and dietary habits of psammophiine snakes (Colubridae) from southern Africa. Copeia 2006, 650–664.CrossRefGoogle Scholar
Smith, KK & Mackay, KA (1990). The morphology of the intrinsic tongue musculature in snakes (Reptilia, Ophidia): Functional and phylogenetic implications. J Morphol 205, 307–324.CrossRefGoogle ScholarPubMed
Starck, JM & Beese, K (2001). Structural flexibility of the intestine of Burmese python in response to feeding. J Exp Biol 204, 325–335.Google ScholarPubMed
Suvarna, K, Layton, C & Bancroft, J (2018)Bancroft's Theory and Practice of Histological Techniques, 8th edn. Elsevier Ltd.Google Scholar
Toubeau, G, Cotman, C & Bels, V (1994). Morphological and kinematic study of the tongue and buccal cavity in the lizard Anguis fragilis (Reptilia: Anguidae). Anat Rec 240, 423–433.CrossRefGoogle Scholar
Trape, J-F, Crochet, P-A, Broadley, D, Sourouille, P, Mané, Y, Burger, M, Böhme, W, Saleh, M, Karan, A, Lanza, B & Mediannikov, O (2019). On the Psammophis sibilans group (Serpentes, Lamprophiidae, Psammophiinae) north of 12 S, with the description of a new species from West Africa. Bonn Zool Bull 68, 61–91.Google Scholar
Valverde, BSL, Fanali, LZ, Franco-Belussi, L & de Oliveira, C (2019). Comparative morphology of the digestive tract of two Neotropical tree frogs (genus Boana). Zool Anz 281, 44–52.CrossRefGoogle Scholar
Vitt, LJ, Pianka, ER, Cooper, WE & Schwenk, K (2003). History and the global ecology of squamate reptiles. Am Nat 162, 44–60.CrossRefGoogle ScholarPubMed
Yang, C & Wang, L (2016). Histological and morphological observations on tongue of Scincella tsinlingensis (Reptilia, Squamata, Scincidae). Micron 80, 24–33.CrossRefGoogle Scholar
Young, BA (1990). Is there a direct link between the ophidian tongue and Jacobson's organ? Amphibia Reptilia 11, 263–276.CrossRefGoogle Scholar
Zahradnicek, O, Buchtova, M, Dosedelova, H & Tucker, AS (2014). The development of complex tooth shape in reptiles. Front Physiol 5, 74–81.CrossRefGoogle ScholarPubMed