Abstract
The northernmost Peruvian Andes, a unique biogeographic region characterized by the confluence of multiple distinct ecosystems (i.e. Amazon basin, Pacific rainforest, the Sechura Desert, the northern and central Andes), is the southernmost geographic range limit of the South American shrews representing the genus Cryptotis. In the northernmost Peruvian Andes, two poorly known species have traditionally been reported (C. peruviensis and C. equatoris). Our study, based on molecular and morphologic traits, confirms the presence of C. peruviensis but also the occurrence of C. montivaga, based on specimens erroneously assigned to C. equatoris. Moreover, a new species of Cryptotis from the páramo and montane forests of the Tabaconas Namballe National Sanctuary near the Ecuadorian border is also described. It is a member of the thomasi group and is distinguished from other South American shrews by a unique set of morphological characters, including large body size, comparatively short tail, simple ectoloph of M3, and large PM4 post protocrista.
References
Albuja, V.L. & Patterson, B.D. (1996) A new species of northern shrew-opossum (Paucituberculata: Caenolestidae) from the Cordillera del Cóndor, Ecuador. Journal of Mammalogy, 77, 41–53.
https://doi.org/10.2307/1382707
Baker, R.J. & Bradley, R.D. (2006) Speciation in mammals and the genetic species concept. Journal of Mammalogy, 87, 643–662.
https://doi.org/10.1644/06-MAMM-F-038R2.1
Barnett, A.A. (1992) Notes on the ecology of Cryptotis montivaga Anthony, 1921 (Insectivora, Soricidae), a high-altitude shrew from Ecuador. Mammalia, 56, 587−592.
https://doi.org/10.1515/mamm.1992.56.4.587
Bilton, D.T. & Jaarola, M. (1996) Isolation and purification of vertebrate DNAs. In: Clapp, J.P. & Kimmel, A.R. (Eds.), PCR and other Nucleic Acid Methods, Methods in Molecular Biology.Humana Press Inc., Totowa, pp. 25−37.
https://doi.org/10.1385/0-89603-323-6:25
Brack, A. (1986) Ecología de un país complejo. In: Manfer-Mejía, B. (Ed.), Gran geografía del Perú. Madrid, pp. 175−319.
Bradley, R.D. & Baker, R.J. (2001) A test of the Genetic Species Concept: cytochrome-b sequences and mammals. Journal of Mammalogy, 82, 960−973.
Chapman, F.M. (1926) The Distribution of Bird Life in Ecuador. Bulletin of the America Museum of Natural History, 55, 1–784.
Choate, J.R. (1970) Systematics and Zoogeography of Middle American Shrews of the Genus Cryptotis. University of Kansas Publications, Museum of Natural History, 19, 195–317.
https://doi.org/10.5962/bhl.part.15450
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
https://doi.org/10.2307/2408678
Garzón-Orduña, I.J., Benetti-Longhini, J.E. & Brower, A.V.Z. (2014) Timing the diversification of the Amazonian biota: butterfly divergences are consistent with Pleistocene refugia. Journal of Biogeography, 41, 1631–1638.
https://doi.org/10.1111/jbi.12330
Hammer, D.A., Harper, T. & Ryan, P.D. (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontología Electrónica, 4 (1), 1−9.
He, K., Woodman, N., Boaglio, S., Roberts, M., Supekar, S. & Maldonado, J.E. (2015) Molecular Phylogeny Supports Repeated Adaptation to Burrowing within Small-Eared Shrews Genus of Cryptotis (Eulipotyphla, Soricidae). Plos One, 10 (10), 1−13.
https://doi.org/10.1371/journal.pone.0140280
Hutterer, R. (1993) Order Insectivora. In: Wilson, D.E. & Reeder, D.E. (Eds.), Mammal species of the World, a taxonomic and geographic reference. Smithsonian Institution Press, Washington, pp. 69−130.
Irwin, D.M., Kocher, T.D. & Wilson, A.C. (1991) Evolution of the cytochrome b gene of mammals. Journal of Molecular and Evolution, 32, 128−144.
https://doi.org/10.1007/BF02515385
Haffer, J. (1969) Speciation in Amazonian Forest Birds. Science, 165 (3889), 131−137.
https://doi.org/10.1126/science.165.3889.131
Haffer, J. (2008) Hypotheses to explain the origin of species in Amazonia. Brazilian Journal of Biology, 68, 917–947.
Hoorn, C., Wesselingh, F.P., ter Steege, H., Bermude, M.A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C.L., Figueiredo, J.P., Jaramillo, C., Riff, D., Negri, F.R., Hooghiemstra, H., Lundberg, J., Stadler, T., Särkinen, T. & Antonelli, A. (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330, 927–931.
https://doi.org/10.1126/science.1194585
Jansa, S.A. & Voss, R.S. (2000) Phylogenetic studies on Didelphid marsupials I introduction and preliminary results from nuclear IRBP gene sequences. Journal of Mammalian Evolution, 7, 43−77.
https://doi.org/10.1023%2FA%3A1009465716811
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular and Evolution, 16, 111−120.
https://doi.org/10.1007/BF01731581
Mena-Vásconez, P. & Hofstede, R. (2006) Los Páramos ecuatorianos. In: Moraes, M., Øllgaard, B., Kvist, L.P., Borchsenius, F. & Balslev, H. (Eds.), Botánica Económica de los Andes Centrales. Universidad Mayor de San Andrés, La Paz, pp. 91−109.
Merriam, C.H. (1897) Descriptions of five new shrews from Mexico, Guatemala, and Colombia. Proceedings of the Biological Society of Washington, 11, 227–230.
Moreno, C.P.A. & Albuja, V.L. (2014) Una nueva especie de musaraña del género Cryptotis Pomel 1848 (Mammalia: Soricomorpha: Soricidae) de Ecuador y estatus taxonómico de Cryptotis equatoris Thomas (1912). Papéis Avulsos de Zoologia, 54, 403–418.
https://doi.org/10.1590/0031-1049.2014.54.28
Pacheco, V.R., Cadenillas, R., Salas, E., Tello, C. & Zeballos, H. (2009) Diversidad y Endemismo de los Mamíferos del Perú. Revista Peruana de Biología, 16, 5−32.
https://doi.org/10.15381/rpb.v16i1.111
Quiroga-Carmona, M. (2013) Descripción de una nueva especie de musaraña del género Cryptotis Pomel 1848 (Mammalia: Soricomorpha: Soricidae) de la Serranía del Litoral en el norte de Venezuela. Mastozoología Neotropical, 20, 1–15.
Quiroga-Carmona, M. & DoNascimento, C. (2016) A new species of small-eared shrew of the genus Cryptotis Pomel, 1848 (Mammalia, Eulipotyphla, Soricidae) from the easternmost mountains of the Venezuelan Andes. Mammalian Biology, 81, 494–505.
https://doi.org/10.1016/j.mambio.2016.04.002
Quiroga-Carmona, M. & Molinari, J. (2012) Description of a new shrew of the genus Cryptotis (Mammalia: Soricomorpha: Soricidae) from the Sierra de Aroa, an isolated mountain range in northwestern Venezuela, with remarks on biogeography and conservation. Zootaxa, 3441, 1–20.
Quiroga-Carmona, M. & Woodman, N. (2015) A new species of Cryptotis (Mammalia, Eulipotyphla, Soricidae) from the Sierra de Perijá, Venezuelan-Colombian Andes. Journal of Mammalogy, 96 (4), 800–809.
https://doi.org/10.1093/jmammal/gyv085
Reed, C.A. (1951) Locomotion and Appendicular Anatomy in Three Soricoid Insectivores. American Midland Naturalist, 45 (3), 513–671.
https://doi.org/10.2307/2421996
Rojas, D., Warsi, O.M. & Dávalos, L.M. (2016) Bats (Chiroptera: Noctilionoidea) Challenge a Recent Origin of Extant Neotropical Diversity. Systematic Biology, 65 (3), 432–448.
https://doi.org/10.1093/sysbio/syw011
Rull, V. (2008) Speciation timing and Neotropical biodiversity: the Tertiary-Quaternary debate in the light of molecular phylogenetic evidence. Molecular Ecology, 17, 2722–2729.
https://doi.org/10.1111/j.1365-294X.2008.03789.x
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725−2729.
https://doi.org/10.1093/molbev/mst197
Tate, G.H.H. (1932) The distribution of South American shrews. Journal of Mammalogy, 18, 223−228.
https://doi.org/10.2307/1373997
Thomas, O. (1912) Three small mammals from South America. Annals and Magazine of Natural History, 8 (9), 408−410.
https://doi.org/10.1080/00222931208693149
Tirira, D. (2007) Mamíferos del Ecuador, Guía de Campo. Ediciones Murciélago Blanco, Quito, 576 pp.
Vivar, E., Pacheco, V. & Valqui, M. (1997) A New Species of Cryptotis (Insectivora: Soricidae) from Northern Peru. American Museum Novitates, 3202, 1−15.
Weksler, M. (2003) Phylogeny of Neotropical Oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Molecular Phylogenetics and Evolution, 29, 331–349.
https://doi.org/10.1016/S1055-7903(03)00132-5
Woodman, N. (1996) Taxonomic status of the enigmatic Cryptotis avia (Mammalia: Insectivora: Soricidae) with comments on the distribution of the Colombia small-eared shrew, Cryptotis colombiana. Proceedings of the Biological Society of Washington, 109 (3), 409–418.
Woodman, N. (2002) A new species of small-eared shrew from Colombia and Venezuela (Mammalia: Soricomorpha: Soricidae: genus Cryptotis). Proceedings of the Biological Society of Washington, 115 (2), 249–272.
Woodman, N. (2003) A new small shrew of the Cryptotis nigrescens-group from Colombia (Mammalia: Soricomorpha: Soricidae). Proceedings of the Biological Society of Washington, 116 (4), 853–872.
Woodman, N. (2010) Two new species of shrews (Soricidae) from the western highlands of Guatemala. Journal of Mammalogy, 91 (3), 566−579.
https://doi.org/10.1644/09-MAMM-A-346.1
Woodman, N. (2011) Patterns of morphological variation amongst semifossorial shrews in the highlands of Guatemala with the description of a new species (Mammalia, Soricomorpha, Soricidae). Zoological Journal of the Linnean Society, 163, 1267–1288.
https://doi.org/10.1111/j.1096-3642.2011.00754.x
Woodman, N. & Péfaur, J. (2008) Magnorder Epitheria. Order Soricomorpha Gregory, 1910. In: Gardner, A.L. (Ed.), Mammals of South America, vol. 1, Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, pp. 177–187.
Woodman, N. & Stephens, R.B. (2010) At the foot of the shrew: manus morphology distinguishes closely-related Cryptotis goodwini and Cryptotis griseoventris (Mammalia: Soricidae) in Central America. Biological Journal of the Linnean Society, 99, 118−134.
https://doi.org/10.1111/j.1095-8312.2009.01343.x
Woodman, N. & Timm, R.M. (1992) A new species of small-eared shrew, Genus Cryptotis (Insectivora: Soricidae) from Honduras. Proceedings of the Biological Society of Washington, 105 (1), 1−12.
Woodman, N. & Timm, R.M. (1993) Intraspecific and interspecific variation in the Cryptotis nigrescens species complex of small-eared shrews (Insectivora Soricidae), with the description of a new species from Colombia. Fieldiana Zoology, 74, 1–30.
Woodman, N. & Timm, R.M. (1999) Geographic variation and evolutionary relationships among broad-clawed shrews of the Cryptotis goldmani-group (Mammalia Insectivora: Soricidae). Fieldiana Zoology, 91, 1–35.
Woodman, N. & Timm, R.M. (2000) Taxonomy and evolutionary relationships of Phillips’ small-eared shrew, Cryptotis phillipsii (Schaldach, 1966), from Oaxaca, Mexico (Mammalia: Insectivora: Soricidae). Proceedings of the Biological Society of Washington, 113 (2), 339–355.
Vuilleumier, F. (1984) Zoogeography of Andean Birds: Two major barriers; and speciation and taxonomy of the Diglossa carbonaria superspecies. National Geographic Society Research Reports, 16, 713–731.