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Type: Article
Published: 2019-03-11
Page range: 301–344
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A new species of Bothrops (Serpentes: Viperidae: Crotalinae) from Pampas del Heath, southeastern Peru, with comments on the systematics of the Bothrops neuwiedi species group

Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Centro de Zoología Aplicada, Rondeau 798, Córdoba 5000, Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto de Diversidad y Ecología Animal (IDEA), Rondeau 798, Córdoba 5000, Argentina.
Laboratório de Coleções Zoológicas, Instituto Butantan, Avenida Vital Brasil, 1500, São Paulo, SP, Brazil.
Área de Herpetología, Museo de Historia Natural de la Universidad Nacional de San Agustín, 051, Arequipa 04000, Perú.
Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany.
Museo de Biodiversidad del Perú, Urbanización Mariscal Gamarra A-61, Zona 2, Cusco, Perú. Museo de Historia Natural de la Universidad Nacional de San Antonio Abad del Cusco, Paraninfo Universitario (Plaza de Armas s/n), Cusco, Perú. Frankfurt Zoological Society-Perú, Residencial Huancaro, Los Cipreses H-21, Santiago, Cusco, Perú.
UEL-CONICET and Fundación Miguel Lillo, Miguel Lillo 251, San Miguel de Tucumán, Tucumán, Argentina
Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Centro de Zoología Aplicada, Rondeau 798, Córdoba 5000, Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto de Diversidad y Ecología Animal (IDEA), Rondeau 798, Córdoba 5000, Argentina.
Museo de Biodiversidad del Perú, Urbanización Mariscal Gamarra A-61, Zona 2, Cusco, Perú. Museo de Historia Natural de la Universidad Nacional de San Antonio Abad del Cusco, Paraninfo Universitario (Plaza de Armas s/n), Cusco, Perú.
Reptilia Bothrops mattogrossensis species delimitation molecular phylogeny morphological characters total evidence

Abstract

We describe a new species of pitviper of the genus Bothrops from the Peruvian Pampas del Heath, in the Bahuaja-Sonene National Park. Pampas del Heath is an area of seasonally flooded savannas and a northwestern extension of the Gran Chaco Boliviano-Paraguayo. The new species is easily distinguished from its congeners by the exclusive combination of dorsal color pattern of body consisting of small C-shaped blotches, postocular stripe originating posteriorly to the eye, covering posterior supralabials, dorsum of the head with paired markings arranged symmetrically, venter cream heavily speckled with brown, prelacunal scale discrete in contact with second supralabial, three to five prefoveals, subfoveal single usually present, postfoveals absent to two, canthals two, seven intersupraoculars, one or two suboculars, two or three postoculars, seven or eight supralabials, nine to eleven infralabials, 26–27 interrictals, 23–25 middorsal scales, 172 ventrals in the female and 169–173 in males, 45 subcaudals in the female and 50 in males. We performed separate and combined phylogenetic analyses based on morphology and five mitochondrial genes and recovered the new species as a member of the Bothrops neuwiedi species group. All lineages of this clade inhabit the South American dry diagonal. This novel species of pitviper increases the known diversity of the genus Bothrops and adds to the number of described taxa from the unique and scarcely known ecosystem of Pampas del Heath.

 

References

  1. Araújo, D.P. (2015) Biogeografia Histórica das Jararacas do grupo Bothrops alternatus (Serpentes, Viperidae). MSc. Dissertation, Universidade Estadual Paulista Júlio de Mesquita Filho, Rio Claro, 54 pp.

    Barbo, F.E., Grazziotin, F.G., Sazima, I., Martins, M. & Sawaya, R. (2012) A new and threatened insular species of lancehead from Southeastern Brazil. Herpetologica, 68, 418–429.

    https://doi.org/10.1655/HERPETOLOGICA-D-12-00059.1

    Barbo, F.E., Gasparini, J.L., Almeida, A.P., Zaher, H., Grazziotin, F., Gusmão, R.B., Ferrarini, J.M.G. & Sawaya, R.J. (2016) Another new and threatened species of lancehead genus Bothrops (Serpentes, Viperidae) from Ilha dos Franceses, Southeastern Brazil. Zootaxa, 4097 (4), 511–529.

    https://doi.org/10.11646/zootaxa.4097.4.4

    Barros, V.A., Rojas, C.A. & Almeida-Santos, S.M. (2014) Is rainfall seasonality important for reproductive strategies in viviparous Neotropical pit vipers? A case study with Bothrops leucurus from the Brazilian Atlantic Forest. Herpetological Journal, 24 (2), 69–77.

    Cadle, J., Icochea, J., Zúñiga, J.P., Portilla, A. & Rivera, C. (2002) La Herpetofauna encontrada en el Refugio Juliaca y en el Puesto de Vigilancia Enahuipa del Santuario Nacional Pampas del Heath. In: Montambault, J.R. (Ed.), Informes de las Evaluaciones Biológicas de Pampas del Heath, Perú, Alto Madidi, Bolivia, y Pando, Bolivia. Conservation International, Washington, D.C., pp. 52–57.

    Campbell, J.A. & Lamar, W.W. (2004) The Venomous Reptiles of the Western Hemisphere. Cornell University Press, Ithaca, 1032 pp.

    Carrasco, P.A., Mattoni, C.I., Leynaud, G.C. & Scrocchi, G.J. (2012) Morphology, phylogeny and taxonomy of Southamerican bothropoid pitvipers (Serpentes: Viperidae). Zoologica Scripta, 41, 109–124.

    https://doi.org/10.1111/j.1463-6409.2011.00511.x

    Carrasco, P.A., Venegas, P.J., Chaparro, J.C. & Scrocchi, G.J. (2016) Nomenclatural instability in the venomous snakes of the Bothrops complex: implications in toxinology and public health. Toxicon, 119, 122–128.

    https://doi.org/10.1016/j.toxicon.2016.05.014

    Colli, G.R., Bastos, R.P. & Araújo, A.F.B. (2002) The character and dynamics of the Cerrado Herpetofauna. In: Oliveira, P.S. & Marquis, R.J. (Eds.), The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York, pp. 223–241.

    https://doi.org/10.7312/oliv12042

    Fenker, J., Tedeschi, L.G., Pyron, R.A. & de C. Nogueira, C. (2014) Phylogenetic diversity, habitat loss and conservation in South American pitvipers (Crotalinae: Bothrops and Bothrocophias). Diversity and Distributions, 2014, 1–12.

    https://doi.org/10.1111/ddi.12217

    Ferrarezzi, H. & Freire, E.M.X. (2001) New species of Bothrops Wagler, 1824 from the Atlantic forest of northeastern Brazil (Serpentes, Viperidae, Crotalinae). Boletim do Museu Nacional, Nova Série, Zoologia, 440, 1–10.

    Giraudo, A.R. (2001). Serpientes de la Selva Paranaense y del Chaco Húmedo. L.O.L.A., Buenos Aires, 285 pp.

    Goloboff, P.A. (1993) Estimating character weights during tree search. Cladistics, 9, 83–91.

    Goloboff, P.A., Mattoni, C.I. & Quinteros, S. (2006) Continuous characters analyzed as such. Cladistics, 22, 589–601.

    https://doi.org/10.1111/j.1096-0031.2006.00122.x

    Goloboff, P.A., Carpenter, J.M., Arias, J.S. & Miranda Esquivel, D.R. (2008) Weighting against homoplasy improves phylogenetic analysis of morphological data sets. Cladistics, 24, 1–16.

    https://doi.org/10.1111/j.1096-0031.2008.00209.x

    Goloboff, P.A. & Catalano, S.A. (2016) TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics, 32 (3), 221–238.

    https://doi.org/10.1111/cla.12160

    Graham, G.L., Graves, G.R., Schulenberg, T.S. & O`Neill, J.P. (1980) Seventeen bird species new to Peru from the Pampas del Heath. The Auk, 97, 366–370. Available from: https://sora.unm.edu/sites/default/files/journals/auk/v097n02/p0366-p0370.pdf (accessed 21 October 2018)

    Grazziotin, F.G., Zaher, H., Murphy, R.W., Scrocchi, G.J., Benavides, M.A., Zhang, Y.P. & Bonatto, S.L. (2012) Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): a reappraisal. Cladistics, 28 (5), 437–459.

    https://doi.org/10.1111/j.1096-0031.2012.00393.x

    Guedes, T.B., Sawaya, R.J. & Nogueira, C.C. (2014) Biogeography, vicariance and conservation of snakes of the neglected and endangered Caatinga region, north-eastern Brazil. Journal of Biogeography, 41, 919–931.

    https://doi.org/10.1111/jbi.12272

    Guedes, T.B., Sawaya, R.J., Zizka, A., Laffan, S., Faurby, S., Pyron, R.A., Bérnils, R.S., Jansen, M., Passos, P., Prudente, A.L.C., Cisneros-Heredia, D.F., Braz, H.B., de C. Nogueira, C. & Antonelli, A. (2018) Patterns, biases and prospects in the distribution and diversity of Neotropical snakes. Global Ecology and Biogeography, 2018, 27, 14–21.

    https://doi.org/10.1111/geb.12679

    Guerra-Duarte, C., Lopes-Peixoto, J., Fonseca-de-Souza, B.R., Stransky, S., Oliveira, D., Schneider, F.S., Lopes-de-Souza, L., Bonilla, C., Silva, W., Tintaya, B., Yarlequé, A. & Chávez-Olórtegui, C. (2015) Partial in vitro analysis of toxic and antigenic activities of eleven Peruvian pitviper snake venoms. Toxicon, 108, 84–96.

    https://doi.org/10.1016/j.toxicon.2015.09.007

    Hartmann, M.T., Marques, O.A. & Almeida-Santos, S.M. (2004) Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae). Amphibia-Reptilia, 25 (1), 77–85.

    https://doi.org/10.1163/156853804322992850

    Harvey, M.B. (1994) A new montane pitviper (Viperidae: Bothrops) from Cochabamba, Bolivia. Proceedings of the Biological Society of Washington, 107, 60–66. Available from http://biostor.org/reference/81222 (accessed 21 October 2018)

    Hillis, D.M., Mable, B.K. & Moritz, C. (1996). Applications of molecular systematics. In: Hillis, D.M., Moritz, C. & Mable, B.K. (Eds.), Molecular Systematics, 2nd ed. Sinauer Associates, Sunderland, pp. 515–544.

    Hoffmann, R.K., Ponce del Prado, C.F. & Otte, K.C. (1976) Registro de dos nuevas especies de mamíferos para el Perú, Odocoileus dichotoraus (Illiger–1811) y Chrysocyon brachyurus (Illiger–1811), con notas sobre su hábitat. Revista Forestal del Perú, 6, 61–81.

    Katho, K., Misawa, K., Kuma, K.I. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.

    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., Meintjes, P. & Drummond, A. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34 (3), 772–773.

    https://doi.org/10.1093/molbev/msw260

    Larrea-Alcázar, D.M., López, R.P., Quintanilla, M. & Vargas, A. (2010) Gap analysis of two savanna-type ecoregions: a two-scale floristic approach applied to the Llanos de Moxos and Beni Cerrado, Bolivia. Biodiversity and Conservation, 19, 1769–1783.

    https://doi.org/10.1007/s10531-010-9802-4

    Luna, L., Emmons, L., Romo, M. & Cornejo Farfán, A. (2002) Mamíferos encontrados en el Santuario Nacional Pampas del Heath durante la expedición del RAP de 1996. In: Montambault, J.R. (Ed.), Informes de las evaluaciones biológicas de Pampas del Heath, Perú, Alto Madidi, Bolivia, y Pando, Bolivia. Conservation International, Washington, D.C., pp. 66–70.

    Machado, T., Silva, V.X. & Silva, M.J.J. (2014) Phylogenetic relationships within Bothrops neuwiedi group (Serpentes, Squamata): geographically highly-structured lineages, evidence of introgressive hybridization and Neogene/Quaternary diversification. Molecular Phylogenetics and Evolution, 71, 1–14.

    https://doi.org/10.1016/j.ympev.2013.10.003

    Monteiro, C., Montgomery, C.E., Spina, F., Sawaya, R.J. & Martins, M. (2006) Feeding, reproduction, and morphology of Bothrops mattogrossensis (Serpentes, Viperidae, Crotalinae) in the Brazilian Pantanal. Journal of Herpetology, 40 (3), 408–413.

    https://doi.org/10.1670/0022-1511(2006)40[408:FRAMOB]2.0.CO;2

    Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.

    https://doi.org/10.1038/35002501

    Nogueira, C., Colli, G.R. & Martins, M. (2009) Local richness and distribution of the lizard fauna in natural habitat mosaics of the Brazilian Cerrado. Austral Ecology, 34, 83–96.

    https://doi.org/10.1111/j.1442-9993.2008.01887.x

    Nogueira, C., Colli, G.R., Costa, G.C. & Machado, R.B. (2010) Diversidade de répteis Squamata e evolução do conhecimento faunístico no Cerrado. In: Diniz, I.R., Marinho-Filho, J., Machado, R.B. & Cavalcanti, R.B. (Eds.), Cerrado: Conhecimento Científico Quantitativo como Subsídio para Ações de Conservação. UnB, Brasília, pp. 333–375.

    Oliveira-Filho, A.T. & Ratter, J.A. (2002) Vegetation physiognomies and woody flora of the cerrado biome. In: Oliveira, P.S. & Marquis, R.J. (Eds.), The Cerrados of Brazil: Ecology and Natural History of a Neotropical Savanna. Columbia University Press, New York, pp. 91–120.

    https://doi.org/10.7312/oliv12042-005

    Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P. & Kassem, K.R. (2001) Terrestrial ecoregions of the world: a new map of life on earth. BioScience, 51 (11), 933–938.

    https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Pennington, R.T., Lewis, G. & Ratter, J. (2006) An overview of the plant diversity, biogeography and conservation of neotropical savannas and seasonally dry forests. In: Pennington, R.T., Lewis, G. & Ratter J. (Eds.), Neotropical Savannas and the Seasonally Dry Forests. Taylor and Francis Group, Boca Raton, 1–29 pp.

    Pesantes, O.S. (1989) Relacões entre Algumas Espécies do Gênero Bothrops pela Eletroforese do Plasma e Morfología do Hemipenis (Serpentes: Viperidae). MSc. Dissertation, Universidade Estadual Paulista Júlio de Mesquita Filho, Rio Claro, 85 pp.

    https://doi.org/10.1201/9781420004496.ch1

    Pesantes, O.S. (1994) A method for preparing the hemipenis of preserved snakes. Journal of Herpetolology, 28, 93–95.

    https://doi.org/10.2307/1564686

    Prado, D.E. & Gibbs, P.E. (1993) Patterns of species distributions in the dry seasonal forests of South America. Annals of the Missouri Botanical Garden, 80, 902–927.

    https://doi.org/10.2307/2399937

    Sabaj M.H. (2016) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Available from: http://www.asih.org/, American Society of Ichthyologists and Herpetologists, Washington, DC. (accessed 21 October 2018)

    Silva, V.X. (2004) The Bothrops neuwiedi complex. In: Campbell, J.A. & Lamar, W.W. (Eds.), The Venomous Reptiles of the Western Hemisphere. Cornell University Press, Ithaca, pp. 410–422.

    Silva, V.X. & Rodrigues, M.T. (2008) Taxonomic revision of the Bothrops neuwiedi complex (Serpentes, Viperidae) with description of a new species. Phyllomedusa, 7, 45–90.

    https://doi.org/10.11606/issn.2316-9079.v7i1p45-90

    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

    Stotz, D.S., Montambault, J.R., Pequeño, T., Valdes, A., Mack, A. & Quiroga, C. (2002) Evaluación de la avifauna de Pampas del Heath, Perú y Alto Madidi, Bolivia. In: Montambault, J.R. (Ed.), Informes de las Evaluaciones Biológicas de Pampas del Heath, Perú, Alto Madidi, Bolivia, y Pando, Bolivia. Conservation International, Washington, D.C., pp. 45–51.

    Uetz, P. & Hošek, J. (2017) The Reptile Database. Available from: http://www.reptile-database.org (accessed 21 October 2018)

    Vanzolini, P.E. (1963) Problemas faunísticos do Cerrado. In: Ferri, M.G. (Ed.), Simpósio Sôbre o Cerrado. University of São Paulo Press, São Paulo, pp. 307–320.

    Werneck, F.P. (2011) The diversification of eastern South American open vegetation biomes: Historical biogeography and perspectives. Quaternary Science Reviews, 30, 1630–1648.

    https://doi.org/10.1016/j.quascirev.2011.03.009

    Werneck, F.P., Costa, G.C., Colli, G.R., Prado, D. & Sites Jr., J.W. (2011) Revisiting the historical distribution of seasonally dry tropical forests: new insights based on palaeodistribution modelling and palynological evidence. Global Ecology and Biogeography, 20, 272–288.

    https://doi.org/10.1111/j.1466-8238.2010.00596.x

    Werneck, F.P., Nogueira, C., Colli, G.R., Sites, J.W. & Costa, G.C. (2012) Climatic stability in the Brazilian Cerrado: implications for biogeographical connections of South American savannas, species richness and conservation in a biodiversity hotspot. Journal of Biogeography, 39 (9), 1695–1706.

    https://doi.org/10.1111/j.1365-2699.2012.02715.x

    Williams, R.S., Torres, E., Magan, J., Cruz, A. & Leite-Pitman, R. (2012) Confirmation of the continued presence of the maned wolf in Peru. Canid news. Available from: http://www.canids.org/canidnews/15/Maned_wolf_in_Peru.pdf (accessed 29 December 2017)

    Zaher, H. (1999) Hemipenial morphology of the South American Xenodontinae, 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: http://hdl.handle.net/2246/1646 (accessed 21 October 2018)