Morphological Variation in the Skull of Nephelomys meridensis (Rodentia, Cricetidae): Evidence for Cryptic Species in Andean Populations from Northern South America

Authors

  • Franger Jesús García Alvarez Universidad de Carabobo, Estado Carabobo, Venezuela
  • Elvira Sánchez-González
  • Marjorie Machado

Keywords:

cranial morphology, geometric morphometrics, Nephelomys albigularis group, Oryzomyini, species complex

Abstract

The genus Nephelomys comprises at least 13 taxa with altitudinal distribution ranging from 900 to 4,000 meters above sea level. Three species are currently known to occur in Venezuela, but some authors suggest that two additional taxa are present in Venezuelan Andes populations and consider N. meridensis as a species complex. We conducted geometric morphometric analyses of skulls and jaws from populations assignable to the monotypic species N. meridensis from the Venezuelan Andes, in order to examine and compare morphological variations in this species. We compared four localities (including the type locality of N. meridensis) situated in northern, central, and western portions of Cordillera de Mérida and the Tamá páramo. We created morphological landmarks on dorsal, ventral, lateral, and jaw views of each skull using the tpsDIG software. Significant differences were found in skull shape and isometric size in most of the populations examined. The discrimination and morphological differentiation of some of these groups with respect to the population from the type locality (Mérida) were aligned with the results from multivariate and cytogenetic analyses carried out previously by other authors. Our data support recognizing N. meridensis as a species complex, comprising at least three still undescribed taxa from the Yacambú National Park (cordillera de Mérida), La Trampita (cordillera de Mérida) and the Tamá páramo (Tamá massif). A more detailed taxonomic study of Nephelomys from Venezuela, molecular and linear morphometric analyses, and revision of morphological characters, are necessary to describe potential new taxa and determine the geographical distribution of the species in this genus.

References

Aguilera, M., A. Pérez-Zapata, and A. Martino. 1995. Cytogenetics and karyosystematics of Oryzomys albigularis (Rodentia, Cricetidae) from Venezuela. Cytogenetics and Cell Genetics 69:44–49.

Anderson, R. P., and A. Raza. 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.

Anderson, R. P., E. E. Gutiérrez, J. Ochoa-G., F. J. García, and M. Aguilera. 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.

Astúa, D., I. Bandeira, and L. Geise. 2015. Cranial morphometric analyses of the cryptic rodent species Akodon cursor and Akodon montensis (Rodentia, Sigmodontinae). Oecología Australis 19:143–157.

Bonvicino, C. R., and M. A. M. Moreira. 2001. Molecular phylogeny of the genus Oryzomys (Rodentia: Sigmodontinae) based on cytochrome b DNA sequences. Molecular Phylogenetics and Evolution 18:282–292.

Bookstein, F. L. 1991. Morphometric tools for landmark data. Geometry and biology Cambridge University Press. New York, U.S.A.

Boroni, L. N., L. S. Lobo, P. S. R. Romanom and G. Lessa. 2017. Taxonomic identification using geometric morphometric approach and limited data: an example using the upper molars of two sympatric species of Calomys (Cricetidae: Rodentia). Zoologia 34:1–11.

Cordeiro-Estrela, P., M. Baylac, C. Denys, and J. Marinho-Filho. 2006. Interspecific patterns of skull variation between sympatric Brazilian vesper mice: geometric morphometrics assessment. Journal of Mammalogy 87:1270–1279.

Cordeiro-Estrela, P., M. Baylac, C. Denys, and J. Polop. 2008. Combining geometric morphometrics and pattern recognition to identify interspecific patterns of skull variation: case study in sympatric Argentinian species of the genus Calomys (Rodentia: Cricetidae: Sigmodontinae). Biological Journal of the Linnean Society 94:365–378.

García, F. J., and E. Sánchez-González. 2013. Morfometría geométrica craneal en tres especies de roedores arborícolas neotropicales (Rodentia: Cricetidae: Rhipidomys) en Venezuela. Therya 4:157–178.

García, F. J., E. Sánchez-González, M. Machado, G. Flórez, D. Araujo-Reyes, O. Vásquez-Parra, and D. Prieto-Torres. 2019. First record of the Santa Marta mouse, Nephelomys maculiventer (Mammalia, Rodentia, Cricetidae), for Venezuela. Mammalia 83:203–207.

García, F. J., E. Sánchez-González, D. Araujo-Reyes, M. Machado, and G. Flórez. 2018. Descripción de una nueva subespecie de ratón mochilero del género Heteromys (Mammalia, Rodentia, Heteromyidae) en Venezuela. Revista de Biodiversidad Neotropical 8:41–54.

Gutiérrez, E. E., J. E. Maldonado, A. Radosavljevic, J. Molinari, B. D. Patterson, J. M. Martínez-C, A. R. Rutter, M. T. R. Hawkins, F. J. García, and J. Maldonado. 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 10:1–24.

Hammer, Ø., and D. A. T. Harper. 2011. PAST: PAlaeontological STAtistics, versión 2.10. http://folk.uio.no/ ohammer/past. Accesed in February 2020

Josse C., F. Cuesta, G. Navarro, V. Barrena, E. Cabrera, E. Chacón-Moreno, W. Ferreira, M. Peralvo, J. Saito, and A. Tovar. 2009. Ecosistemas de los Andes del Norte y Centro. Bolivia, Colombia, Ecuador, Perú y Venezuela. Secretaría General de la Comunidad Andina, Programa Regional ECOBONA-Intercooperation, CONDESAN-Proyecto Páramo Andino, Programa BioAndes, EcoCiencia, NatureServe, IAvH, LTA-UNALM, ICAE-ULA, CDC-UNALM, RUMBOL SRL. Lima, Perú.

Klingenber, C. P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11:353–357.

La Marca, E. 1997. Origen y evolución geológica de la Cordillera de Mérida, Andes de Venezuela. Geografía 1:1–110.

Márquez, E. J., M. Aguilera M., and M. Corti. 2000. Morphometric and chromosomal variation in populations of Oryzomys albigularis (Muridae: Sigmodontinae) from Venezuela: multivariate aspects. Zeitschriftfür Säugetierkunde 65:84–99.

Meloro, C, P. Raia, P. Piras, C. Barbera, and P. O’ Higgins. 2008. The shape of the mandibular corpus in large fissiped carnivores: allometry, function and phylogeny. Zoological Journal of the Linnean Society 154:832–845.

Musser, G. G., M. D. Carleton, E. M. Brothers, and A. L. Gardner. 1998. Systematic studies of oryzomyine rodents (Muridae, Sigmodontinae): diagnoses and distributions of species formerly assigned to Oryzomys‘‘capito’’. Bulletin of the American Museum of Natural History 236:1–376.

Ochoa-G., J., M. Aguilera, V. Pacheco, and P. J. Soriano. 2001. A new species of Aepeomys Thomas, 1898 (Rodentia: Muridae) from the Andes of Venezuela. Mammalian Biology 66:228–237.

Percequillo, A. R. 2003. Sistemática de Oryzomys Baird, 1858: definicão dos grupos de espécies e revisãotaxonômica do grupo albigularis (Rodentia, Sigmodontinae). PhD Thesis, Universidade de São Paulo, Brazil.

Percequillo, A. R. 2015. Genus Nephelomys Weksler, Percequillo and Voss 2006. Pp. 377–390 in Mammals of South America Volume 2. (Patton, J. L., Pardiñas, U. F. J., y G. D’Elía, eds). The University of Chicago Press. Chicago, U.S.A.

Quiroga-Carmona, M., and C. DoNascimiento. 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.

Rivas, B. A., and J. E. Péfaur. 1999a. Variación geográfica en poblaciones venezolanas de Oryzomys albigularis (Rodentia: Muridae). Mastozoología Neotropical 6:47–59.

Rivas, B. A., and J. E. Péfaur. 1999b. Variación craneana entre sexo y edad en Oryzomys albigularis (Rodentia: Muridae). Mastozoología Neotropical 6:61–70.

Rohlf, F. J. 2006. tpsDig, Digitize landmarks and outlines. Version 2.05. New York: Stony Brook. Department of Ecology and Evolution, State University of New York. New York, U.S.A.

Sheets H. D. 2010. Integrated Morphometrics Package (IMP) 7. http://www3.canisius.edu/~sheets/imp7.htm. Accesed in February 2020.

Soriano, P. J., A. Díaz de Pascual, J. Ochoa-G., and M. Aguilera. 1999. Biogeographic analysis of the mammal communities in the Venezuelan Andes. Interciencia 24:17–25.

Weksler, M. 2003. Phylogeny of Neotropical oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Molecular Phylogenetics and Evolution 29:331–349.

Weksler, M. 2006. Phylogenetic relationships of oryzomyine rodents (Muroidea: Sigmodontinae): separate and combined analyses of morphological and molecular data. Bulletin of the American Museum of Natural History 296:1–149.

Weksler, M., A. R. Percequillo, and R. S. Voss. 2006. Ten new genera of oryzomyine rodents (Rodentia. Cricetidae). American Museum Novitates 3537:1–29.

Woodman, N. A. 2002. New species of small-eared shrew from Colombia and Venezuela (Mammalia: Soricomorpha: Soricidae: Genus Cryptotis). Proceedings of the Biological Society of Washington 115:249–272.

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2020-03-23

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