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18 - An Overview of the Morphology of Oral Glands in Snakes

from Part V - Anatomical and Functional Morphological Perspectives

Published online by Cambridge University Press:  30 July 2022

By
Leonardo de Oliveira  and
Hussam Zaher
Edited by
David J. Gower  and
Hussam Zaher
David J. Gower
Affiliation:
Natural History Museum, London
Hussam Zaher
Affiliation:
Universidade de São Paulo
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Summary

Oral glands underwent substantial modification during the origin and diversification of snakes. Oral glands have provided rich data for snake systematics, and for informing evolutionary scenarios about the adaptive radiation of snake feeding. However, sampling has been patchy, and many questions remain about gland homology, function and evolution. This chapter addresses labial (supra- and infralabial), temporomandibular, rictal, sublingual, premaxillary, accessory and dental (= venom and Duvernoy’s) glands. We review and synthesize developments and data and present new histological sections and high-resolution tomography of some snakes and lizards, providing descriptions and illustrations of oral glands and associated structures. We comment on labial and dental glands of some toxicoferan and non-toxicoferan lizards, and report the first observation of a possible infralabial gland in a dibamian lizard. There are insufficient data to resolve all outstanding questions about gland homology across lizards and snakes, but the ancestral snake possibly had rictal and lacked dental (venom) glands, the latter perhaps evolving only within colubroidean caenophidians.

Keywords

anatomyfunctionhistologyToxicoferavenomrictal glandlizardsSquamatatomographyancestral state
Type
Chapter
Information
The Origin and Early Evolutionary History of Snakes , pp. 410 - 436
Publisher: Cambridge University Press
Print publication year: 2022

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References

Kochva, E., The origin of snakes and evolution of the venom apparatus. Toxicon, 25 (1987), 65–106.Google Scholar
Deufel, A. and Cundall, D., Functional plasticity of the venom delivery system in snakes with focus on the poststrike prey release behavior. Zoologischer Anzeiger, 245 (2006), 249–267.CrossRefGoogle Scholar
Kochva, E., Oral glands of the reptilia. In Gans, C. K. and Gans, A., eds., Biology of the Reptilia, Vol. 8 (London and New York: Academic Press, 1978), pp. 43–162.Google Scholar
Cundall, D., Functional morphology. In Siegel, R. A., Collins, J. T., and Novak, S. S., eds., Snakes, Ecology and Evolutionary Biology (New York: MacMillan, 1987), pp. 106–140.Google Scholar
Underwood, G., An overview of venomous snake evolution. In Thorpe, R. S., Wüster, W., and Malhotra, A., eds., Venomous Snakes. Ecology, Evolution and Snakebite, n. 70 (Oxford: Clarendon Press, 1997), pp. 1–13.Google Scholar
Jackson, K., The evolution of venom-delivery systems in snakes. Zoological Journal of the Linnean Society, 137 (2003), 227–354.Google Scholar
Fry, B. G., Vidal, N., Norman, J. A., et al., Early evolution of the venom system in lizards and snakes. Nature, 439 (2006), 584–588.Google Scholar
Taub, A. M., Ophidian cephalic glands. Journal of Morphology, 118 (1966), 529–542.Google Scholar
Pearse, A. G., Histochemistry: Theoretical and Applied. Volume 2. 4th ed. (Edinburgh: Churchill Livingstone, 1985).Google Scholar
Kiernan, J. A., Histological and Histochemical Methods: Theory and Practice. 3rd ed. (London: Oxford University Press, 2001).Google Scholar
Metscher, B. D., MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiology, 9 (2009), 1–14.Google Scholar
Underwood, G., On the rictal structures of some snakes. Herpetologica, 58 (2002), 1–17.Google Scholar
Zaher, H., Comments on the evolution of the jaw adductor musculature of snakes. Zoological Journal of the Linnean Society, 111 (1994), 339–384.Google Scholar
Weinstein, S. A., ‘Venomous’ bites from non-venomous snakes: a critical analysis of risk and management of ‘colubrid’ snake bites. (Waltham, MA: Elsevier, 2011).Google Scholar
Jackson, T. N. W., Young, B., Underwood, G., et al., Endless form most beautiful: the evolution of ophidian oral glands, including the venom system, and the use of appropriate terminology for homologous structures. Zoomorphology, 136 (2017), 107–130.Google Scholar
Zaher, H., Grazziotin, F. G., Cadle, J. E., et al., Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis South American Xenodontines: a revised classification and description of new taxa. Papéis Avulso de Zoologia, 49 (2009), 115–153.Google Scholar
Zaher, H., Murphy, R. W., Arredondo, J. C., et al., Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS ONE, 14 (2019), e0216148.Google Scholar
Taub, A. M., Comparative studies on Duvernoy’s gland of colubrid snakes. Bulletin of the American Museum of Natural History, 138 (1967), 1–50.Google Scholar
Vidal, N., Colubroid systematics: evidence for an early appearance of the venom apparatus followed by extensive evolutionary tinkering. Journal of Toxinology: Toxin Review, 21 (2002), 21–41.Google Scholar
Kardong, K. V., Colubrid snakes and Duvernoy’s ‘venom’ glands. Journal of Toxicology: Toxin Reviews, 21 (2002), 1–19.Google Scholar
Weinstein, S. A., Smith, T. L., and Kardong, K., Reptile venom glands form, function, and future. In Mackessy, S. P., ed., Handbook of Venoms and Toxin of Reptiles (Boca Raton, NY: CRC Taylor & Francis, 2010), pp. 65–91.Google Scholar
Fry, B. G., Casewell, N. R., Wüster, W., et al., The structural and functional diversification of the Toxicofera reptile venom system. Toxicon, 60 (2012), 434–448.Google Scholar
Burbrink, F. T., Grazziotin, F. G., Pyron, R. A., et al., Interrogating genomic-scale data for Squamata (lizards, snakes, and amphisbaenians) shows no support for key traditional morphological relationships. Systematic Biology, 69 (2020), 502–520.Google Scholar
Smith, M. and Bellairs, A. A., The head glands of snakes, with remarks on the evolution of the parotid gland and teeth of the Opisthoglypha. Zoological Journal of the Linnean Society, 41 (1947), 353–368.Google Scholar
Gygax, P., Entwicklung, Bau und Funktion der Giftdrüse (Duvernoy’s gland) von Natrix tessellata . Acta Tropica, Zoology, 28 (1971), 225–274.Google Scholar
Oliveira, L., Guerra-Fuentes, R. A., and Zaher, H., Embryological evidence of a new type of seromucous labial gland in neotropical snail-eating snakes of the genus Sibynomorphus . Zoologischer Anzeiger, 266 (2017), 89–94.Google Scholar
Saint-Girons, H., Évolution de la function venimeuse chez les reptiles. In Compte-rendu du colloque organisé à la Faculté Catholique des Sciences (Lyon: Societé Herpétologique de France & Fondation Marcel Merieuse, 1987), pp. 9–22.Google Scholar
Gabe, M. and Saint-Girons, H., Données histologiques sur les glandes salivaires des lépidosauriens. Memoires du Museum National d’Histoire Naturelle, 58 (1969), 3–116.Google Scholar
Haas, G., Anatomical observations on the head of Liotyphlops albirostris (Typhlopidae, Ophdia). Acta Zoologica, 1964 (1964), 1–62.Google Scholar
Saint-Girons, H., Les glandes céphaliques exocrines des Reptiles. II. – Considérations fonctionnelles et évolutives. Annales des Sciences Naturelles, Zoologie, 10 (1989), 1–17.Google Scholar
Penteado, D. C., Estudos histológicos das glândulas da cabeça dos ofídeos brasileiros. Memórias do Instituto Butantan, 1 (1918), 27–57.Google Scholar
Taub, A. M., Systematic implications from the labial glands of the Colubridae. Herpetologica, 23 (1967), 145–148.Google Scholar
Fry, B. G., Scheib, H., van der Weerd, L., et al., Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Molecular and Cellular Proteomics, 7 (2008), 215–46.Google Scholar
Underwood, G. and Kochva, E., On the affinities of the burrowing asps Atractaspis (Serpentes: Atractaspididae). Zoological Journal of the Linnean Society, 107 (1993), 3–64.Google Scholar
Lopes, R. A., de Oliveira, C., Campos, M. N. M., Campos, S. M., and Birman, E. G., Morphological and histochemical study of cephalic glands of Bothrops jararaca (Ophidia, Viperidae). Acta Zoologica, 55 (1974), 17–24.CrossRefGoogle Scholar
Ineich, I. and Tellier, J. M., Une glande supralabiale à débouché externe chez le genre Echis (Reptilia, Viperidae), cas unique chez les serpents. Comptes Rendus de l’Académie des Sciences Paris, 315 (1992), 49–53.Google Scholar
Saint-Girons, H. and Ineich, I.. Donnés histologiques sur la glande labiale supérieure externe des Viperidae du genre Echis . Amphibia-Reptilia, 14 (1993), 315–319.Google Scholar
Savitzky, A. H., The origin of the New World proteroglyphous snakes and its bearing on the study of venom delivery systems in snakes . Unpublished PhD dissertation, University of Kansas, Lawrence, United States, 1979.Google Scholar
Oliveira, L., Buononato, M. A., and Zaher, H., Chapter 12 - The cephalic glands and venom apparatus of coralsnakes. In N. J. Silva Jr., L. W. Porras, S. T. Aird, and A. L. C. Prudente, eds., Advances in coralsnake biology: with an emphasis on South America. (Eagle Mountain, Utah: Eagle Mountain Publishing, LC, Utah, USA, 2021), pp. 371–390.Google Scholar
Burns, B. and Pickwell, G. V., Cephalic glands in sea snakes (Pelamis, Hydrophis and Laticauda). Copeia, 1972 (1972), 547–559.Google Scholar
Oliveira, L., Prudente, A. L. C., and Zaher, H., H. Unusual labial glands in snakes of the genus Geophis Wagler, 1830 (Serpentes: Dipsadinae). Journal of Morphology, 275 (2014), 87–99.Google Scholar
Zaher, H., Oliveira, L., Grazziotin, F. G., et al., Consuming viscous prey: a novel protein-secreting delivery system in Neotropical snail-eating snakes. BMC Evolutionary Biology, 14 (2014), 58.Google Scholar
Savitzky, A. H., The relationship of the xenodontine colubrid snakes related to Ninia . Unpublished Masters dissertation, University of Kansas, United States, 1972.Google Scholar
Harvey, M. B., Fuenmayor, G. R., Portilla, J. C. R., and Rueda-Almonacid, J. V., Systematics of the enigmatic dipsadinae snake Tropidophis perijanensis Alemán (Serpentes: Colubridae) and review of morphological characters of Dipsadini. Herpetological Monographs, 22 (2008), 106–132.Google Scholar
Underwood, G., A Contribution to the Classification of Snakes. (London: British Museum (Natural History), 1967).Google Scholar
Haas, G., Anatomical observations on the head of Anomalepis aspinosus (Typhlopidae, Ophidia). Acta Zoologica, 49 (1967), 63–139.Google Scholar
Martins, A., Passos, P., and Pinto, R., Unveiling diversity under the skin: comparative morphology study of the cephalic glands in threadsnakes (Serpentes: Leptotyphlopidae: Epictinae). Zoomorphology, 137 (2018), 433–443.Google Scholar
Haas, G., Über die Kaumuskulatur und die Schädelmechanik einiger Wühlschlangen. Zoologische Jahrbücher (Anatomie), 52 (1930), 95–218.Google Scholar
Brongersma, L. D., Some features of the Dipsadinae and Pareinae (Serpentes, Colubridae). Proceedings van de Koninklijke Nederlandse Akademie van Wetenschappen Section C, 61, (1958), 7–12.Google Scholar
Haas, G., A note on the origin of solenoglyph snakes. Copeia, 1938 (1938), 73–78.Google Scholar
Zaher, H., Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bulletin of the American Museum of Natural History, 240 (1999), 1–168.Google Scholar
Cadle, J. E. and Greene, H. W., Phylogenetic patterns, biogeography, and the ecological structure of Neotropical snake assemblages. In Ricklefs, R. E and Schluter, D., eds., Species Diversity in Ecological Communities: Historical and Geographical Perspective (Chicago: University of Chicago Press, 1993), pp. 281–293.Google Scholar
Laporta-Ferreira, I. L. and Salomão, M. G., Morphology, physiology and toxicology of the oral glands of a tropical cochleophagous snake, Sibynomorphus neuwiedi (Colubridae – Dipsadinae). Zoologischer Anzeiger, 27 (1991), 198–208.Google Scholar
Salomão, M. G. and Laporta-Ferreira, I. L., The role of secretions from the supralabial, infralabial, and Duvernoy’s glands of the slug-eating snake Sibynomorphus mikanii (Colubridae: Dipsadinae) in the immobilization of molluscan prey. Journal of Herpetology, 28 (1994), 369–371.Google Scholar
Oliveira, L., Jared, C., and Prudente, A. L. C., Oral glands in dipsadinae ‘goo-eater’ snakes: Morphology and histochemistry of the infralabial glands in Atractus reticulatus, Dipsas indica, and Sibynomorphus mikanii . Toxicon, 51 (2008), 898–913.Google Scholar
Campos, P. F., Oliveira, L., Grazziotin, F. G., et al., Transcriptomic analysis of snake infralabial glands highlights a plasticity in the site of expression of venom genes. Toxicon, 158 (2019), pp. S48.Google Scholar
Phisalix, M., Animaux venimeux et venins, Vol. 2 (Paris: Masson & Cie, 1922).Google Scholar
Phisalix, M. and Caius, R.. L’extension de la fonction venimeuse dans l’ordre entière des ophidiens et son existence chez des familles ou elle n’avait pas été soupçonnée jusqu’içi. Journal de Physiologie et de Pathologie Générale, 17 (1918), 923–964.Google Scholar
Kochva, E., The development of the venom gland in the opisthoglyph snake Telescopus fallax with remarks on Thamnophis sirtalis (Colubridae, Reptilia). Copeia, 1965 (1965), 147–154.Google Scholar
McDowell, S. B., The architecture of the corner of the mouth of colubroid snakes. Journal of Herpetology, 20 (1986), 353–407.Google Scholar
Wollberg, M., Kochva, E., and Underwood, G., On the rictal glands of some atractaspid snakes. Herpetological Journal, 8 (1998), 137–143.Google Scholar
Cundall, D. and Rossman, D. A., Cephalic anatomy of the rare Indonesian snake Anomochilus weberi . Zoological Journal of the Linnean Society, 109 (1993), 235–273.Google Scholar
Oliveira, L., Buononato, M. A., and Zaher, H., Glândulas cefálicas e aparato de veneno das cobras-corais. In Silva, N. J. Jr., ed., As cobras-corais do Brasil: Biologia, taxonômica, venenos e envenamentos (Goiânia: Editoria de Pontifica Universidade Católica de Goiás, Brasil, 2016), pp. 217–241.Google Scholar
Dix, M. W., A venom gland in the lower jaw of the coral snake (Micrurus nigrocinctus mosquitensis Schmidt). In Rosenberg, P., ed., Toxins. Animal, Plant and Microbial (Oxford: Pergamon Press, 1978), pp. 16–28.Google Scholar
Fry, B. G., Undheim, E. A. B., Ali, S. A, et al., Squeezers and leaf-cutters: differential diversification and degeneration of the venom system in toxicoferan reptiles. Molecular and Cellular Proteomics 12 (2013), 1881–1899.Google Scholar
Babonis, L. S. and Brischoux, F., Perspectives on the convergent evolution of tetrapod salt glands. Integrative and Comparative Biology, 52 (2012), 245–56.Google Scholar
Dunson, W. A., Packer, R. K., and Dunson, M. K., Sea snakes: an unusual salt gland under the tongue. Science, 173 (1971), 437–441.Google Scholar
Dunson, W. A. and Dunson, M. K., Convergent evolution of sublingual salt glands in the marine file snake and true sea snakes. Journal of Comparative Physiology, 86 (1973), 193–208.Google Scholar
Dunson, W. A. and Dunson, M. K., Possible new salt gland in a marine homalopsid snake (Cerberus rhynchops). Copeia, (1979), 661–673.Google Scholar
Fry, B. G., Venomous Reptiles and Their Toxins: Evolution, Pathophysiology and Biodiscovery (New York: Oxford University Press, 2015).Google Scholar
Fry, B. G., Winter, K., Norman, J. A., et al., Functional and structural diversification of the Anguimorpha lizard venom system. Molecular and Cellular Proteomics, 9 (2010), 2369–2390.Google Scholar
Tucker, A. S., Salivary gland adaptations: modification of the glands for novel uses. In Tucker, A. S. and Miletich, I., eds., Salivary Glands. Development, Adaptations and Disease. Frontiers of Oral Biology, Vol. 14 (Basel: Karger, 2010), pp. 21–31.Google Scholar
Kerkkamp, H. M. I., Casewell, N. R., and Vonk, F. J., Evolution of the snake venom delivery system. In. Gopalakrishnakone, P. and Malhotra, A., eds., Evolution of Venomous Animals and Their Toxins, Toxinology (Berlin: Springer, 2017), pp. 303–315.Google Scholar
Kochva, E., Development of the venom gland and trigeminal muscles in Vipera palaestinae , Acta Anatomica, 52 (1963), 49–89.Google Scholar
Shayer-Wollberg, M. and Kochva, E., Embryonic development of the venom apparatus in Causus rhombeatus (Viperidae, Ophidia). Herpetologica, 23 (1967), 249–259.Google Scholar
Vonk, F. J., Admiraal, J. R., Jackson, K., et al., Evolutionary origin and development of snakes fangs. Nature, 454 (2008), 630–633.Google Scholar
Boulenger, G. A., Remarks on the dentition of snakes and on the evolution of the poison-fangs. Proceedings of the Zoological Society of London, 64 (1896), 614–618.Google Scholar
Mackessy, S. P., Morphology and ultrastructure of the venom gland of the Northern Pacific Rattlesnake Crotalus viridis oreganus . Journal of Morphology, 208 (1991), 109–128.Google Scholar
Sakai, F., Carneiro, S. M., and Yamanouye, N., Morphological study of accessory gland of Bothrops jararaca and its secretory cycle. Toxicon, 59 (2012), 393–401.Google Scholar
Kochva, E. and Gans, C., Salivary glands of snakes. Clinical Toxicology, 3 (1970), 363–387.Google Scholar
Rosenberg, H. I., Histology, histochemistry, and emptying mechanism of the venom glands of some elapid snakes. Journal of Morphology, 123 (1967), 133–156.Google Scholar
Kochva, E. and Wollberg, M., The salivary glands of Aparallactinae (Colubridae) and the venom glands of Elaps (Elapidae) in relation to the taxonomic status of this genus. Zoological Journal of the Linnean Society, 49 (1970), 217–224.Google Scholar
McCarthy, C. J., Morphology of elapid snakes (Serpentes: Elapidae). An assessment of the evidence. Zoological Journal of the Linnean Society, 83 (1985), 79–93.Google Scholar
Gopalakrishnakone, P. and Kochva, E., Venom glands and some associated muscles in sea snakes. Journal of Morphology, 205 (1990), 85–96.CrossRefGoogle ScholarPubMed
Gopalakrishnakone, P., Structure of the venom gland of the Malayan Banded Snake Maticora intestinalis . Snake, 18 (1986), 19–26.Google Scholar
Kochva, E., Atractaspis (Serpentes, Atractaspididae) the burrowing asp; a multidisciplinary minireview. Bulletin of the Natural History Museum of London (Zoology), 68 (2002), 91–99.Google Scholar
Young, B. A. and Kardong, K. V., Dentitional surface features in snakes (Reptilia: Serpentes). Amphibia–Reptilia, 17 (1996), 261–276.Google Scholar
Salomão, M. G. and Ferrarezzi, H., A morphological, histochemical and ultrastructural analysis of the Duvernoy’s glands of elapomorphine snakes: the evolution of their venom apparatus and phylogenetic implications . Abstract (Campinas: III Congresso Latino Americano de Herpetologia, 43, Instituto de Biociências da Universidade Estadual de Campinas, 1993).Google Scholar

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