Oral glands in dipsadine "goo-eater" snakes: Morphology and histochemistry of the infralabial glands in Atractus reticulatus, Dipsas indica, and Sibynomorphus mikanii

Toxicon

Volumn 51, Issue 5, 2008, Pages 898-913

  de Oliveira, Leonardo ^a   Jared, Carlos ^a   da Costa Prudente, Ana Lúcia ^b   Zaher, Hussam ^c   Antoniazzi, Marta Maria ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b MUSEU PARAENSE EMÍLIO GOELDI   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Colubridae; Dipsadinae; Goo eaters; Infralabial glands; Morphology; Serpentes

Indexed keywords

SNAKE VENOM;

ANIMAL TISSUE; ARTICLE; BRAZIL; CONTROLLED STUDY; FEEDING BEHAVIOR; HISTOCHEMISTRY; MALE; MUCOUS CELL; NONHUMAN; PRIORITY JOURNAL; SECRETORY GRANULE; SNAKE;

ANIMALS; COLUBRIDAE; FEEDING BEHAVIOR; FEMALE; HISTOCYTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MOUTH; SALIVARY GLANDS, MINOR;

ATRACTUS; COLUBRIDAE; DIPSADINAE; DIPSAS INDICA; GASTROPODA; INVERTEBRATA; SERPENTES;

EID: 40649102368     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2007.12.021     Document Type: Article

References (63)

1. Antoniazzi, M., Oliveira, L., Zaher, H., Jared, C., 2005. Morphological characterization of the infralabial glands of "goo-eater" snakes (Colubridae: Dipsadinae). IN: Abstracts of Fifth World Congress of Herpetology, Stellemboch, South Africa, p. 119.
2. Baccari G.C., Ferrara D., Di Matteo L., and Minucci S. Morphology of the salivary glands of three Squamata species: Podarcis sicula sicula, Tarentola mauritanica and Coluber viridiflavus. Acta Zool. (Stockholm) 83 (2002) 117-124
3. Bancroft J.D., and Stevens A. Theory and Practice of Histological Techniques. fourth ed (1996), Churchill Livingstone, New York 766pp
4. Brongersma. The palato-maxillary arch in some Asiatic Dipsadinae (Serpentes). Proc. Kon. Ned. Akad. Wet., Amsterdam, Ser. C 59 (1956) 439-446
5. 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 (1993), University of Chicago Press, Chicago 281-293
6. Campbell J.A., and Smith E.N. A new genus and species of colubrid snake from the Sierra de Las Minas of Gratemala. Herpetologica 54 2 (1998) 207-220
7. Contrera M.G.D., Lopes R.A., Costa J.R.V., Petenusci S.O., and Lima-Verde J.S. The histology of salivary glands in the colubrid snake Sibynomorphus mikanii (Schlegel, 1837). Can. J. Zool. 61 (1983) 936-941
8. Dowling H.G., and Duellman W.E. Systematic Herpetology: A Synopsis of Families and Higher Categories (1978), HISS Publications, New York
9. Dunn E.R. The status of the snake genera Dipsas and Sibon, a problem for "quantum evolution". Evolution 5 (1951) 355-358
10. Fernandes, R., 1995. Phylogeny of the dipsadine snakes. Thesis (Doctor of Philosophy), The University of Texas at Arlington, 115pp.
11. Ferrarezzi, H., 1994. Uma sinópse dos gêneros e classificação das serpentes "Squamata". II. Família Colubridae. In: Nascimento, L.B., Bernardes, A.T., Cotta, G.A. (Eds.), Herpetologia no Brasil 1. Editora PUC-MG, Fundação Esequiel Dias, Fundação Biodiversitas, Belo Horizonte, pp. 81-91.
12. Franco, F.L., 1994. O gênero Sibynomorphus Fitzinger, 1843, no Brasil (Colubridae: Xenodontinae, Dipsadini). Dissertação (Mestrado em Zoologia), Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre.
13. Fry B.G., Vidal N., Norman J.A., Vonk F.J., Scheib H., Ramjan S.F.R., Kuruppu S., Fung K., Hedges S.B., Richardson M.K., Hodgson W.C., Ignjatovic V., Summerhayes R., and Kochva E. Early evolution of the venom system in lizards and snakes. Nature 439 (2006) 584-589
14. Gabe M., and Saint-Girons H. Données histologiques sur les glandes salivaires des lépidosauriens. Mem. Mus. Nat. Hist. Nat. A 58 1 (1969) 3-116
15. Gans C. Feeding in Dipsas indica and Dunn's paradox. Am. Zool. 12 4 (1972) 730
16. Gopalakrishnakone P., and Kochva E. Histological features of the venom apparatus of sea snake Lapemis curtus. Snake 25 (1993) 27-37
17. Haas. Anatomical observations on the head of Liotyphlops albirostris (Typhlopidae, Ophidia). Acta Zool. 45 (1964) 1-62
18. Jackson K. The evolution of venom-delivery systems in snakes. Zool. J. Linn. Soc. 137 (2003) 227-354
19. Junqueira L.C.U. Histology revisited-technical improvement promoted by the use of hydrophilic resin embedding. Rev. Ciên. Cult. 47 (1995) 92-95
20. Kardong K.V. Snake toxins and venoms: an evolutionary perspective. Herpetologica 52 1 (1996) 36-46
21. Kardong K.V. Colubrid snakes and Duvernoy's "venom" glands. J. Toxicol.-Toxin Rev. 21 1&2 (2002) 1-19
22. Kardong K.V., and Luchtel D.L. Ultrastructure of Duvernoy's gland from the wandering garter snake, Thamnophis elegans vagrans (Serpentes, Colubridae). J. Morphol. 188 (1986) 1-13
23. Karnovsky M.J. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27A (1965) 137-138
24. Kelly C.M.R., Barker N.P., and Villet M.H. Phylogenetics of advanced snakes (Caenophidia) based on four mitochondrial genes. Syst. Biol. 52 (2003) 439-459
25. Kiernan J.A. Histological and Histochemical Methods-Theory and Practice. third ed (2001), Oxford University Press, London 213-220
26. Kley N.J. Morphology of the lower jaw and suspensorium in the Texas blindsnake, Leptotyphlops dulcis (Scolecophidia: Leptotyphlopidae). J. Morphol. 267 (2006) 494-515
27. Kochva E. Oral glands of the reptilia. In: Gans C. (Ed). Biology of the reptilia vol. 8 (1978), Academic Press, London, New York 782pp
28. Kochva E. The origin of snakes and evolution of the venom apparatus. Toxicon 25 1 (1987) 65-106
29. Kraus F., and Brown W.M. Phylogenetic relationships of colubroid snakes based on mitochondrial DNA sequences. Zool. J. Linn. Soc. 122 (1998) 455-487
30. Laporta-Ferreira I.L. Fisioecologia da serpente moluscófaga-Sibynomorphus neuwiedi-(Colubridae, Dipsadinae) (1985), Dissertação (Mestrado em Fisiologia)-Instituto de Biociências, Universidade de São Paulo, São Paulo
31. 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). Zool. Anz. 227 (1991) 198-208
32. Laporta-Ferreira I.L., Salomão M.G., Sawaya P., and Puorto G. Mecanismo de tomada de alimento por serpentes tropicais moluscófagas (Sibynomorphus neuwiedi e Sibynomorphus mikanii) adaptações morfofisiológicas do esqueleto cefálico. Bol. Fisiol. Anim. São Paulo 12 (1988) 81-88
33. Lawson R., Slowinski J.B., Crother B.I., and Burbrink F.T. Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Mol. Phylogenet. Evol. 37 (2005) 581-601
34. Lopes R.A., Valeri V., Campos G.M., and Faria R.M. Estudo morfológico e histoquímico de mucopolissacarídeos em glândulas cefálicas de Micrurus c. corallinus (Ophidia, Elapidae). Rev. Ciên. Cult. 24 (1972) 214
35. Lopes R.A., Costa J.R.V., Petenusci S.O., and Contrera M.G.D. The salivary glands of Leimadophis viridis (Günther, 1862) (Ophidea Colubridae): a morphological, morphometric and histochemical study. Monit. Zool. Ital. (N.S.) 15 (1981) 249-261
36. Lopes R.A., Contrera M.G.D., Costa J.R.V., Petenusci S.O., and Lima-Verde J.S. Les glandes salivaires de Philodryas patagoniensis Girard, 1857 (Serpentes Colubridae). Etude morphologique, morphométrique et histochimique. Arch. Anat. Microsc. 71 3 (1982) 175-182
37. Marques O.A.V., Eterovic A., and Sazima I. Serpentes da Mata Atlântica. Guia ilustrado para a Serra do Mar (2001), Holos, Ribeirão Preto 184pp
38. McDowell S.B. Systematics. In: Seigel R.A., Collins J.T., and Novak S.S. (Eds). Snakes: Ecology and Evolutionary Biology (1987), Macmillan Publishing, New York, NY 3-50
39. Oliveira J.L. Ecologia de três espécies de dormideira, Sibynomorphus (Serpentes: Colubridae) (2001), Dissertação (Mestrado em Ecologia)-Instituto de Biociências, Universidade de São Paulo, São Paulo
40. Pearse A.G. Histochemistry: Theoretical and Applied, vol. 2. fourth ed (1985), Churchill Livingstone, Edinburg 684-687
41. Pough F.H. Feeding mechanisms, body size, and the ecology and evolution of snakes. Am. Zool. 23 (1983) 339-342
42. Pough F.H., and Groves J.D. Specializations of the body form and food habits of snakes. Am. Zool. 23 (1983) 443-454
43. Sakai T. Major ocular glands (Harderian gland and lacrimal gland) of the musk shrew (Suncus murinus) with a review on the comparative anatomy and histology of the mammalian lacrimal glands. J. Morphol. 2001 (1989) 39-57
44. Salomão M.G. Estrutura e secreção das glândulas de Duvernoy de Sibynomorphus mikanii (Colubridae: Dipsadinae) e Philodryas olfersii (Colubridae: Xenodontinae), e das glândulas de veneno de Bothrops jararaca (Viperidae: Crotalinae) e Micrurus frontalis (Elapidae: Elapinae) e sua influência dos estados de alimentação e jejum (1991), Tese (doutorado em Fisiologia)-Instituto de Biociências, Universidade de São Paulo, São Paulo 122pp
45. 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. J. Herpetol. 28 (1994) 369-371
46. Salomão M.G., and Sawaya P. Propriedades tóxicas da saliva de serpentes áglifas: Sibynomorphus mikani (Colubridae: Dipsadinae). Ann. Acad. Bras. Ci. 64 2 (1992)
47. Savitzky A.H. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. Amer. Zool. 23 (1983) 397-409
48. Sazima I. Feeding behavior of the snail-eating snake, Dipsas indica. J. Herpetol. 23 (1989) 464-468
49. 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. J. Linn. Soc. (Zool.) (London) 41 (1947) 353-368
50. Tandler B., Nagato T., and Phillips C.J. Systematic implications of comparative ultrastructure of secretory acini in the submandibular salivary gland in Artibeus (Chiroptera: Phyllostomidae). J. Mammal. 67 1 (1986) 81-90
51. Taub A.M. Ophidian cephalic glands. J. Morphol. 118 (1966) 529-542
52. Taub A.M. Comparative studies on Duvernoy's gland of colubrid snakes. Bull. Am. Mus. Nat. Hist. 138 (1967) 1-50
53. Underwood G. A Contribution to the Classification of Snakes (1967), British Museum (Natural History), London, UK
54. Underwood G. An overview of venomous snake evolution. Symp. Zool. Soc. Lond. 70: 1-13. In: Thorpe R.S., Wüster W., and Malhotra A. (Eds). Venomous Snake. Ecology, Evolution and Snakebite (1997), The Zoological Society of London. Clarendon Press, Oxford
55. Underwood G. On the rictal structures of some snakes. Herpetologica 58 1 (2002) 1-17
56. Vidal N. Colubroid systematics: evidence for an early appearance of the venom apparatus followed by extensive evolutionary timkering. J. Toxicol.-Toxin Rev. 21 1&2 (2002) 21-41
57. Voris H.K., and Voris H.H. Feeding strategies in marine snakes: an analysis of evolutionary, morphological, behavioral and ecological relationships. Am. Zool. 23 (1983) 411-425
58. Yoshie S., Ishiyama M., and Ogawa T. Fine structure of Duvernoy's gland of the japanese colubrid snake, Rhabdophis tigrinus. Arch. Histol. Jap. 45 4 (1982) 375-384
59. Zago D.A. Estudo morfológico e histoquímico de glândulas salivares relacionadas com a evolução da função venenosa nos ofídios (1971), Tese (doutorado), Universidade de São Paulo, São Paulo
60. Zaher H. Comments on the evolution of the jaw adductor musculature of snakes. Zool. Lin. Soc. 111 (1994) 339-384
61. Zaher, H., 1996. A musculatura associada à glândula infralabial de Dipsas neivai: um novo sistema de inoculação de veneno relacionado à malacofagia (Serpentes, Dipsadinae). In: Resumos do XXI Congresso Brasileiro de Zoologia, vol. 940, p. 201.
62. Zaher H. 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 (1999) 168pp
63. Zalisko E.J., and Kardong K. Histology and histochemistry of the Duvernoy's gland of the brown snake Boiga irregularis (Colubridae). Copeia 1992 3 (1992) 791-799