First records of the Brahminy blindsnake, Indotyphlops braminus (Daudin, 1803) (Squamata: Typhlopidae) from Malta with genetic and morphological evidence

Year 2020, Volume: 5 Issue: 3, 122 - 135, 27.11.2020

Adriana Vella Noel Vella Clare Marie Mifsud Denis Magro

https://doi.org/10.28978/nesciences.832967

Abstract

This publication reports the first two records of the Brahminy blindsnake Indotyphlops braminus (Daudin, 1803), representing a new alien species in Malta. This species, native to Indo-Malayan region, has over the years broadened its distribution through anthropogenic international transportation of goods. Its unique parthenogenic reproductive strategy increases its potential for fast population expansion, becoming invasive. The two specimens analysed in this study were found in May, 2020, and were identified through external morphology and genetic sequencing of 12S rRNA, 16S rRNA and COI genes. These sequences were compared to other genetic data available for I. braminus from other locations, where it was found that the mitochondrial DNA variation for this species is very low at a global scale.

Keywords

Indotyphlops braminus, introduced species, reptiles, mtDNA

References

• Adalsteinsson, S.A., Branch, W.R., Trape, S., Vitt, L.J., & Hedges, S.B. (2009). Molecular phylogeny, classification, and biogeography of snakes of the family Leptotyphlopidae (Reptilia, Squamata). Zootaxa, 2244(1), 1-50.
• Auliya, M., Altherr, S., Ariano-Sánchez, D., & Ziegler, T. (2016). Trade in live reptiles, its impact on wild populations, and the role of the European market. Biological Conservation, 204, 103–119.
• Baha el Din, M.B. (1996). Ramphotyphlops braminus (Daudin, 1803) a new addition to the Egyptian herpetofauna. Journal of the National Museum (Prague), Natural History Series, 165(1-4), 130.
• Baha el Din, S.M. (2001). On the first report of Ramphotyphlops braminus from Egypt: how many times can a flower-pot snake be run over for the first time? Herpetological Review, 32(1), 11.
• Baldacchino, A.E., & Schembri, P.J. (Eds) (2002). Amfibji, rettili u mammiferi tal-gzejjer Maltin. Pubblikazzjoni Indipendenza (PIN), Pieta, Malta. 256pp.
• Bamford, M., & Prendergast, K. (2017). A further record and observations on the flowerpot snake Indotyphlops braminus in suburban Perth. The Western Australian Naturalist, 30, 229-234.
• Borroto-Paez, R., Bosch, R.A., Fabres, B.A., & Garcia, A. (2015). Introduced amphibians and reptiles in the Cuban archipelago. Herpetological Conservation and Biology, 10(3), 985-1012.
• Broadley, D.G., & Wallach, V. (2009). A review of the eastern and southern African blind-snakes (Serpentes: Typhlopidae), excluding Letheobia Cope, with the description of two new genera and a new species. Zootaxa, 2255, 1-100.
• Capinha, C., Seebens, H., Cassey, P., García‐Díaz, P., Lenzner, B., Mang, T., Moser, D., Pyšek, P., Rödder, D., Scalera, R., Winter, M., Dullinger, S., & Essl, F. (2017). Diversity, biogeography and the global flows of alien amphibians and reptiles. Diversity and Distributions, 23, 1313-1322.
• Castoe, T.A., Jiang, Z.J., Gu, W., Wang, Z.O., & Pollock, D.D. (2008). Adaptive evolution and functional redesign of core metabolic proteins in snakes. PLoS ONE, 3(5), e2201.
• Darriba, D., Taboada, G.L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772.
• Ehmann, H., & Bamford, M.J. (1993). Family Typhlopidae. In: Glasby, C.G., Ross, G.J.B., & Beesley, P.L. (eds.) Fauna of Australia - Volume 2A Amphibia and Reptilia. Canberra: AGPS Canberra.
• ERA (2012). Malta’s National Biodiversity Strategy and Action Plan 2012-2020. Available at: https://era.org.mt/en/Documents/MaltaNBSAP_2012-2020.pdf (15.06.20).
• ERA. (2018). National Strategy for Preventing and Mitigating the Impact of Invasive Alien Species (IAS) in the Maltese Islands. Available at: https://era.org.mt/en/Documents/IAS-Strategy-Final_Public_Consultation.pdf (20.06.20).
• Faraone, F.P., Barraco, L., Giacalone, G., Muscarella, C., Schifani, E., & Vecchioni, L. (2019). First records of the Brahminy blind snake, Indotyphlops braminus (Daudin, 1803) (Squamata: Typhlopidae), in Italy. Herpetology Notes, 12, 1225-1229.
• Fields, A., & Horrocks, J.A. (2011). The herpetofauna of Barbados: Anthropogenic impacts and conservation status. In: Hailey, A., Wilson, B.S., & Horrocks, J.A., (eds) Conservation of Caribbean Island Herpetofaunas, vol. 2, Leiden, Brill. pp89-104.
• Geller, J., Meyer, C., Parker, M., Hawk, H. (2013). Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources. 13, 851-861.
• Global Invasive Species Database (GISD). (2020). Species profile: Ramphotyphlops braminus. World Wide Web electronic publication. http://www.iucngisd.org/gisd/speciesname/Ramphotyphlops+braminus, version (06/2020).
• Google Earth (2020). Google Earth Pro v7.1. http://www.google.com/earth/index.html, version (06/2020).
• Hasegawa, M., Kishino, H., & Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution. 22(2): 160–174.
• Hawlitschek, O., Nagy, Z.T., Berger, J., & Glaw, F. (2013). Reliable DNA barcoding performance proved for species and island populations of comoran squamate reptiles. PLoS One. 8(9), e73368.
• Hedges, S.B., Marion, A.B., Lipp, K.M., Marin, J., & Vidal, N. (2014). A taxonomic framework for typhlopid snakes from the Caribbean and other regions (Reptilia, Squamata). Caribbean Herpetology, 49, 1-61.
• Hulme, P.E. (2015). Invasion pathways at a crossroad: policy and research challenges for managing alien species introductions. Journal of Applied Ecology, 52, 1418-1424.
• Hulme, P.E., Bacher, S., Kenis, M., Klotz, S., Kühn, I., Minchin, D., Nentwig, W., Olenin, S., Panov, V., Pergl, J., Pyšek, P., Roques, A., Sol, D., Solarz, W., & Vilà, M. (2008). Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Journal of Applied Ecology, 45, 403-414.
• ITIS (2020). Integrated Taxonomic Information System on-line database. http://www.itis.gov (13.09.20).
• Jesus, J., Goncalves, R., Spinola, C., & Brehm, A. (2013). First record of Ramphotyphlops braminus (Daudin, 1803) on Madeira Island (Portugal). Herpetozoa, 26, 106-109.
• Joger, U., Bshenia, I., & Essghaier, F. (2008). First record of the parthenogenetic Brahminy blind snake, Ramphotyphlops braminus (Daudin, 1803), from Libya (Serpentes: Typhlopidae). Herpetology Notes, 1, 13-16.
• Kamosawa, M., & Ota, H. (1996). Reproductive biology of the Brahminy blind snake (Ramphotyphlops braminus) from the Riukiu Archipelago, Japan. Journal of Herpetology, 30, 9-14.
• Kark, S., Solarz, W., Chiron, F., Clergeau, P., & Shirley, S. (2009). Alien birds, amphibians and reptiles of Europe. In: DAISIE (ed.) Handbook of Alien Species in Europe. (Springer, Berlin), pp105-118.
• Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P., & Drummond, A. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647-1649.
• Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
• Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.W., Pääbo, S., Villablanca, F.X., & Wilson, A.C. (1989). Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the United States of America, 86, 6196-6200.
• Kornilios, P. (2019). The complete mitogenome of the Eurasian blindsnake Xerotyphlops vermicularis (Reptilia, Typhlopidae). Mitochondrial DNA Part B, 4(1), 1990-1991.
• Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549.
• Lanfranco, G.G. (1955). Reptiles, amphibians of the Maltese Islands: snakes, geckos, lizards, turtles, frogs, found in Malta. Malta Yearbook 1955, 198-203.
• Legislation Malta (2020). Available at: https://legislation.mt (15.06.20).
• Lever, C. (2003). Naturalized Reptiles and Amphibians of the World. Oxford University Press, Oxford, UK.
• Liu, X., Blackburn, T.M., Song, T., Li, X., Huang, C., & Li, Y. (2019). Risks of Biological Invasion on the Belt and Road. Current Biology, 29(3), 499-505.
• Mateo, J.A. (2013). Culebrilla de las macetas - Ramphotyphlops braminus. In: Salvador, A., Marco, A. (eds.) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. Available at: http://www.vertebradosibericos.org/reptiles/rambra.html (15.06.20).
• Mateo, J.A., Ayres, C., & López-Jurado, L.F. (2011). Los anfibios y reptiles naturalizados en España; historia y evolución de una problemática creciente. Boletín de la Asociación Herpetológica Española, 22, 2-42.
• Meshaka, W.E. (2011). A runaway train in the making: the exotic amphibians, reptiles, turtles, and crocodilians of Florida. Monograph 1. Herpetological Conservation and Biology, 6, 1-101.
• Mizuno, T. & Kojima, Y. (2015), A blindsnake that decapitates its termite prey. Journal of Zoology, 297, 220-224.
• Nagy, Z.T., Marion, A.B., Glaw, F., Miralles, A., Nopper, J., Vences, M., & Hedges, S.B. (2015). Molecular systematics and undescribed diversity of Madagascan scolecophidian snakes (Squamata: Serpentes). Zootaxa, 4040(1), 31-47. 3
• NCBI (2020). Blastn suite. Available at: https://blast.ncbi.nlm.nih.gov (12.06.20).
• Ota, H., Hikida, T., Matsui, M., Mori, A., & Wynn, A. (1991). Morphological variation, karyotype and reproduction of the parthenogenetic blind snake, Ramphotyphlops braminus, from the insular region of East Asia and Saipan. Amphibia-Reptilia, 12, 181-193.
• Page, A., Kirkpatrick, W., & Massam, M. (2008). Flowerpot Snake (Ramphotyphlops braminus) risk assessments for Australia. Western Australia: Department of Agriculture and Food, Western Australia. Available at: https://www.pestsmart.org.au/wp content/uploads/2010/10/Ramphotyphlops_braminus_270410.pdf (15.06.20).
• Palumbi, S. (1996). Nucleic acids II: The polymerase chain reaction. In: Hillis, D.M., Moritz, C., & Maple, B.K. (eds). Molecular systematics. Sinauer, Sunderland, pp 205-248.
• Paolino, G., Scotti, R., & Grano, M. (2019). First detection of the “flowerpot snake” Indotyphlops braminus (Daudin, 1803) (Serpentes Typhlopidae) in Ischia (Italy): a new possible invasive species. Biodiversity Journal, 10(4), 321-324.
• Patawang, I., Tanomtong, A., Kaewmad, P., Chuaynkern, Y., & Duengkae, P. (2016). New record on karyological analysis and first study of NOR localization of parthenogenetic brahminy blind snake, Ramphotyphlops braminus (Squamata, Typhlopidae) in Thailand. Nucleus, 59, 61-66.
• Planning Authority (2002). Guidelines on Trees, Shrubs and Plants for Planting and Landscaping in the Maltese Islands. 63pp. Available at: https://www.mta.com.mt/en/file.aspx?f=31927 (12.06.20).
• Rato, C., Silva-Rocha, I., Gonzalez-Miras, E., Rodriguez- Luque, F., Farina, B., & Carretero, M.A. (2015). A molecular assessment of European populations of Indotyphlops braminus (Daudin, 1803). Herpetozoa, 27, 179-182.
• Scalera, R., (2019). Report on alien pathogens and pathogens spread by invasive alien species in Europe. Convention on the conservation of European wildlife and natural habitats. 39th meeting, Strasbourg, Dec 2019. T-PVS/Inf(2019)18. pp.25.
• Seebens, H., Blackburn, T.M., Dyer, E.E., Genovesi, P., Hulme, P.E., Jeschke, J.M., Pagad, S., Pysek, P., van Kleunen, M., Winter, M., et al. (2018). Global rise in emerging alien species results from increased accessibility of new source pools. Proceedings of the National Academy of Sciences of the United States of America, 115(10), E2264-E2273.
• Silva-Rocha, I., Salvi, D., Sillero, N., Mateo, J.A., & Carretero, M.A. (2015). Snakes on the Balearic Islands: an invasion tale with implications for native biodiversity conservation. PLoS ONE, 10, e0121026.
• Snyder, S.J., Schmidt, R.E., & Tirard, N. (2019). First report of the Brahminy Blindsnake, Indotyphlops braminus (Daudin), from the Caribbean island of Montserrat. Caribbean Herpetology, 65, 1-2.
• Speybroeck, J., Beukema, W., & Crochet, P.A. (2010). A tentative species list of the European herpetofauna (Amphibia and Reptilia) - An Update. Zootaxa, 2492, 1-27.
• Sultana, J., & Falzon, V. (eds). (1996). Wildlife of the Maltese Islands. Birdlife, Malta 336pp.
• Tamura, K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution, 9, 678-687.
• The Malta Independent (2015). Available at: https://www.independent.com.mt/articles/2016-08-07/local-news/Malta-Football-Association-plans-ahead-new-hybrid-pitch-at-Ta-Qali-Stadium-6736162071 (16.06.20).
• Uetz, P., Freed, P., & Hošek, J. (eds.) (2020) The Reptile Database. World Wide Web electronic publication. http://www.reptile-database.org, version (06/2020).
• Urioste, J.A. de, & Mateo, J.A. (2011). Nuevos datos acerca de la culebrilla ciega de las macetas, Ramphotyphlops braminus (Daudin 1803), en Canarias. Boletín de la Asociación Herpetológica Española, 22, 135-137.
• Vidal, N., & Hedges, S.B. (2002). Higher-level relationships of caenophidian snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus Biologies, 325(9), 987-995.
• Wallach, V. (2009). Ramphotyphlops braminus (Daudin): a synopsis of morphology, taxonomy, nomenclature and distribution (Serpentes: Typhlopidae). Hamadryad, 34, 34-61.
• Wynn, A., Cole, C.J., & Gardner, A.L. (1987). Apparent triploidy in the unisexual Brahminy blind snake, Ramphotyphlops braminus. American Museum Novitates, 2868, 1-7.
• Yan, J., Li, H., & Zhou, K. (2008). Evolution of the mitochondrial genome in snakes: gene rearrangements and phylogenetic relationships. BMC genomics, 9, 569.
• Young, H.S, Parker, I.M., Gilbert, G. S., Guerra, A.S. & Nunn, C.L. (2016). Introduced species, disease ecology and biodiversity-disease relationships. Trends in Ecology & Evolution, 32(1):41-54.
• Zamora-Camacho, F.J. (2017): On the role of plant nurseries introducing Indotyphlops braminus (Daudin, 1803), in Spain. Herpetozoa, 30, 69-72.