Abstract
The monotypic Mimophis mahfalensis is an opisthoglyphous snake endemic of Madagascar. The goal of this study is to clarify the presence of toxin-secreting oral glands through a multidisciplinary approach. We thus provide data on the internal anatomy of the head of M. mahfalensis’ and demonstrate the presence of Duvernoy’s glands. Furthermore, we refer to two cases of human bitten by this species and compared this with the reported case of mild envenomation mentioned by Domergue (Arch Inst Pasteur Madagascar 56(1):299–311, 1989). Symptoms included brief slight local pain and minor bleeding.
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References
Akat E, Cakici Ö, Dinçasland YE, Arikan H (2011) Histochemical and histological investigations on Duvernoy’s gland in Natrix tessellata (Squamata: Colubridae). Kafkas Univ Vet Fak Derg 17(2):285–289
Aprea G, Odierna G, Andreone F, Glaw F, Vences M (2003) Unusual karyotype in the Malagasy colubrid snake Mimophis mahfalensis. Amphib-Reptil 24(2):215–219
Boistel R, Aubin T, Cloetens P, Langer M, Gillet B, Josset P, Pollet N, Herrel A (2011a) Whispering to the deaf: communication by a frog without external vocal sac or tympanum in noisy environments. PLoS ONE 6(7):e22080
Boistel R, Swoger J, Kržič U, Fernandez V, Gillet B, Reynaud EG (2011b) The future of three dimensional microscopic imaging in marine biology. Mar Ecol 32(4):438–452
Branch B (2005) Photographic guide to snakes, other reptiles and amphibians of East Africa. Struik, Cape Town
Broadley DG, Cock EV (1975) Snakes of Rhodesia. Longman, Salisbury
Broadley DG, Doria CT, Wigge J (2003) Snakes of Zambia. Chimaira, Frankfurt
Brygoo ER (1982) Les ophidiens de Madagascar. Mem Inst Butantan 46:19–58
Chippaux JP (2002) Venins de serpent et envenimations. IRD Éditions, Paris
Crottini A, Madsen O, Poux C, Strauß A, Vieites DR, Vences M (2012) Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K-T boundary in Madagascar. Proc Natl Acad Sci USA 109(14):5358–5363
D’Cruze N (2008) Envenomation by the Malagasy colubrid snake Langaha madagascariensis. J Venom Anim Toxins Incl Trop Dis 14(3):546–551
de Haan CC (2003) Extrabuccal infralabial secretion outlets in Dromophis, Mimophis and Psammophis species (Serpentes, Colubridae, Psammophiini). A probable substitute for “self-rubbing” and cloacal scent gland functions, and a cue for a taxonomic account. C R Biol 326(3):275–286
Domergue CA (1962) Un serpent venimeux de Madagascar: Madagascarophis colubrina. Bull Acad Malgache 40:97–98
Domergue CA (1989) Un serpent venimeux de Madagascar: observation de deux cas de morsure par Madagascarophis (Colubrida opisthoglyphe). Arch Inst Pasteur Madagascar 56(1):299–311
Fry BG, Wuster W, Ramjan SFR, Jackson T, Martelli P, Kini RM (2003) Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionary and toxinological implications. Rapid Commun Mass Spectrom 17(18):2047–2062
Fry BG, Scheib H, van der Weerd L, Young B, McNaughtan J, Ramjan SF, Vidal N, Poelmann RE, Norman JA (2008) Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics 7(2):215–246
Fry BG, Vidal N, van der Weerd L, Kochva E, Renjifo C (2009) Evolution and diversification of the Toxicofera reptile venom system. J Proteomics 72:127–136
Glaw F, Vences M (2007) A field guide to the amphibians and reptiles of Madagascar, 3rd edn. Vences and Glaw Verlag, Cologne
Glover P, Mansfield P (2002) Limits to magnetic resonance microscopy. Rep Prog Phys 65(10):1489–1511
Greene HW (1997) Snakes: the evolution of mystery in nature. University of California Press, Berkeley
Haas G (1931) Über die morphologie der kiefermuskulatur und die Schädelmechanik einiger Schlangen. Zool Jahrb 54:332–416
Herrel A, Tolley KA, Measey GJ, da Silva JM, Potgieter DF, Boller E, Boistel R, Vanhooydonck B (2013) Slow but tenacious: an analysis of running and gripping performance in chameleons. J Exp Biol 216(6):1025–1030
Kardong KV (2002) Colubrid snakes and Duvernoy’s “venom” glands. Toxin Rev 21(1–2):1–19
Kochva E (1978) Oral glands of the reptilia. In: Gans C (ed) Biology of the reptilia. Academic Press, New York, pp 43–160
Kochva E, Shayer-Wollberg M, Sobol R (1967) The special pattern of the venom gland in Atractaspis and its bearing on the taxonomic status of the genus. Copeia 1967:763–772
Kochva E, Bdolah A, Wollberg Z (1993) Sarafotoxins and endothelins: evolution, structure and function. Toxicon 31:541–568
Lauridsen H, Hansen K, Wang T, Agger P, Andersen JL, Knudsen PS, Rasmussen AS, Pedersen M (2011) Inside out: modern imaging techniques to reveal animal anatomy. PLoS ONE 6(3):e17879
McDowell SB (1986) The architecture of the corner of the mouth of colubroid snakes. J Herpetol 20:353–407
McKinstry DM (1983) Morphologic evidence of toxic saliva in colubrid snakes: a checklist of world genera. Herp Rev 14:12–15
Mori A (2002) A case of envenomation by the Madagascan colubrid snake, Leioheterodon modestus. Snake 29:7–8
Mori A, Mizuta T (2006) Envenomation by the madagascan colubrid snake, Ithycyphus miniatus. J Venom Anim Toxins Incl Trop Dis 12(3):512–520
Nagy ZT, Joger U, Wink M, Glaw F, Vences M (2003) Multiple colonization of Madagascar and Socotra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proc R Soc Lond B Biol Sci 270(1533):2613–2621
Noonan BP, Chippindale PT (2006) Dispersal and vicariance: the complex evolutionary history of boid snakes. Mol Phylogenet Evol 40:347–358
Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93
Taub AM (1967) Comparative histological studies on Duvernoy’s gland of colubrid snakes. Bull Am Mus Nat Hist 138(article 1):1–50
Underwood G (2002) On the rictal structures of some snakes. Herpetologica 58:1–17
Vidal N, Delmas A, David P, Cruaud C, Couloux A, Hedges S (2007) The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. C R Biol 330(2):182–187
Vidal N, Marin J, Morini M, Donnellan S, Branch WR, Thomas R, Vences M, Wynn A, Cruaud C, Hedges SB (2010) Blindsnake evolutionary tree reveals long history on Gondwana. Biol Lett 6:558–561
Warrell DA (1995) Clinical toxicology of snakebite in Africa and the Middle East/Arabian Peninsula. In: Meier J, White J (eds) Handbook of clinical toxicology of animal venoms and poisons. CRC Press, Boca Raton, pp 433–492
Wollberg M, Kochva E, Underwood G (1998) On the rictal glands of some atractaspid snakes. Herpetol J 8:137–143
Zaher H (1999) Hemipenial morphology of the South American xenodontine snakes: with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bull Am Mus Nat Hist 240:1–168
Zanette I, Daghfous G, Weitkamp T, Gillet B, Adriaens D, Langer M, Cloetens P, Helfen L, Bravin A, Peyrin F, Baumbach T, Dischler J-M, Van Loo D, Praet T, Poirier-Quinot M, Boistel R (2013) Looking inside marine organisms with magnetic resonance and X-ray imaging. In: Reynaud EG (ed) Imaging marine life: macrophotography and microscopy approaches for marine biology. Wiley-Blackwell, Weinheim, pp 122–184
Ziegler A, Kunth M, Mueller S, Bock C, Pohmann R, Schröder L, Faber C, Giribet G (2011) Application of magnetic resonance imaging in zoology. Zoomorphology 130(4):227–254
Acknowledgments
We are indebted to the University of Antananarivo, Parc Botanique et Zoologique de Tsimbazaza (PBZT), the Direction des Eaux et Forêts, and the MNP for permission to visit the protected area of Isalo and to conduct research activity (authorization No. 357/10/MEF/SG/DGF/DCB.SAP/SCB of 17.XII.2010). The team of MNP at Ranohira–Isalo was very helpful, especially its director A. Rajaonarivo. The people of Madagascar Institut pour la Conservation des Ecosystèmes Tropicaux (MICET) helped with logistics and assistance. We thank our guide Anicet, our assistant Fetra, N. H. C. Rabibisoa, H. Randrianizahana, T. J. Razafindrabe, J. E. Randrianirina, D. Edmonds, and I. Lau for assistance in the field and useful talks. We also thank the team of the Centre de Microscopie de fluorescence et d'IMagerie numérique (CeMIM) (M. Gèze and M. Dellinger, Muséum National d’Histoire Naturelle) for allowing us to use the graphics workstation; and G. Tessa for helping with the microphotographs. The work was supported by the Mohamed bin Zayed Species Conservation Fund, EDGE, Zoological Society of London, Amphibian Specialist Group, Conservation International, Gondwana Conservation and Research, Regione Piemonte, and the Zurich Zoo. Additionally, we thank R. Griffiths and the anonymous reviewers for their comments that greatly improved the manuscript. G. M. Rosa holds a doctoral scholarship from the Fundação para a Ciência e a Tecnologia (SFRH/BD/69194/2010).
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Communicated by Andreas Schmidt-Rhaesa.
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Rosa, G.M., Boistel, R., Campantico, E. et al. Case solved: presence of toxin-secreting oral glands in the lamprophiid snake Mimophis mahfalensis (Grandidier, 1867) from Madagascar. Zoomorphology 133, 417–423 (2014). https://doi.org/10.1007/s00435-014-0234-7
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DOI: https://doi.org/10.1007/s00435-014-0234-7