Vol. 20 No. 1 (2025)
Short Note

On the maxillary dentition of the Western whip snake, Hierophis viridiflavus (Lacépède, 1789): heterodonty is not opisthoglyphy

PDF
  • Matteo R. Di Nicola,
  • Massimo Delfino
Matteo R. Di Nicola
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Turin, Italy
Massimo Delfino
Dipartimento di Scienze della Terra, Università degli Studi di Torino, via Valperga Caluso 35, 10125 Turin, Italy
DOI: https://doi.org/10.36253/a_h-16673

Published 2024-12-27

Keywords

  • Aglyphous,
  • Colubrid,
  • Non-front-fanged snakes,
  • Opisthoglyphous,
  • Proteroglyphous,
  • rear-fanged,
  • Solenoglyphous,
  • Tooth morphology
    • ...More
    Less

How to Cite

Di Nicola, M. R., & Delfino, M. (2024). On the maxillary dentition of the Western whip snake, Hierophis viridiflavus (Lacépède, 1789): heterodonty is not opisthoglyphy. Acta Herpetologica, 20(1), 75–81. https://doi.org/10.36253/a_h-16673

Copyright (c) 2025 Matteo Riccardo Di Nicola, Massimo Delfino

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

The Western whip snake (Hierophis viridiflavus) is a colubroid snake typically considered aglyphous and non-venomous, although this is currently a subject of debate. Indeed, the maxillary dentition of this species has recently been described as opisthoglyphous due to the presence of enlarged rear maxillary teeth, reportedly characterised by prominent grooves and ridges. Aiming to test the actual presence of these structures and provide a clearer characterisation of the maxillary dentition of the species, we analysed 17 dry-prepared and disarticulated H. viridiflavus specimens using both scanning electron and optical microscopy. The imaging confirmed the presence of posterior, enlarged maxillary teeth displaying a distal carina, highlighted by shallow longitudinal inflections on the disto-labial and disto-lingual tooth surfaces. Nonetheless, the analysis revealed the consistent absence of the meso-labially placed groove typical of opisthoglyphous taxa. Based on the results of our study, the maxillary dentition of the Western whip snake is heterodont, specifically opisthomegadont, and is confirmed to be aglyphous.

PDF

References

  1. Avella, I., Barajas-Ledesma, E., Casewell, N.R., Harrison, R.A., Rowley, P.D., Crittenden, E., Wüster, W., Castiglia, R., Holland, C., Van Der Meijden, A. (2021): Unexpected lack of specialisation in the flow properties of spitting cobra venom. J. Exp. Biol. 224: jeb229229.
  2. Avella, I., Castiglia, R., Senczuk, G. (2017): Who are you? The genetic identity of some insular populations of Hierophis viridiflavus s.l. from the Tyrrhenian Sea. Acta Herpetol. 12: 209-214.
  3. Avella, I., Savini, F., Di Nicola, M.R. (2024): A prolonged bite by a Western Whip Snake, Hierophis viridiflavus carbonarius (Bonaparte 1833) (Serpentes, Colubridae), resulting in pronounced local oedema. RandA 31: e21448.
  4. Bea, A. (1998): Coluber viridiflavus Lacépède, 1789. In: Reptiles, Fauna Ibérica, Vol. 10, pp. 358-363. Salvador, A., Ramos, M.A., Eds, Madrid, Museo Nacional de Ciencias Naturales.
  5. Bédry, R., Hilbert, G., Goyffon, M., Laffort, P., Parrens, E. (1998): Is the saliva of the European whip snake (Coluber viridiflavus) neurotoxic? Toxicon 12: 1729-1730.
  6. Berkovitz, B.K.B., Shellis, R.P. (2017): The teeth of non-mammalian vertebrates - 1st ed. London, Academic press.
  7. Berkovitz, B.K.B., Shellis, R.P. (2023): The teeth of non-mammalian vertebrates: form, function, development and growth. Amsterdam, Academic Press.
  8. Boie, H. (1826): Merkmale einiger japanischer Lurche. Isis von Oken 2: 203-216.
  9. Bonaparte, C.L.J.L. (1833): Iconographia della fauna Italica per le quattro classi degli animali vertebrati. Roma, Salviucci.
  10. Bonaparte, C.L.J.L. (1838): Amphibiorum tabula analytica. Nuovi Ann. Sci. Nat. 1: 391-393.
  11. Boulenger, G.A. (1893): Catalogue of the snakes in the British Museum (Natural History). Vol. I. London, British Museum (Natural History).
  12. Boulenger, G.A. (1894): Catalogue of the snakes in the British Museum (Natural History). Vol. II. London, British Museum (Natural History).
  13. Boulenger, G.A. (1896): Catalogue of the snakes in the British Museum (Natural History). Vol. III. London, British Museum (Natural History).
  14. Broeckhoven, C., Du Plessis, A. (2017): Has snake fang evolution lost its bite? New insights from a structural mechanics viewpoint. Biol. Lett. 13: 20170293.
  15. Cope, E.D. (1864): On the characters of the higher groups of Reptilia Squamata: And especially of the Diploglossa. Proc. Acad. Nat. Sci. Philadelphia 16: 224-231.
  16. Delfino M., Villa A. (2024). An overview of the skeleton of reptiles. In: Handbook of Zoology, Reptilia, Volume 1: General Biology, Archosauria, Chelonia, pp. 39-56. Joger, U., Ed., Berlin/Boston, Walter de Gruyter GmbH.
  17. Di Nicola, M.R., Cavigioli, L., Luiselli, L., Andreone, F. (2021a): Anfibi & Rettili d’Italia. Edizione aggiornata. Latina, Edizioni Belvedere.
  18. Di Nicola, M.R., Di Rosa, D., Mariacher, A., Zabbia, T. (2021b): Hierophis viridiflavus carbonarius (Western whip snake). Coloration. Herpetol. Rev. 52: 873-874.
  19. Dutto, M., Ineich, I., Serre-Collet, F., Goyffon, M., Bédry, R. (2015): Trois cas de morsures du Colubridé Hierophis viridiflavus (Lacépède, 1789). Bull. Soc. Herp. Fr. 156: 55-62.
  20. Duvernoy, D.M. (1832): Memoire sur le caracteres tires de l’anatomie pour distinquer les serpens venimeux des serpens non venimeux. Ann. Sci. Nat., 26: 113-160.
  21. Edmund, A.G. (1969): Dentition. In: Biology of the Reptilia, pp. 117-200. Vol. 1. Gans, C., Parsons, T.S., Bellairs, A.d’A., Eds, London, Academic Press.
  22. Fitzinger, L.J.F.J. (1826): Neue Classification der Reptilien nach ihren natürlichen Verwandtschaften: nebst einer Verwandtschafts-Tafel und einem Verzeichnisse der Reptilien-Sammlung des K. K. Zoologischen Museum zu Wien. Wien, J.G. Heubner.
  23. Fleischmann, F.L. (1831): Dalmatiae nova serpentum genera. Erlangae, C. Heyderi.
  24. Geoffroy Saint-Hilaire, I. (1827): Description des reptiles qui se trouvent en Égypte. In: Description de l’Egypte ou recueil des observations et des recherches qui ont été faites en Égypte pendant l’expedition de l’Armée française, publié par les ordres de sa Majesté-L’Empereur Napoléon le Grand. Histoire Naturelle. Tome premier. Première partie, pp. 121-160. Savigny, M.J.C.L., Ed., Paris, Imprimerie Impériale.
  25. Gmelin, J.F. (1789): Caroli a Linné, Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species; cum Characteribus, Differentiis, Synonymis, Locis. Editio Decima Tertia, Aucta, Reformata. Vol. I, part 3. Leipzig, G.E. Beer.
  26. Golay, P., Smith, H. M., Broadley, D. G., Dixon, J. R., McCarthy, C., Rage, J. C., Schätti B., Toriba, M. (1993). Endoglyphs and other major venomous snakes of the world. A checklist. Geneva, Azemiops herpetological data center.
  27. Gower, D.J., Zaher, H. (2022): The origin and early evolutionary history of snakes. Cambridge, Cambridge University Press.
  28. Herrera, Y., Fuentes-Retamal, S., Kemmerling, U., Peichoto, M.E., Ortiz, J.C., Urra, F.A. (2022): Shedding light on the dentition and venom delivery system of the rear-fanged snake, Galvarinus chilensis chilensis (Serpentes: Dipsadidae: Tachymenini) from Chile. Biology 11: 1788.
  29. Hoffstetter, R. (1939): Contribution a l’étude des Elapidae actuels et fossiles et de l’ostéologie des ophidians. Arch. Mus. Hist. Nat. Lyon 15: 1-78.
  30. Lacepède, B.G.É.d.L. (1789): Histoire naturelle des quadrupèdes ovipares et des serpens, vol. 2. Paris, Hôtel de Thou.
  31. LeBlanc, A.R.H., Palci, A., Anthwal, N., Tucker A.S., Araujo R., Pereira M.F.C., Caldwell M.W. (2023): A conserved tooth resorption mechanism in modern and fossil snakes. Nat. Commun. 14: 742
  32. Lee, M.S., Scanlon, J.D. (2002): Snake phylogeny based on osteology, soft anatomy and ecology. Biol. Rev. 77: 333-401.
  33. Lillywhite, H.B. (2014): How snakes work: structure, function and behavior of the world’s snakes. Oxford, Oxford University Press.
  34. Mahler, D.L., Kearney, M.R. (2006): The palatal dentition in squamate reptiles: Morphology, development, attachment, and replacement. Fieldiana Zool. 2006: 1-61.
  35. Merriam-Webster (2024): Merriam-Webster.com dictionary. Retrieved September 1, 2024, from https://www.merriam-webster.com/.
  36. Modahl, C.M., Mackessy, S.P. (2019): Venoms of rear-fanged snakes: New proteins and novel activities. Front. Ecol. Evol. 7: 279.
  37. Nopcsa, F. (1923): Die Familien der Reptilien. Fortschritte der Geologie und Paläontologie, vol. 2. Berlin, Verlag Gebrüder Borntraeger.
  38. Oppel, M. (1811): Die Ordnungen, Familien und Gattungen der Reptilien als Prodrom einer Naturgeschichte derselben. Munich, J. Lindauer.
  39. Paolino, G., Di Nicola, M. R., Ballouard, J. M., Bonnet, X., Damm, M., Le Roux, G., Lüddecke, T., Marini, D., Weinstein, S. A., Avella, I. (2024). A review of bites by non-front-fanged snakes (NFFS) of Europe. Toxicon 250: 108116.
  40. Paterna, A. (2023): The role of modified teeth in the function of prolonged bites in Hierophis viridiflavus (Serpentes: Colubridae). Phyllomedusa 22: 121-130.
  41. Paterna, A., Grano, M. (2024). Morphology of the maxillary bones in the Caspian whip-snake Dolichophis caspius (Serpentes Colubridae) supports the opisthoglyphous model within western palearctic whipsnakes. Biodivers. J. 15: 693-700.
  42. Phisalix, M. (1922): Animaux venimeux et venins: la fonction venimeuse chez tous les animaux; les appareils venimeux; les venins et leurs propriétés; les fonctions et usages des venins; l’envenimation et son traitement. Paris, Masson & cie.
  43. Pin, T.C. (2009): The study of the mediation of Ohanin, a king cobra (Ophiophagus hannah) toxin through the central nervous system. Unpublished MSc thesis. National University of Singapore.
  44. Pough, F.H., Andrews, R.M., Crump, L.C., Savitzky, A.H., Wells, K.D., Brandley, M.C. (2016): Herpetology. Sunderland, Sinauer associates Inc.
  45. Racca, L., Villa, A., Wencker, L.C.M., Camaiti, M., Blain, H., Delfino, M. (2020): Skull osteology and osteological phylogeny of the Western whip snake Hierophis viridiflavus (Squamata, Colubridae). J. Morphol. 281: 808-833.
  46. Ryerson, W.G., Van Valkenburg, T. (2021): Linking tooth shape to strike mechanics in the Boa constrictor. Integr. Comp. Biol. 61: 759-771.
  47. Sánchez, M.N., Teibler, G.P., Sciani, J.M., Casafús, M.G., Maruñak, S.L., Mackessy, S.P., Peichoto, M.E. (2019): Unveiling toxicological aspects of venom from the Aesculapian false coral snake Erythrolamprus aesculapii. Toxicon 164: 71-81.
  48. Segall, M., Houssin, C., Delapré, A., Cornette, R., Herrel, A., Milgram, J., Shahar, R., Dumont, M. (2023): Armed to the teeth: The underestimated diversity in tooth shape in snakes and its relation to feeding behavior and diet. Ecol. Evol. 13: e10011.
  49. Senczuk, G., Gramolini, L., Avella, I., Mori, E., Menchetti, M., Aloise, G., Castiglia, R. (2021): No association between candidate genes for color determination and color phenotype in Hierophis viridiflavus, and characterization of a contact zone. J. Zool. Syst. Evol. Res. 59: 748-759.
  50. Sindaco, R., Razzetti, E. (2021): An updated check-list of Italian amphibians and reptiles. Nat. Hist. Sci. 8: 35-46.
  51. Storniolo, F., Mangiacotti, M., Zuffi, M.A.L., Scali, S., Sacchi, R. (2023): Large scale phenotypic characterisation of Hierophis viridiflavus (Squamata: Serpentes): climatic and environmental drivers suggest the role of evolutionary processes in a polymorphic species. Evol. Ecol. 37: 419-434.
  52. Taub, A.M. (1967): Comparative histological studies on Duvernoy’s gland of colubrid snakes. Bull. Am. Mus. Nat. Hist. 138: 1-50.
  53. Treccani (2024): Enciclopedia Italiana. Accessed August 28, 2024. https://www.treccani.it/.
  54. Trevine, V.C., Grazziotin, F.G., Giraudo, A., Sallaberry‐Pincheira, N., Vianna, J.A., Zaher, H. (2022): The systematics of Tachymenini (Serpentes, Dipsadidae): An updated classification based on molecular and morphological evidence. Zool. Scr. 51: 643-663.
  55. Triep, M., Hess, D., Chaves, H., Brücker, C., Balmert, A., Westhoff, G., Bleckmann, H. (2013): 3D flow in the venom channel of a spitting cobra: Do the ridges in the fangs act as fluid guide vanes? PLOS One 8: e61548.
  56. Vanni, S., Zuffi, M.A.L. (2011): Hierophis viridiflavus (Lacépède, 1789). In: Fauna d’Italia, vol. 45, Reptilia, pp. 509-516. Corti, C., Capula, M., Luiselli, L., Razzetti, E., Sindaco, R., Eds, Bologna, Calderini.
  57. Wagler, J.G. (1830): Natürliches System der Amphibien: mit vorangehender Classification der Säugethiere und Vögel: ein Beitrag zur vergleichenden Zoologie. Munich, J.G. Cotta.
  58. Weinstein, S.A., Warrell, D.A., Keyler, D. (2022): ‘Venomous’ bites from non-venomous snakes. Second edition. Amsterdam, Elsevier.
  59. Westeen, E.P., Durso, A.M., Grundler, M.C., Rabosky, D.L., Davis Rabosky, A.R. (2020): What makes a fang? Phylogenetic and ecological controls on tooth evolution in rear-fanged snakes. BMC Evol. Biol. 20: 80.
  60. Young, B.A., Kardong, K.V. (1996): Dentitional surface features in snakes (Reptilia: Serpentes). Amphib.-Reptil. 17: 261-276.

Most read articles by the same author(s)