Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-06-01
Page range: 151-188
Abstract views: 1240
PDF downloaded: 691

Systematics and biogeography of Anoura cultrata (Mammalia, Chiroptera, Phyllostomidae): a morphometric, niche modeling, and genetic perspective, with a taxonomic reappraisal of the genus

Departamento de Biología; Facultad de Ciencias; Universidad de Los Andes; Mérida; Venezuela
Programa de Pos-Graduação em Biodiversidade Animal; Centro de Ciências Naturais e Exatas; Universidade Federal de Santa Maria; Rio Grande do Sul; Brazil
Department of Natural History; Royal Ontario Museum; Toronto; Ontario; Canada
Mammalia body size DNA barcoding ecogeographic barriers geographic variation past distributions subspecies tropical mountains

Abstract

The nectar-feeding bats of the genus Anoura are widely distributed in the Neotropics, but are most speciose in the Andes. Anoura cultrata is a rare mid-elevation bat occurring in South and Central America. It is thought to be one of the few bat species exemplifying a latitudinal cline in body size. We address three systematic and biogeographic questions: 1) is the geographic variation in A. cultrata continuous, as argued to justify its current monotypic status? 2) do ecogeographic barriers to dispersal affect such variation? and 3) how do the genetic divergence and biogeography of the species compare to those of other members of the genus? To answer these questions, we used morphometric analyses, ecological niche modeling, and DNA barcoding. We divided the samples of A. cultrata into six geographic groups, delimited by topographic depressions separating mountain systems. We did not find significant correlations between body size and the geographic coordinates within five groups. Therefore, we conclude that ecogeographic barriers to dispersal between the regions occupied by such groups influenced morphometric variation in A. cultrata, and that despite its general north to south reduction in body size, the species does not show continuous clinal variation. A recent phylogenetic study of the genus Anoura concluded that it contains seven valid species. Our DNA barcoding analysis and morphological examination indicated that at least 10 species should be recognized, including A. peruana distinct from A. geoffroyi, and A. aequatoris and A. luismanueli distinct from A. caudifer. Moreover, we show that Central and South American populations of A. cultrata differ from each other at least at the subspecific level, thus we respectively refer to them as A. cultrata cultrata and as A. c. brevirostrum. Similarly, we refer to Central American and Mexican populations of ‘A. geoffroyi’ as A. peruana lasiopyga, and to their South American counterparts as A. p. peruana. The range of the latter subspecies reaches northeastern Venezuela. The Andes from southern Colombia to northern Peru appear to be the ancestral range of the genus.

 

References

  1. Anderson, R.P. (2012) Harnessing the world’s biodiversity data: promise and peril in ecological niche modeling of species distributions. Annals of the New York Academy of Sciences, 1260, 66–80. https://doi.org/10.1111/j.1749-6632.2011.06440.x
  2. Anderson, R.P. (2013) A framework for using niche models to estimate impacts of climate change on species distributions. Annals of the New York Academy of Sciences, 1297, 8–28. https://doi.org/10.1111/nyas.12264
  3. Anderson, R.P. & Gutiérrez, E.E. (2009) Taxonomy, distribution, and natural history of the genus Heteromys (Rodentia: Heteromyidae) in central and eastern Venezuela, with the description of a new species from the Cordillera de la Costa. Bulletin of the American Museum of Natural History, 331, 33–93. https://doi.org/10.1206/582-2.1
  4. Anderson, R.P., Gutiérrez, E.E., Ochoa-G, J., García, F.J. & Aguilera, M. (2012) Faunal nestedness and species–area relationship for small non-volant mammals in “sky islands” of northern Venezuela. Studies on Neotropical Fauna and Environment, 47, 157–170. https://doi.org/10.1080/01650521.2012.745295
  5. Anderson, R.P. & Raza, A. (2010) The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. Journal of Biogeography, 37, 1378–1393. https://doi.org/10.1111/j.1365-2699.2010.02290.x
  6. Anthelme, F., Jacobsen, D., Macek, P., Meneses, R.I., Moret, P., Beck, S. & Dangles, O. (2014) Biodiversity patterns and continental insularity in the tropical High Andes. Arctic, Antarctic, and Alpine Research, 46, 811–828. https://doi.org/10.1657/1938-4246-46.4.811
  7. Arroyo-Cabrales, J. & Gardner, A.L (2003) The type specimen of Anoura geoffroyi lasiopyga (Chiroptera: Phyllostomidae). Proceedings of the Biological Society of Washington, 116, 737–741.
  8. Ashton, K.G., Tracy, M.C. & de Queiroz, A. (2000) Is Bergmann’s rule valid for mammals? American Naturalist, 156, 390–415. https://doi.org/10.1086/303400
  9. Avendaño, J.E., Stiles, F.G. & Cadena, C.D. (2013) A new subspecies of Common Bush-Tanager (Chlorospingus flavopectus, Emberizidae) from the east slope of the Andes of Colombia. Ornitología Colombiana, 13, 45–58.
  10. Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher, S.P., Peterson, A.T., Soberón, J. & Villalobos, F. (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling, 222, 1810–1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011
  11. Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B, 57, 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
  12. Bogdanowicz, W. (1990) Geographic variation and taxonomy of Daubenton's bat, Myotis daubentoni in Europe. Journal of Mammalogy, 71, 205–218. https://doi.org/10.2307/1382169
  13. Bonifaz, E., Mena, J.L. & Oporto, R. (2020) Moscas de murciélagos en algunas localidades de la costa peruana. Revista Peruana de Biología, 27, 241–250. https://doi.org/10.15381/rpb.v27i2.17881
  14. Cabrera, A. (1957) Catálogo de los mamíferos de América del Sur. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia, 4, 1–307.
  15. Cadena, C.D., Pedraza, C.A. & Brumfield, R.T. (2016) Climate, habitat associations and the potential distributions of Neotropical birds: Implications for diversification across the Andes. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 40, 275–287. https://doi.org/10.18257/raccefyn.280
  16. Cadle, J.E. (1991) Systematics of the lizards of the genus Stenocercus (Iguania: Tropiduridae) from northern Peru: new species and comments on the relationships and distribution patterns. Proceedings of the Academy of Natural Sciences of Philadelphia, 143, 1–96.
  17. Calderón-Acevedo, C.A., Bagley. J.C. & Muchhala, N. (2022) Genome-wide ultraconserved elements resolve phylogenetic relationships and biogeographic history among Neotropical leaf-nosed bats in the genus Anoura (Phyllostomidae). Molecular Phylogenetics and Evolution, 167, 107356. https://doi.org/10.1016/j.ympev.2021.107356
  18. Calderón-Acevedo, C.A. & Muchhala, N. (2018) Identification and diagnosis of Anoura fistulata with remarks on its presumed presence in Bolivia. Journal of Mammalogy, 99, 131–137. https://doi.org/10.1093/jmammal/gyx159
  19. Calderón-Acevedo, C.A., Rodríguez-Posada, M.E. & Muchhala, N. (2021) Morphology and genetics concur that Anoura carishina is a synonym of Anoura latidens (Chiroptera, Glossophaginae). Mammalia, 2021, 1–11. https://doi.org/10.1515/mammalia-2020-0183
  20. Carter, D.C., Pine, R.H. & Davis, W.B. (1966) Notes on Middle American bats. Southwestern Naturalist, 11, 488–499. https://doi.org/10.2307/3668862
  21. Chaves, M.E., Uieda, W., Bolochio, C.E., Souza, C.A. I., Braga, D.A., Ferreira, C.H., Firmo, C.L., Mariano, R.G.G.C., Oliveira, K.C.S., Santos, E.G. & Costa, F.M. (2012) Bats (Mammalia: Chiroptera) from Guarulhos, state of São Paulo, Brazil. Check List, 8, 1117–1121. https://doi.org/10.15560/8.6.1117
  22. Claps, G.L., Autino, A.G. & Barquez, R.M. (2005) Streblidae de murciélagos de Lima: dos citas nuevas para Perú. Revista de la Sociedad Entomológica Argentina, 64, 95–98.
  23. Clare, E.L., Lim, B.K., Engstrom, M.D., Eger, J.L. & Hebert, P.D.N. (2007) DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Molecular Ecology Notes, 7, 184–190. https://doi.org/10.1111/j.1471-8286.2006.01657.x
  24. Clare, E.L., Lim, B.K., Fenton, M.B. & Hebert, P.D.N. (2011) Neotropical bats: estimating species diversity with DNA barcodes. PLoS ONE, 6 (7), e22648. https://doi.org/10.1371/journal.pone.0022648
  25. Cleef, A.M. (1981) The vegetation of the páramos of the Colombian Cordillera Oriental. Dissertationes Botanicae, 61, 1–321.
  26. Dick, C.W. (2013) Review of the bat flies of Honduras, Central America (Diptera: Streblidae). Journal of Parasitology Research, 2013, 1–17. https://doi.org/10.1155/2013/437696
  27. Dick, C.W., Gettinger, D. & Gardner, S.L. (2007) Bolivian ectoparasites: A survey of bats (Mammalia Chiroptera). Comparative Parasitology, 74, 372–377. https://doi.org/10.1654/4264.1
  28. Díaz, M.M. & Barquez, R.M (2009) Primer registro de Micronycteris microtis (Phyllostomidae, Phyllostominae) para la Argentina. Chiroptera Neotropical, 15, 461–465.
  29. Duellman, W.E. (1979) The herpetofauna of the Andes: patterns of distribution, origin, differentiation, and present communities. In: Duellman, W.E. (Ed.), The South American herpetofauna: its origin, evolution, and dispersal, University of Kansas, Lawrence, pp. 371–459. https://doi.org/10.5962/bhl.title.3207
  30. Elith, J., Graham, C.H., Anderson, R.P., Dudík, M., Ferrier, S., Guisan, A., Hijmans, R.J., Huettmann, F., Leathwick, J.R., Lehmann, A., Li, J., Lohmann, L.G., Loiselle, B.A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J.McC., Peterson, A.T., Phillips, S.J., Richardson K., Scachetti-Pereira, R., Schapire, R.E., Soberón, J., Williams, S., Wisz, M.S. & Zimmermann, N.E. (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography, 29, 129–151. https://doi.org/10.1111/j.2006.0906-7590.04596.x
  31. Faircloth, B.C., J.E. McCormack, N.G. Crawford, M.G. Harvey, R.T. Brumfield, & Glenn, T.C. (2012) Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Systematic Biology, 61, 717–726. https://doi.org/10.1093/sysbio/sys004
  32. Frank, R., Münster, J., Schulze, J., Liston, A. & Klimpel, S. (2014) Macroparasites of Microchiroptera: bat ectoparasites of Central and South America. In: Klimpel, S. & Mehlhorn, H. (Eds.), Bats (Chiroptera) as Vectors of Diseases and Parasites. Parasitology Research Monographs, 5, pp. 87–130. https://doi.org/10.1007/978-3-642-39333-4_5
  33. Galimberti, A., Sandionigi, A., Bruno, A., Bellati, A. & Casiraghi, M. (2015) DNA barcoding in mammals: what's new and where next? Hystrix, 26, 13–24. https://doi.org/10.4404/hystrix-26.1-11347
  34. García, F.J., Delgado-Jaramillo, M.I., Machado, M. & Aular, L. (2016) Mamíferos de la Sierra de Aroa, estado Yaracuy, Venezuela: listado taxonómico y la importancia de su conservación. Memoria de la Fundación La Salle de Ciencias Naturales, 73, 17–34.
  35. Gardner, A.L., LaVal, R.K. & Wilson, D.E. (1970) The distributional status of some Costa Rican bats. Journal of Mammalogy, 51, 712–729. https://doi.org/10.2307/1378297
  36. Garg, K.M. & Chattopadhyay, B. (2021) Gene flow in volant vertebrates: species biology, ecology and climate change. Journal of the Indian Institute of Science, 101, 165–176. https://doi.org/10.1007/s41745-021-00239-z
  37. Gene Codes Corporation (2007) Sequencher version 4.8. Gene Codes Corporation. Ann Arbor, Michigan.
  38. Genoways, H.H., Phillips, C.J. & Baker, R.J. (1998) Bats of the Antillean island of Grenada: a new zoogeographic perspective. Occasional Papers, The Museum, Texas Tech University, 177, 1–27. https://doi.org/10.5962/bhl.title.143306
  39. Graham, G.L. (1983) Changes in bat species diversity along an elevational gradient up the Peruvian Andes. Journal of Mammalogy, 64, 559–571. https://doi.org/10.2307/1380511
  40. Griffiths, T.A. & Gardner, A.L. (2008) Subfamily Glossophaginae Bonaparte, 1845. In: Gardner, A.L. (Ed.), Mammals of South America, Vol 1. Marsupials, xenarthrans, shrews, and bats, University of Chicago Press, Chicago, pp. 224–244.
  41. Gutiérrez, E.E. (2016) Ecological niche modelling requires real presence data and appropriate study regions: a comment on Medone et al. (2015). Philosophical Transactions of the Royal Society B, 371 (1699), 20160027. https://doi.org/10.1098/rstb.2016.0027
  42. Gutiérrez, E.E., Boria, R.A. & Anderson, R.P. (2014) Can biotic interactions cause allopatry? Niche models, competition, and distributions of South American mouse opossums. Ecography, 37, 741–753. https://doi.org/10.1111/ecog.00620
  43. Gutiérrez, E.E., Madonado, J.E., Radosavljevic, A., Molinari, J., Patterson, B.D., Martínez-C., J.M., Rutter, A.R., Hawkins, M.T.R., Garcia, F.J. & Helgen, K.M. (2015) The taxonomic status of Mazama bricenii and the significance of the Táchira Depression for mammalian endemism in the Cordillera de Mérida, Venezuela. PLoS ONE, 10 (6), e0129113. https://doi.org/10.1371/journal.pone.0129113
  44. Gutiérrez, E.E. & Molinari, J. (2008) Morphometrics and taxonomy of bats of the genus Pteronotus (subgenus Phyllodia) in Venezuela. Journal of Mammalogy, 89, 292–305. https://doi.org/10.1644/06-MAMM-A-452R.1
  45. Haffer, J. (1970) Geologic-climatic history and zoogeographic significance of the Urabá region in northwestern Colombia. Caldasia, 10, 603–636.
  46. Hammer, Ø. (2021) PAST, Paleontological Statistics, Version 4.07, Reference manual. University of Oslo, Oslo, 304 pp.
  47. Handley, C.O., Jr. (1976) Mammals of the Smithsonian Venezuelan Project. Brigham Young University Science Bulletin, Biological Series, 20 (5), 1–89. https://doi.org/10.5962/bhl.part.5667
  48. Handley, C.O., Jr. (1984) New species of mammals from northern South America: a long-tongued bat, genus Anoura Gray. Proceedings of the Biological Society of Washington, 97, 513–521.
  49. Hazzia, N.A., Moreno, J.S., Ortiz-Movliav, C. & Palacio, R.D. (2018) Biogeographic regions and events of isolation and diversification of the endemic biota of the tropical Andes. Proceedings of the National Academy of Sciences, 115, 7985–7990. https://doi.org/10.1073/pnas.1803908115
  50. Hedrick, B.P. (2021) Inter- and intraspecific variation in the Artibeus species complex demonstrates size and shape partitioning among species. PeerJ, 9, e11777. https://doi.org/10.7717/peerj.11777
  51. Hershkovitz, P. (1969) The recent mammals of the Neotropical region: a zoogeographic and ecological review. Quarterly Review of Biology, 44, 1–70. https://doi.org/10.1086/405975
  52. Herzog, S.K. & Kattan, G.H. (2011) Patterns of diversity and endemism in the birds of the tropical Andes. In: Herzog, S.K., Martínez, R., Jørgensen, P.M. & Tiessen, H. (Eds.), Climate change and biodiversity in the tropical Andes, Inter-American Institute for Global Change Research (IAI) and Scientific Committee on Problems of the Environment (SCOPE), Paris, pp. 245–259.
  53. Hijmans, R.J. (2017) raster: Geographic data analysis and modeling. R package version 2.6-7. Available from: https://CRAN.R-project.org/package=raster (accessed 10 January 2018)
  54. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978. https://doi.org/10.1002/joc.1276
  55. Husson, A.M. (1962) The bats of Suriname. Zoologische Verhandelingen, 58, 1–282.
  56. Jarrín-V.P. & Coello, D. (2012) Quantification of morphological variation within species of Anoura from Ecuador, with an emphasis on A. fistulata (Chiroptera: Phyllostomidae). Acta Chiropterologica, 14, 317–333. https://doi.org/10.3161/150811012X661648
  57. Jarrín-V.P. & Kunz, T.H. (2008) Taxonomic history of the genus Anoura (Chiroptera: Phyllostomidae) with insights into the challenges of morphological species delimitation. Acta Chiropterologica, 10, 257–269. https://doi.org/10.3161/150811008X414836
  58. Jiménez-Valverde, A. & Lobo, J.M. (2007) Threshold criteria for conversion of probability of species presence to either-or presence-absence. Acta Oecologica, 31, 361–369. https://doi.org/10.1016/j.actao.2007.02.001
  59. Killeen, T.J., Douglas, M., Consiglio, T., Jørgensen, P.M. & Mejia, J. (2007). Dry spots and wet spots in the Andean hotspot. Journal of Biogeography, 34, 1357–1373. https://doi.org/10.1111/j.1365-2699.2006.01682.x
  60. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054
  61. Lew, D. & Lim, B.K. (2019) Mammals. In: Rull, V., Vegas-Vilarrúbia, T., Huber, O. & Señaris, C. (Eds.), Biodiversity of Pantepui: the pristine “lost world” of the Neotropical Guiana Highlands. Academic Press, London, pp. 333–371. https://doi.org/10.1016/B978-0-12-815591-2.00014-8
  62. Lim, B.K. (2017) Review of genetic diversification of bats in the Caribbean and biogeographic relationships to Neotropical species based on DNA barcodes. Genome, 60, 65–73. https://doi.org/10.1139/gen-2015-0204
  63. Lim, B.K. & Tavares, V.C. (2012) Review of species richness and biogeography of bats (Chiroptera) from the Guiana subregion of South America with comments on conservation. Ecotropica, 18, 105–118.
  64. Liu, C., Berry, P.M., Dawson, T.P. & Pearson, R.G. (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography, 3, 385–393. https://doi.org/10.1111/j.0906-7590.2005.03957.x
  65. Liu, C., White, M. & Newell, G. (2013) Selecting thresholds for the prediction of species occurrence with presence‐only data. Journal of Biogeography, 40, 778–789. https://doi.org/10.1111/jbi.12058
  66. Manel, S., Williams, H.C. & Ormerod, S.J. (2001) Evaluating presences-absence models in ecology: the need to account for prevalence. Journal of Applied Ecology, 38, 921–931. https://doi.org/10.1046/j.1365-2664.2001.00647.x
  67. Mantilla-Meluk, H. & Baker, R.J. (2006) Systematics of small Anoura (Chiroptera: Phyllostomidae) from Colombia, with description of a new species. Occasional Papers, Museum of Texas Tech University, 261, 1–18. https://doi.org/10.5962/bhl.title.156897
  68. Mantilla-Meluk, H. & Baker, R.J. (2010) New species of Anoura (Chiroptera: Phyllostomidae) from Colombia, with systematic remarks and notes on the distribution of the A. geoffroyi complex. Occasional Papers, Museum of Texas Tech University, 292, 1–19.
  69. Mantilla-Meluk, H., Jiménez-Ortega, A.M. & Baker, R.J. (2009) Range extension of Anoura aequatoris and notes on distributional limits of small Anoura in Colombia. Investigación, Biodiversidad y Desarrollo, 28, 107–112.
  70. Meiri, S. & Dayan, T. (2003) On the validity of Bergmann’s rule. Journal of Biogeography, 30, 331–351. https://doi.org/10.1046/j.1365-2699.2003.00837.x
  71. Mendes, P., Vieira, T.B., Oprea, M., Brito, D. & Ditchfield, A.D. (2011) Roost use by bats in Espírito Santo, Brazil: comparison of a protected area, a rural landscape, and an urban landscape. Cuadernos de Investigación UNED, 3, 195–201. https://doi.org/10.22458/urj.v3i2.148
  72. Miller, A.H. (1952) Supplementary data on the tropical avifauna of the arid upper Magdalena Valley of Colombia. Auk, 69, 450–457. https://doi.org/10.2307/4081026
  73. Molina, C.A. (2005) Patrones de variación morfométrica de cuatro especies del género Anoura (Chiroptera: Phyllostomidae). Tesis de Licenciatura, Pontificia Universidad Católica del Ecuador, Quito, Ecuador.
  74. Molinari, J. (1994) A new species of Anoura (Mammalia Chiroptera Phyllostomidae) from the Andes of northern South America. Tropical Zoology, 7, 73–86. https://doi.org/10.1080/03946975.1994.10539242
  75. Molinari, J. (2023a) A bare-bones scheme to choose between the species, subspecies, and ‘evolutionarily significant unit’ categories in taxonomy and conservation. Journal for Nature Conservation, 72, 126335. https://doi.org/10.1016/j.jnc.2023.126335
  76. Molinari, J. (2023b) A global assessment of the ‘island rule’ in bats based on functionally distinct measures of body size. Journal of Biogeography, https://doi.org/10.1111/jbi.14624
  77. Molinari J., Bustos X.E., Burneo, S.F., Camacho, M.A., Moreno, S.A. & Fermín, G. (2017) A new polytypic species of yellow-shouldered bats, genus Sturnira (Mammalia: Chiroptera: Phyllostomidae), from the Andean and coastal mountain systems of Venezuela and Colombia. Zootaxa, 4243, 075–096. https://doi.org/10.11646/zootaxa.4243.1.3
  78. Muscarella, R., Galante, P.J., Soley‐Guardia, M., Boria, R.A., Kass, J.M., Uriarte, M. & Anderson, R.P. (2014) ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution, 5, 1198–1205. https://doi.org/10.1111/2041-210X.12261
  79. Nagorsen, D. & Tamsitt, J.R., Jr. (1981) Systematics of Anoura cultrata, A. brevirostrum, and A. werckleae. Journal of Mammalogy, 62, 82–100. https://doi.org/10.2307/1380480
  80. Nenzén, H.K. & Araújo, M.B. (2011) Choice of threshold alters projections of species range shifts under climate change. Ecological Modelling, 222, 3346–3354. https://doi.org/10.1016/j.ecolmodel.2011.07.011
  81. Owen, J., Schmidly, D. & Davis, W.B. (1984) A morphometric analysis of three species of Carollia (Chiroptera, Glossophaginae) from Middle America. Mammalia, 48, 85–94. https://doi.org/10.1515/mamm.1984.48.1.85
  82. Pacheco, V., Patterson, B.D., Patton, J.L., Emmons, L.H., Solari, S. & Ascorra, C.F. (1993) List of mammal species known to occur in Manu Biosphere Reserve, Peru. Publicaciones del Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Serie A, Zoología, 44, 1–12.
  83. Pacheco, V., Sánchez-Vendizú, P. & Solari, S. (2018) A new species of Anoura Gray, 1838 (Chiroptera: Phyllostomidae) from Peru, with taxonomic and biogeographic comments on species of the Anoura caudifer complex. Acta Chiropterologica, 20, 31–50. https://doi.org/10.3161/15081109ACC2018.20.1.002
  84. Parker, T.A., Schulenberg, T.S., Graves, G.R. & Braun, M.J. (1985) The avifauna of the Huancabamba Region, northern Peru. Ornithological Monographs, 36, 169–197. https://doi.org/10.2307/40168282
  85. Patterson, B.D., Solari, S. & Velazco, P.M. (2012) The role of the Andes in the diversification and biogeography of Neotropical mammals. In: Patterson, B.D. & Costa, L.P. (Eds.), Bones, clones, and biomes: the history and geography of recent neotropical mammals, University of Chicago Press, Chicago, pp. 351–78. https://doi.org/10.7208/chicago/9780226649214.003.0015
  86. Paynter, R.A., Jr. (1997) Ornithological gazetteer of Colombia. Second Edition. Harvard University, Cambridge, USA. ix + 537 pp. https://doi.org/10.5962/bhl.title.14638
  87. Pennington, T. & Lavin, M. (2017) Dispersal, isolation and diversification with continued gene flow in an Andean tropical dry forest. Molecular Ecology, 26, 3327–3329. https://doi.org/10.1111/mec.14182
  88. Peterson, A.T., Papes, M. & Soberon, J. (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modelling, 213, 63–72. https://doi.org/10.1016/j.ecolmodel.2007.11.008
  89. Peterson, A.T., Soberón, J., Pearson, R.G., Anderson, R.P., Martínez‐Meyer, E., Nakamura, M. & Araújo, M.B. (2011) Ecological niches and geographic distributions. Princeton University Press, Princeton, xii + 316 pp. https://doi.org/10.1515/9781400840670
  90. Phillips, C.J. (1971) The dentition of glossophagine bats: development, morphological characteristics, variation, pathology and evolution. Miscellaneous Publications of the Museum of Natural History University of Kansas, 54, 1–138.
  91. Phillips, S.J., Anderson, R.P. & Schapire, R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
  92. Phillips, S.J. & Dudík, M. (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography, 31, 161–175. https://doi.org/10.1111/j.0906-7590.2008.5203.x
  93. Prado, J.R. & Percequillo, A.R. (2018) Systematic studies of the genus Aegialomys Weksler et al., 2006 (Rodentia: Cricetidae: Sigmodontinae): geographic variation, species delimitation, and biogeography. Journal of Mammalian Evolution, 25, 71–118. https://doi.org/10.1007/s10914-016-9360-y
  94. Pyron, R.A. & Burbrink, F.T. (2010) Hard and soft allopatry: physically and ecologically mediated modes of geographic speciation. Journal of Biogeography, 37, 2005–2015. https://doi.org/10.1111/j.1365-2699.2010.02336.x
  95. 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. https://doi.org/10.11646/zootaxa.3441.1.1
  96. Radosavljevic, A. & Anderson, R.P. (2014) Making better Maxent models of species distributions: complexity, overfitting, and evaluation. Journal of Biogeography, 41, 629–643. https://doi.org/10.1111/jbi.12227
  97. Radua, J. & Albajes-Eizagirre, A. (2010) Seed-based d Mapping (AES-SDM) software package: FDR online calculator. Available from: https://www.sdmproject.com/utilities/?show=FDR (accessed on 11 January 2022)
  98. Rahbek, C., Borregaard, M.K., Antonelli, A., Colwell, R.K., Holt, B.G., Nogues-Bravo, D., Rasmussen, C.M.Ø., Richardson, K., Rosing, M.T., Whittaker, R.J. & Fjeldså, J. (2019a) Building mountain biodiversity: geological and evolutionary processes. Science, 365, 1114–1119. https://doi.org/10.1126/science.aax0151
  99. Rahbek, C., Borregaard, M.K., Colwell, R.K., Dalsgaard, B., Holt, B.G., Morueta-Holme, N., Nogues-Bravo, D., Whittaker, R.J. & Fjeldså, J. (2019b) Humboldt’s enigma: what causes global patterns of mountain biodiversity? Science, 365, 1108–1113. https://doi.org/10.1126/science.aax0149
  100. RDCT, R Development Core Team. (2004) R: A language and environment for statistical Computing. R Foundation for Statistical Computing, Vienna. Available from: http://www.R-project.org (accessed 10 January 2018)
  101. Rivas-Pava, M.P., Ramírez-Chaves, H.E., Álvarez, Z.I. & Niño-Valencia, B.L. (2007) Catálogo de los mamíferos presentes en las colecciones de referencia y exhibición del Museo de Historia Natural de la Universidad del Cauca. Universidad del Cauca, Popayán, 94 pp.
  102. Rodríguez-Muñoz, E., Montes, C., Rojas-Runjaic, F.J. & Crawford, A.J. (2022) Synthesis of geological data and comparative phylogeography of lowland tetrapods suggests recent dispersal through lowland portals crossing the Eastern Andean Cordillera. PeerJ, 10, e13186. https://doi.org/10.7717/peerj.13186
  103. Saldaña, I.S., Ugaz, A., Baldeón, A., Benites, D.A., Barrionuevo, R. & Vallejos, L.M. (2020) Bird diversity and noteworthy records from the western side of the Porculla Pass and the Huancabamba-Chamaya river sub-basin, northwest of Peru [with Erratum]. Arnaldoa, 27, 611–672.
  104. Salomon, M. (2002) A revised cline theory that can be used for quantified analyses of evolutionary processes without parapatric speciation. Journal of Biogeography, 29, 509–517. https://doi.org/10.1046/j.1365-2699.2002.00675.x
  105. Sanborn, C.C. (1933) Bats of the genera Anoura and Lonchoglossa. Field Museum of Natural History, Zoological Series, 20, 23–28.
  106. Särkinen, T., Pennington, R.T., Lavin, M., Simon, M.F. & Hughes, C.E. (2012) Evolutionary islands in the Andes: persistence and isolation explain high endemism in Andean dry tropical forests. Journal of Biogeography, 39, 884–900. https://doi.org/10.1111/j.1365-2699.2011.02644.x
  107. Starrett, A. (1969) A new species of Anoura (Chiroptera: Phyllostomatidae) from Costa Rica. Los Angeles County Museum Contributions in Science, 157, 1–9. https://doi.org/10.5962/p.241145
  108. Tamsitt, J.R. & Nagorsen, D. (1982) Anoura cultrata. Mammalian Species, 179, 1–5. https://doi.org/10.2307/3503899
  109. Tamsitt, J.R. & Valdivieso, D. (1963) Records and observations on Colombian bats. Journal of Mammalogy, 44, 168–180. https://doi.org/10.2307/1377449
  110. Tamsitt, J.R. & Valdivieso, D. (1966) Taxonomic comments on Anoura caudifer, Artibeus lituratus and Molossus molossus. Journal of Mammalogy, 47, 230–238. https://doi.org/10.2307/1378119
  111. Tenorio, E.A., Montoya, P., Norden, N., Rodríguez-Buriticá, S., Salgado-Negret, B. & González, M.A. (2023) Mountains exhibit a stronger latitudinal diversity gradient than lowland regions. Journal of Biogeography, 50, 1026–1036. https://doi.org/10.1111/jbi.14597
  112. Torres, D.A., Henao, J.R. & Castaño, J.H. (2014) Primer registro de Anoura cultrata (Chiroptera: Phyllostomidae) para la cuenca del río Cauca, Colombia. Mammalogy Notes, 1, 9–11. https://doi.org/10.47603/manovol1n2.9-11
  113. Ujueta G. (1999) La Cordillera Oriental colombiana no se desprende de la Cordillera Central. Geología Colombiana, 24, 3–28.
  114. Vargas-Arboleda A., Cuadrado-Ríos, S. & Mantilla-Meluk, H. (2020) Systematic considerations on two species of nectarivorous bats (Anoura caudifer and A. geoffroyi) based on barcoding sequences. Acta Biológica Colombiana, 25, 194–201. https://doi.org/10.15446/abc.v25n2.75848
  115. Velazco, P.M. & Patterson, B.D. (2019) Small mammals of the Mayo river basin in northern Peru, with the description of a new species of Sturnira (Chiroptera: Phyllostomidae). Bulletin of the American Museum of Natural History, 429, 1–70. https://doi.org/10.1206/0003-0090.429.1.1
  116. Voss, R.S., Fleck, D.W., Strauss, R.E., Velazco, P.M. & Simmons, N.B. (2016). Roosting ecology of Amazonian bats: evidence for guild structure in hyperdiverse mammalian communities. American Museum Novitates, 3870, 1–43. https://doi.org/10.1206/3870.1
  117. Warren, D.L. & Seifert, S.N. (2011) Ecological niche modeling in Maxent: the importance of model complexity and the performance of model selection criteria. Ecological Applications, 21, 335–342. https://doi.org/10.1890/10-1171.1
  118. Warren, D.L., Wright, A.N., Seifert, S.N. & Shaffer, H.B. (2014) Incorporating model complexity and spatial sampling bias into ecological niche models of climate change risks faced by 90 California vertebrate species of concern. Diversity and Distributions, 20, 334–343. https://doi.org/10.1111/ddi.12160
  119. Watanabe, S., Hajima, T., Sudo, K., Nagashima, T., Takemura, T., Okajima, H., Nozawa, T., Kawase, H., Abe, M., Yokohata, T., Ise, T., Sato, H., Kato, E., Takata, K., Emori, S. & Kawamiya, M. (2011) MIROC-ESM 2010: model description and basic results of CMIP5-20c3m experiments. Geoscientific Model Development, 4, 845–872. https://doi.org/10.5194/gmd-4-845-2011
  120. Wenzel, R.L. (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin, Biological Series, 20, 1–177. https://doi.org/10.5962/bhl.part.5666
  121. Zhang, Y.M., Williams, J.L. & Lucky, A. (2019) Understanding UCEs: a comprehensive primer on using ultraconserved elements for arthropod phylogenomics. Insect Systematics and Diversity, 3 (5), 3. https://doi.org/10.1093/isd/ixz016