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Unveiling diversity under the skin: comparative morphology study of the cephalic glands in threadsnakes (Serpentes: Leptotyphlopidae: Epictinae)

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Abstract

The subfamily Epictinae contains about 75 currently recognized species of strictly fossorial snakes distributed along the Neotropics (subtribe Renina) and Equatorial Africa (subtribe Rhinoleptini). Although several studies have addressed some internal phenotypic characters complexes for the taxa included in this subfamily, most of the available data are limited to skull morphology and visceral topology. Additionally, many studies, when reporting glandular information, do not provide comparative data obtained through of a replicable methodology. In this study, we aimed to describe in detail the macrostructure of the cephalic glands for the members of the subfamily Epictinae. We provide herein the first report of a rictal gland for the infraorder Scolecophidia, as well as the first report of an infralabial accessory gland for the family Leptotyphlopidae. We highlight the utility of glandular qualitative characters for the systematics and even alpha taxonomy of this group of snakes that frequently exhibits a conserved external morphology. Furthermore, we also discuss possible functional aspects related to the Harderian gland in association to the M. adductor externus superficialis based on macrostructure observations of Epictinae specimens.

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Acknowledgements

We are thankful to the following persons for allowing them to conduct dissections in the specimens: F. L. Franco and G. Puorto (IBSP), H. Zaher (MZUSP), A. L. C. Prudente (MPEG), F. F. Curcio (UFMT), G. Colli and M. Zatz (CHUNB), M. Pires (LZV/UFOP), C. Raxworthy (AMNH), (FMNH), K. de Queiroz, R. Wilson, R. McDiarmid and A. Wynn (USNM), C. Phillips (UIMNH), J. L. Watters (OMNH), R. Brown (KU), B. Hollingsworth (SDMNH), N. Camacho (LACM), J. Rosado (MCZ), O. Torres-Carvajal (QCAZ), S. Kretzschmar (FML). Angele Martins is grateful to the Smithsonian Institute for the Short-Term Fellowship Grant provided and to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship (process 99999.010032/2014-02) provided during her PhD; and to K. de Queiroz, D. Johnson, A. Nonaka, R. McDiarmid and all USNM staff for the support during the conduction of the project in the USA. Angele Martins was supported by Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro (FAPERJ, E-26/202.403/2017). Paulo Passos was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq processes 8256995713198058, 482086/2012-2, and 306227/2015-0) and Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro (FAPERJ, E-26/110.434/2012 and E-26/111.636/2012). We would also like to thank the anonymous reviewers for valuable contributions to the first version of the manuscript.

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Contributions

AM, PP and RP conceived the study. AM performed dissections, evaluated the characters state and produced the illustrations. All authors analyzed and discussed the findings and wrote the manuscript.

Corresponding author

Correspondence to Angele Martins.

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Research involving human participants and/or animals

This article does not contain any studies with human participants performed by any of the authors. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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International, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Additional information

Material examined

Epictia ater (n = 1): EL SALVADOR: SAN MIGUEL: KU18384.

Epictia phenops (n = 1): MEXICO: OAXACA: FMNH 111477.

Epictia tenella (n = 2): BRAZIL: PARÁ: Oriximiná: Porto Trombetas: MNRJ 16827. TRINIDAD AND TOBAGO: TRINIDAD: Guayagueyare: MCZ 60801.

Mitophis lepitepileptus (n = 1): HAITI: SUD-EST: Soliette: USNM275548.

Rena dulcis (n = 2): UNITED STATES OF AMERICA: OKLAHOMA: Comanche: OMNH35564, 35580.

Rena humilis (n = 2): UNITED STATES OF AMERICA: CALIFORNIA: San Diego: FMNH 33950, 34302.

Rena segrega (n = 2): UNITED STATES OF AMERICA: NEW MEXICO: Doña Ana: LACM, 134007, 134009.

Rena unguirostris (n = 1): ARGENTINA: TINOGASTA: Palo Blanco: FML 1773.

Siagonodon cupinensis (n = 1): BRAZIL: MATO GROSSO: Barra do Tapirapés: Guarantã do Norte: UFMT 5627.

Tetracheilostoma bilineatum (n = 1): MARTINIQUE: LE LAMENTIN: without locality: USNM 564808.

Trilepida brasiliensis (n = 1): BRAZIL: MATO GROSSO DO SUL: Corumbá: UFMT 1159.

Trilepida dimidiata (n = 1): BRAZIL: RORAIMA: Boa Vista: MZUSP 10090.

Trilepida fuliginosa (n = 1): BRAZIL: GOIÁS: Luziânia: CHUNB 40847.

Trilepida jani (n = 1): BRAZIL: MINAS GERAIS: Ouro Preto: LZV 813S.

Trilepida joshuai (n = 1): COLOMBIA: ANTIOQUIA: Jericó: IBSP 8919.

Trilepida koppesi (n = 1): BRAZIL: GOIÁS: Aporé: MNRJ 24715.

Trilepida macrolepis (n = 1): BRAZIL: PARÁ: Parauapebas: Floresta Nacional de Carajás: MPEG 23017.

Trilepida salgueiroi (n = 1). BRAZIL: ESPÍTITO SANTO: Governador Lindemberg: MNRJ 12132.

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Martins, A., Passos, P. & Pinto, R. Unveiling diversity under the skin: comparative morphology study of the cephalic glands in threadsnakes (Serpentes: Leptotyphlopidae: Epictinae). Zoomorphology 137, 433–443 (2018). https://doi.org/10.1007/s00435-018-0409-8

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