Unveiling an enigma from the Cerrado: taxonomic revision of two sympatric species of Apostolepis Cope, 1862 (Dipsadidae: Xenodontinae: Elapomorphini) from central Brazil
Abstract
Apostolepis albicollaris and A. cerradoensis are two Elapomorphini snake species, described within a short timespan, from the Cerrado of central Brazil. In their brief descriptions, these two species were diagnosed from congeners largely based on highly variable external morphological characters. Interestingly enough, A. cerradoensis has remained known based on a single specimen since its description. Here, we present a reanalysis of both type specimens, as well as a careful examination of a large series of specimens formerly assigned to these species, based on the comparison of internal and external morphology. We conclude that both species are synonymous, providing evidence for the recognition of A. cerradoensis as a junior synonym of A. albicollaris. Furthermore, an account of its updated diagnosis, morphological variation, geographic distribution, hemipenial morphology, phylogenetic relationships and an osteological description are also provided. We also discuss its conservation status, suggesting that the species is under threat and qualifies to be listed as Vulnerable (VU ab(iii)), considering its rarity, small geographic range, and persistent environmental threats.
References
Bachman S., Moat J., Hill A.W., de la Torre J. & Scott B. 2011. Supporting Red List threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117–126. https://doi.org/10.3897/zookeys.150.2109
Bullock R.E. & Tanner W.W. 1966. A comparative osteological study of two species of Colubridae (Pituophis and Thamnophis). Brigham Young University Science Bulletin Biological Series 8: 1–29.
Burgos-Gallardo F., Baldo J.L., Vilte A. & Scrocchi G. 2017. Apostolepis multicincta Harvey 1999 (Squamata, Dipsadidae) in Argentina. Check List 13: 913–916. https://doi.org/10.15560/13.6.913
Cabral H., Lema T.D. & Renner M.F. 2017. Revalidation of Apostolepis barrioi (Serpentes: Dipsadidae). Phyllomedusa 16: 243–254. https://doi.org/10.11606/issn.2316-9079.v16i2p243-254
Cundall D. & Irish F. 2008. The snake skull. In: Gans C., Gaunt A.S. & Adler K. (eds) Biology of Reptilia. The Skull of Lepidosauria: 349–692. Society for the Study of Amphibians and Reptiles Press, USA.
Curcio F.F., Nunes P.M.S., Harvey M.B. & Rodrigues M.T. 2011. Redescription of Apostolepis longicaudata (Serpentes: Xenodontinae) with comments on its hemipenial morphology and natural history. Herpetologica 67 (3): 318–331. https://doi.org/10.1655/HERPETOLOGICA-D-10-00043.1
Dowling H.G. 1951. A proposed standard system of counting ventrals in snakes. British Journal of Herpetology 1: 97–99.
Drummond A., Ashton B., Buxton S., Cheung M., Cooper A., Duran C. & Wilson A. 2010. Geneious pro. Geneious Biomatters Ltd, Auckland.
Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32 (5): 1792–1797. https://doi.org/10.1093/nar/gkh340
Entiauspe-Neto O.M., de Sena A., Tiutenko A. & Loebmann D. 2019. Taxonomic status of Apostolepis barrioi Lema, 1978, with comments on the taxonomic instability of Apostolepis Cope, 1862 (Serpentes, Dipsadidae). ZooKeys 841: 71–78. https://doi.org/10.3897/zookeys.841.33404
Entiauspe-Neto O.M., Koch C., Guedes T.B. & Tiutenko A. 2020a. Revisiting the taxonomic status of Apostolepis sanctaeritae, a forgotten Neotropical dipsadid snake. Salamandra 56: 329–341.
Entiauspe-Neto O.M., Guedes T.B., Loebmann D. & Lema T. 2020b. Taxonomic status of two simultaneously described Apostolepis Cope, 1862 species (Dipsadidae: Elapomorphini) from Caatinga Enclaves moist forests, Brazil. Journal of Herpetology 54: 225–234. https://doi.org/10.1670/19-053
Entiauspe-Neto O.M., Rangel G.M.F., Guedes T.B. & Tiutenko A. 2020c. Raising of Lazarus: rediscovery and redescription of Apostolepis niceforoi Amaral, 1935 (Serpentes: Dipsadidae: Elapomorphini). Holotipus 1: 21–35.
Entiauspe-Neto O.M., Koch C., Gray R.J., Tiutenko A., Loebmann D. & Guedes T.B. 2021a. On the identity of Apostolepis tertulianobeui Lema, 2004 and integrative revision of Apostolepis assimilis (Reinhardt, 1861) (Serpentes: Dipsadidae). Zoologischer Anzeiger 291: 123–138. https://doi.org/10.1016/j.jcz.2021.01.004
Entiauspe-Neto O.M., Koch C., Harvey M.B., Colli G.R. & Guedes T.B. 2021b. Redescription of Apostolepis ambiniger (Peters, 1869) (Serpentes: Dipsadidae: Elapomorphini). Vertebrate Zoology 71: 231–251. https://doi.org/10.3897/vz.71.e65097
Entiauspe-Neto O.M., Abegg A.D., Koch C., Nuñez L.P., Azevedo W.D.S., Moraes L.J., Tiutenko A., Bialves T.S. & Loebmann D. 2021c. A new species of Erythrolamprus (Serpentes: Dipsadidae: Xenodontini) from the savannas of northern South America. Salamandra 57 (2): 196–218.
Ferrarezzi H. 1993. Sistemática Filogenética de Elapomorphus, Phalotris e Apostolepis (Serpentes, Colubridae, Xenodontinae). PhD thesis, Universidade de São Paulo, Brazil.
Ferrarezzi H. 1994. Uma sinopse 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: 81–91. PUCMG, Belo Horizonte.
Ferrarezzi H., Barbo F.E. & Albuquerque C.E. 2005. Phylogenetic relationships of a new species of Apostolepis from Brazilian Cerrado, with notes on the assimilis group (Serpentes: Colubridae: Xenodontinae: Elapomorphini). Papéis Avulsos de Zoologia 45: 215–229. https://doi.org/10.1590/S0031-10492005001600001
Giraudo A.R. & Scrocchi G.J. 1998. A new species of Apostolepis (Serpentes: Colubridae) and comments on the genus in Argentina. Herpetologica 54 (4): 470–476.
Guedes T.B., Nogueira C. & Marques O.A.V. 2014. Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa 3863 (1): 1–93. https://doi.org/10.11646/zootaxa.3863.1.1
Harvey M.B. 1999. Revision of Bolivian Apostolepis (Squamata: Colubridae). Copeia 1999: 388–409. https://doi.org/10.2307/1447485
Hasegawa M., Kishino H. & Yano T.A. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22 (2): 160–174. https://doi.org/10.1007/BF02101694
Huelsenbeck J.P. & Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17 (8): 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
ICMBio 2021. Mapa temático e Dados geoestatísticos das Unidades de Conservação Federais. Available from https://icmbio.gov.br [accessed 4 Nov. 2021].
Lema T.D. 1993. Polimorfismo em Apostolepis dimidiata (Jan, 1862) com a invalidação de Apostolepis villaricae Lema, 1978 e Apostolepis barrioi Lema, 1978 (Serpentes: Colubridae: Xenodontinae: Elapomorphini). Acta Biologica Leopoldensia 15: 35–52.
Lema T.D. 2002. Nova espécie de Apostolepis Cope do grupo dimidiata do Cerrado do Brasil (Serpentes: Elapomorphinae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia 15 (2): 227–238.
Lema T.D. 2003. Descrição de nova espécie de Apostolepis Cope do cerrado do Brasil, pertencente ao grupo dimidiata (Serpentes, Elapomorphinae). Acta Biologica Leopoldensia 25 (1): 123–131.
Lema T.D. 2004a. Nova espécie de Apostolepis Cope do estado de Rondônia, Brasil (Serpentes, Elapomorphinae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia 17 (2): 81–89.
Lema, T.D. 2004b. Description of a new species of Apostolepis Cope, 1861 (Serpentes, Elapomorphinae) from Brazilian Cerrado. Acta Biologica Leopoldensia 26 (1): 155–160.
Lema T.D. & Hofstadler-Deiques C. 2010. Description of a new genus for allocation of Elapomorphus lepidus and the status of Elapomorphus wuchereri (Serpentes: Dipsadidae: Xenodontinae: Elapomorphini). Neotropical Biology and Conservation 5 (2): 113–119. https://doi.org/10.4013/4756
Lema T.D. & Renner M.F. 2005. Contribuição ao conhecimento taxonômico de Apostolepis flavotorquata (Serpentes, Elapomorphinae). Biociências 13 (2): 163–175.
Lema T.D. & Renner M.F. 2011. A new species of Apostolepis (Serpentes, Colubridae, Elapomorphini), belonging to assimilis group, found in Brazilian Cerrado. Ciência em Movimento 13 (27): 71–76.
MapBiomas 2021. Collections 1 and 4 of the Annual Series of Brazilian Land Use and Land Cover. Available from https://mapbiomas.org [accessed 4 Nov. 2021].
Montingelli G.G., Barbo F.E., Pereira Filho G.A., Santana G.G, França F.G.R., Grazziotin F.G. & Zaher H. 2020. A second new species for the rare dipsadid genus Caaeteboia Zaher et al., 2009 (Serpentes: Dipsadidae) from the Atlantic Forest of northeastern Brazil. Cuadernos de Herpetología 34: 219–230.
Moraes L.J., Entiauspe-Neto O.M., de Fraga R., Fernandes I.Y. & Werneck F.P. 2021. Systematics of the rare Amazonian genus Eutrachelophis (Serpentes: Dipsadidae), with an emended diagnosis for Eutrachelophis papilio. Zoologischer Anzeiger 295: 191–204. https://doi.org/10.1016/j.jcz.2021.10.003
Nogueira C.C., Barbo F.E. & Ferrarezzi H. 2012. Redescription of Apostolepis albicollaris Lema, 2002, with a key for the species groups of the genus Apostolepis (Serpentes: Dipsadidae: Elapomorphini). South American Journal of Herpetology 7 (3): 213–225. https://doi.org/10.2994/057.007.0303
Nogueira C.C., Argôlo A.J.S., Arzamendia V., Azevedo J.A., Barbo F.E., Bérnils R.S., Bolochio B.E., Borges-Martins M., Brasil-Godinho M., Braz H., Buononato M.A., Cisneros-Heredia D.F., Colli G.R., Costa H.C., Franco F.L., Giraudo A., Gonzales R.C., Guedes T., Hoogmoed M.S., Marques O.A.V., Montingelli G.G., Passos P., Prudente A.L.C., Rivas G.A., Sanchez P.M., Serrano F.C., Silva-Jr N.J., Strüssmann C., Vieira-Alencar J.P.S., Zaher H., Sawaya R.J. & Martins M. 2019. Atlas of Brazilian snakes: verified point-locality maps to mitigate the Wallacean shortfall in a megadiverse snake fauna. South American Journal of Herpetology 14 (Suppl. 1): 1–274. https://doi.org/10.2994/SAJH-D-19-00120.1
Paradis E. & Schliep K. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35 (3): 526–528. https://doi.org/10.1093/bioinformatics/bty633
Peters J.A. 1964. Supplemental notes on snakes of the subfamily Dipsadinae (Reptilia: Colubridae). Studies on Neotropical Fauna and Environment 4 (1): 45–50. https://doi.org/10.1080/01650526409360376
QGIS Development Team 2021. QGIS Geographic Information System. Version 3.16.3. Available from http://www.qgis.org [accessed 1 Aug. 2021].
R Core Team 2015. Team R: a language and environment for statistical computing, Release 3.2. Available from http://cran.r-project.org [accessed 1 Aug. 2021].
Rodrigues M.T. 1992. Herpetofauna das dunas interiores do Rio São Francisco: Bahia: Brasil. V. Duas novas espécies de Apostolepis (Ophidia, Colubridae). Memórias do Instituto Butantan 54 (2): 53–59.
Sabaj M.H. 2019. Standard Symbolic Codes for Institutional Resource Collections in Herpetology and Ichthyology: An Online Reference. Version 6.5. American Society of Ichthyologists and Herpetologists, Lawrence, KS. Available from http://www.asih.org [accessed 10 Sep. 2021].
Saint K.M., Austin C.C., Donnellan S.C. & Hutchinson M.N. 1998. C-mos, a nuclear marker useful for squamate phylogenetic analysis. Molecular Phylogenetics and Evolution 10 (2): 259–263. https://doi.org/10.1006/mpev.1998.0515
Savitzky A.H. 1979. The Origin of the New World Proteroglyphous Snakes and its Bearing on the Study of Venom Delivery Systems in Snakes. PhD thesis, University of Kansas, Lawrence, KS.
Souza Jr. C.M., Shimbo J.Z., Rosa M.R., Parente L.L., Alencar A.A., Rudorff B.F.T., Hasenack H., Matsumoto M., Ferreira L.G., Souza-Filho P.W.M., Oliveira S.W., Rocha W.F., Fonseca A.V., Marques C.B., Diniz C.G., Costa D., Monteiro D., Rosa E.R., Vélez-Martin E., Weber E.J., Lenti F.E.B., Paternost F.F., Pareyn F.G.C., Siqueira J.V., Viera J.L., Neto L.C.F., Saraiva M.M., Sales M.H., Salgado M.P.G., Vasconcelos R., Galano S., Mesquita V.V. & Azevedo T. 2020. Reconstructing three decades of land use and land cover changes in Brazilian biomes with Landsat Archive and Earth Engine. Remote Sensing 12 (7): e2735. https://doi.org/10.3390/rs12172735
Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28 (10): 2731–2739. https://doi.org/10.1093/molbev/msr121
Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17 (2): 57–86.
Zaher H. 1994. Phylogénie des Pseudoboini et Évolution des Xenodontinae Sud-américains (Serpentes, Colubridae). PhD thesis, Muséum national d’histoire naturelle, Paris.
Zaher H. 1999. 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: 1–168. Available from https://www.biodiversitylibrary.org/bibliography/90073 [accessed 6 Apr. 2022].
Zaher H., Grazziotin F.G., Cadle J.E., Murphy R.W., Moura-Leite J.C.D. & Bonatto S.L. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia 49: 115–153. https://doi.org/10.1590/S0031-10492009001100001
Zaher H., Murphy R.W., Arredondo J.C., Graboski R., Machado-Filho P.R., Mahlow K., Montingelli G.G., Quadros A.B., Orlov N.L., Wilkinson M., Zhang Y.-P. & Grazziotin F.G. 2019. Large-scale molecular phylogeny, morphology, divergence-time estimation, and the fossil record of advanced caenophidian snakes (Squamata: Serpentes). PLoS ONE 14 (5): e0216148. https://doi.org/10.1371/journal.pone.0216148
Zar J.H. 1999. Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, USA.
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