SciELO - Scientific Electronic Library Online

 
vol.35Leucismo en Reithrodontomys Mexicanus Soederstroemi (Rodentia: Cricetidae), Quito, EcuadorVariación en el patrón de coloración de Abronia lythrochila (Reptilia: Anguidae) y su conservación en la Estación Biológica San José, San Cristóbal de las Casas, Chiapas, México índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Journal

Artigo

Indicadores

Links relacionados

  • Não possue artigos similaresSimilares em SciELO

Compartilhar


Acta zoológica mexicana

versão On-line ISSN 2448-8445versão impressa ISSN 0065-1737

Acta Zool. Mex vol.35  Xalapa  2019  Epub 30-Dez-2019

http://dx.doi.org/10.21829/azm.2019.3502082 

Notas Científicas

Retrieving Peromyscus Bullatus from p. Difficilis (Rodentia: Cricetidae) through cranial morphometry in a mammal collection

Recuperando especímenes de Peromyscus Bullatus de p. Difficilis (Rodentia: Cricetidae) mediante morfometría craneal en una colección mastozoológica

Ina Falfán1 

Sandra H. Montero Bagatella2  * 

Alvar González Christen3 

1Red de Ambiente y Sustentabilidad, Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, Xalapa, Veracruz, 91073, México. <isfalfan@yahoo.com.mx>

2Red de Biología y Conservación de Vertebrados, Instituto de Ecología, A.C., Carretera Antigua a Coatepec 351, Xalapa, Veracruz, 91073, México. <helena.bagatella@gmail.com>

3Instituto de Investigaciones Biológicas, Universidad Veracruzana, Avenida Dr. Luis Castelazo Ayala S/N, Xalapa, Veracruz, 91190, México. <agonzalez@uv.mx>

Abstract

Peromyscus bullatus and Peromyscus difficilis are sympatric and phenotypically similar rodents. Because of this, misidentification of both species is frequent in the field and in mammal collections. In this study, P. bullatus specimens were retrieved from the P. difficilis specimens, in the mammal collection of the Instituto de Investigaciones Biológicas of the Universidad Veracruzana, through the analysis of morphometric measurements of the tympanic bulla, proposed by González-Ruíz et al. (2005) as discrimination key variables between both species.

Resumen

La identificación errónea de ejemplares de Peromyscus bullatus como Peromyscus difficilis es frecuente, tanto en el campo como en las colecciones mastozoológicas, debido a que ambas especies son simpátricas y similares fenotípicamente. En este estudio se recuperaron ejemplares de P. bullatus incorrectamente catalogados como P. difficilis en la colección mastozoológica del Instituto de Investigaciones Biológicas de la Universidad Veracruzana, mediante el análisis de medidas morfométricas de la bula timpánica, propuestas por González-Ruíz et al. (2005) como claves para la discriminación entre ambas especies.

Peromyscus is one of the most representative genera of rodents in North America (Bedford & Hoekstra, 2015) displaying a wide range of morphological, physiological, and behavioral variation (Kirkland & Layne, 1989). Nevertheless, for some species, overlapping of morphological characters, color pattern, and shared distribution areas may make it difficult to accurately identify them in the field and scientific collections (Ramírez-Pulido et al., 2001; González-Ruíz et al., 2005). This is the case of the Southern rock deer mouse Peromyscus difficilis (J. A. Allen, 1891), widely distributed from Chihuahua to Oaxaca (Fernández et al., 2010), and the Perote mouse Peromyscus bullatus (Osgood, 1904), endemic to the Oriental basin in Veracruz and Puebla (González-Ruíz & Álvarez-Castañeda, 2005). Peromyscus difficilis is an abundant species found mainly in rocky volcanic areas with xerophytes and in forests with pinyon pines, junipers, and oaks. On the other hand, populations of P. bullatus are small, isolated, and restricted to flat sandy arid areas with grasses and scattered trees (Galindo-Leal & Krebs, 2004; González-Ruíz et al., 2005). According to Mexican legislation, the Perote mouse is classified under special protection and is considered critically endangered by the IUCN (Álvarez-Castañeda, 2018; SEMARNAT, 2018). To contribute to the correct discrimination of P. bullatus and P. difficilis, our objective was to evaluate the usefulness of using tympanic bulla morphometric measures, recommended by Osgood (1904) and Hoffmeister (1951), and corroborated by González-Ruíz et al. (2005) as key characters for the accurate discrimination between these species. For this purpose, we search for P. bullatus specimens erroneously identified as P. difficilis in the mammal collection of the Instituto de Investigaciones Biológicas of the Universidad Veracruzana (IIB - UV). Since misassignment of P. bullatus specimens as P. difficili IUCN s is frequent (González-Ruíz et al., 2005), we expected to find at least one miscataloged P. bullatus specimen, achieving hence an accurate discernment between studied species with the proposed tympanic bulla measures.

We obtained morphometric data from 109 adult specimens (according to Hoffmeister, 1951) cataloged as P. difficilis in the IIB-UV mammal collection (SEMARNAT VER-MAM-191-10-06); 52 females and 57 males. All specimens were from the region of San Antonio Limón (Totalco), currently a Protected Natural Area (Gobierno del Estado de Veracruz, 2016), in central Veracruz, Mexico. From each specimen’s tag, we obtained sex and body measurements: total length - TL, tail length - CL, hindfoot length - HL, ear length - EL. We measured seven dimensions from the right side of craniums: occipito-nasal length (OL), braincase breadth (BC), postorbital constriction (PC), nasal length (NL), maxillary tooth row length (LX), bulla length (BL), and bulla breadth (BW) after Santos-Moreno et al. (1998) and González-Ruíz et al. (2005). All measurements were taken using an electronic caliper (Mitutoyo series 500; 0.01 mm accuracy) by the same person (IF). We calculated the hindfoot to ear length ratio (HL-EL) and the occipito-nasal length to bulla length ratio (OL-BL; González-Ruíz et al., 2005).

To find specimens which were different within the P. difficilis group, possibly P. bullatus whose identity (i.e. catalog number) we did not know, we generated a hierarchical cluster dendrogram (Euclidian distance, average linkage; Kettenring, 2006) in R (R Core Team, 2018) for the joint sexes, since sexual dimorphism is absent in both species (González-Ruíz & Álvarez-Castañeda, 2005; Fernández et al., 2010). For the dendrogram, we used the BL, BW, OL-BL and LX measurements; reported by González-Ruíz et al. (2005) as key characters to differentiate P. bullatus from P. difficilis. We used hierarchical cluster analysis because it is based on groups’ similarities/dissimilarities and is not necessary to know a priori the number of groups nor the identity of their elements (Kettenring, 2006).

According to the cluster dendrogram, four specimens were different from the remaining sample (IIB-UV catalog number: 1052, 1053, 1673, 1695) at a linkage distance > 1.5 (Fig. 1). After a thorough inspection, we identified these four specimens as P. bullatus since they showed, on average, smaller somatic (TL, CL, HL) and cranial (OL, NL, LX, BC, PC) values and larger ear (EL) and bulla measurements (BL, BW, OL-BL ratio) than P. difficilis (Table 1). These specimens were corroborated as P. bullatus by González-Ruíz from the Universidad Autónoma Metropolitana and were re-cataloged in the IIB-UV mammal collection. The four specimens identified as P. bullatus constituted the first ones for the IIB-UV mammal collection and were added up to those already deposited in other collections.

Figure 1 Cluster dendrogram for the joint sexes. Dashed box indicates the specimens different on average from the rest of the group, which was re-cataloged as P. bullatus in the IIB-UV mammal collection. 

Table 1 Descriptive statistics of measurements (mm) for retrieved Peromyscus bullatus and Peromyscus difficilis. n: number of measured specimens, SD: standard deviation. Refer to text for the use of measures acronyms. 

Variable Peromyscus bullatus Peromyscus difficilis
n Average ± SD n Average ±SD
TL 4 190.00 ± 26.26 105 213.69 ± 16.37
CL 4 93.00 ± 24.45 105 111.83 ± 11.23
HL 4 23.75 ± 0.50 105 24.22 ± 1.76
EL 4 25.75 ± 0.96 105 25.40 ± 1.65
OL 4 27.80 ± 0.69 85 29.58 ± 0.82
NL 4 10.31 ± 0.38 85 11.37 ± 0.45
LX 4 4.30 ± 0.08 105 4.67 ± 0.15
BC 4 13.03 ± 0.09 103 13.58 ± 0.29
PC 4 4.33 ± 0.09 105 4.53 ± 0.16
BL 4 6.01 ± 0.21 102 5.86 ± 0.20
BW 4 4.87 ± 0.03 102 4.76 ± 0.16
OL-BL 4 21.60 ± 0.43 83 19.81 ± 0.53
HL-EL 4 1.08 ± 0.06 105 1.06 ± 0.14

For both P. bullatus and P. difficilis our measurements were lower than those recorded by González-Ruíz et al. (2005), likely due to variation of the studied populations or to inter-measurer variation (Santos-Moreno et al., 1998). Regardless of these differences, the data and description of species provided by González-Ruíz et al. (2005) greatly helped us to discriminate specimens’ species. While the BL, BW, and LX measurements were valuable for discriminating specimens through hierarchical cluster analysis, we found that the OL-BL ratio was the most important measurement for species identification. In P. bullatus specimens OL-BL ratio exceeded the average value for P. difficilis, corroborating the findings reported by González-Ruíz et al. (2005). Furthermore, we did not find overlapping average ± SD values for the OL-BL ratio between species. While average ± SD values for P. bullatus cranial measurements should be interpreted cautiously due to our n = 4, the showed tendency by morphometric data for this species was clear and agreed with the findings of González-Ruíz et al. (2005). However, contrary to descriptions by Osgood (1909) and conclusions by González-Ruíz et al. (2005), the HL-EL ratio was not useful to us since all the studied specimens presented values within the same range, possibly due to HL values were taken by several measurers.

The contribution by González-Ruíz et al. (2005), together with cluster analysis, were valuable for discriminating species when craniums were studied, nevertheless, for identification of P. bullatus in the field, besides total length and coloration (slightly smaller and lighter than P. difficilis), the habitat type where the specimens are captured is a valuable criterion due to the specific requirements of the species, (Hoffmeister, 1951; González-Ruíz et al., 2005). Since only 3.67% of the studied specimens turned out to be P. bullatus, whose rarity and small populations in the field are corroborated, our findings support the conservation efforts for this species, which has been left with a reported 6.3% of remnant habitat (Sánchez-Cordero et al., 2005).

Since the scientific collections are a valuable bank of information, an accurate assignment of species to specimens is fundamental. Especially for underrepresented species, which in turn are often endemic or poorly studied ones. Additionally, erroneous identification can be detrimental for systematic, taxonomic, morphometric, and conservation studies of species. Even more, due to information deposited in collections has a greater scope and availability through digital platforms. Because of this, a routine review of the specimens to update or correct the information has been widely recommended (Lorenzo et al., 2012). Given our findings and the importance of having accurately designated specimens, we support a further search for P. bullatus among the P. difficilis specimens in collections, when they have been collected from the Oriental basin region in Mexico. The use of the bulla variables, particularly the OL-BL ratio, is useful for performing such task.

Acknowledgements

We are grateful to N. González Ruíz for verification of specimens, to C. Hernández-Lara for their valuable comments, and to K. MacMillan and H. J. Bowen for the language revision.

Literature cited

Álvarez-Castañeda, S. T. (2018)Peromyscus bullatus. The IUCN Red List of Threatened Species 2018: e.T16653A22361454. http://dx.doi.org/10.2305/IUCN.UK.2018-1.RLTS.T16653A22361454.en (accessed on July 2019). [ Links ]

Bedford, N. L., Hoekstra, H. E. (2015) Peromyscus mice as a model for studying natural variation. Elife, 4: e06813. https://elifesciences.org/content/4/e06813Links ]

Fernández, J. A., García-Campusano, F., Hafner, M. S. (2010) Peromyscus difficilis (Rodentia: Cricetidae). Mammalian Species, 42, 220-229. https://doi.org/10.1644/867.1 [ Links ]

Galindo-Leal, C., Krebs, C. J. (2004) Habitat structure and demographic variability of a habitat specialist: The Rock Mouse (Peromyscus difficilis). Revista Mexicana de Mastozoología, 2, 72-89. [ Links ]

Gobierno del Estado de Veracruz (2016) Decreto por el que se declara Área Natural Protegida Reserva Ecológica San Antonio Limón Totalco en el Ejido San Antonio Limón Totalco, Municipio de Perote, Ver. Gaceta Oficial del Estado de Veracruz. Xalapa, México. [ Links ]

González-Ruíz, N., Álvarez-Castañeda, S. T. (2005) Peromyscus bullatus. Mammalian Species, 770, 1-3. https://doi.org/10.1644/1545-1410(2005)770[0001:PB]2.0.CO;2 [ Links ]

González-Ruíz, N. , Álvarez-Castañeda, S. T. , Álvarez, T. (2005) Distribution, taxonomy, and conservation status of the Perote Mouse Peromyscus bullatus (Rodentia: Muridae) in México. Biodiversity and Conservation, 14, 3423-3436. https://doi.org/10.1007/s10531-004-0548-8 [ Links ]

Hoffmeister, D. F. (1951) A taxonomic and evolutionary study of the piñon mouse Peromyscus truei. Illinois, Biological Monograph, 21, 1-104. [ Links ]

Kettenring, J. R. (2006) The practice of cluster analysis. Journal of Classification, 23, 3-30. https://doi.org/10.1007/s00357-006-0002-6 [ Links ]

Kirkland, G. L., Layne, J. N. (1989) Advances in the study of Peromyscus (Rodentia). Texas Tech University Press. Lubbock, EE.UU, 366 pp. [ Links ]

Lorenzo, C., Álvarez-Castañeda, S. T. , Arellano, E., Arroyo-Cabrales, J., Bolaños, J., Briones-Salas, M., Cervantes, F. A., Chablé-Santos, J., Corral, L., Cortés, M., Cortés-Calva, P., Cuevas, M. P., Elizalde-Arellano, C., Escobedo-Cabrera, E., Espinoza, E., Estrella, E., Gallo-Reynoso, J. P., García-Mendoza, D. F., Garza-Torres, H. A., González Christen, A., González-Cózatl, F. X., González-Monroy, R. M., González-Ruiz, N., Guzmán, D., Guzmán, A. F., Hernández-Betancourt, S. F., Hortelano-Moncada, Y., Iñiguez, L. I., Jiménez-Guzmán, A., Kantum, Y. N., León-Paniagua, L., López-González, C., López-Soto, J. H., López-Vidal, J. C., Martin, N., Martínez-Vázquez, J., Mejenes-López, S. M. A., Morales-Vela, B., Muñiz-Martínez, R., Niño-Ramírez, J. A., Núñez-Garduño, A., Pozo, C., Ramírez-Pulido, J., Retana, O. G., Ruan, I., Selem, C. I., Vargas, J., Zúñiga-Ramos, M. Á. (2012) Los mamíferos de México en las colecciones científicas de Norteamérica. Therya, 3, 239-262. http://dx.doi.org/10.12933/therya-12-65 [ Links ]

Osgood, W. H. (1904) Thirty new mice of the genus Peromyscus from Mexico and Guatemala. Proceeding of the Biological Society of Washington, 17, 55-77. [ Links ]

Osgood, W.H. (1909) Revision of the mice of the American genus Peromyscus. North American Fauna, 28, 1-285. [ Links ]

R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available in: https://www.R-project.org/. [ Links ]

Ramírez-Pulido, J. , Castro-Campillo, A., Salame-Méndez, A. (2001) Los Peromyscus (Rodentia: Muridae) en la colección de mamíferos de la Universidad Autónoma Metropolitana-Unidad Iztapalapa (UAMI). Acta Zoológica Mexicana, 83, 83-114. [ Links ]

Sánchez-Cordero, V., Illoldi-Rangel, P., Linaje, M., Sarkar, S., Peterson, A. T. (2005) Deforestation and extant distributions of Mexican endemic mammals. Biological Conservation, 126, 465-473. https://doi.org/10.1016/j.biocon.2005.06.022 [ Links ]

Santos-Moreno, J. A., Gaona, S., Hortelano, Y. (1998) Importancia de la experiencia y de la variación intermedidor en la toma de medidas craneales para estudios morfométricos. Revista Mexicana de Mastozoología, 3, 137-145. http://dx.doi.org/10.22201/ie.20074484e.1998.3.1.65 [ Links ]

SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales) (2018) Proyecto de modificación del Anexo Normativo III, Lista de Especies en Riesgo de la Norma Oficial Mexicana NOM-059-SEMARNAT-2010: Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Secretaría de Medio Ambiente y Recursos Naturales. Ciudad de México, México. 13 de agosto de 2018. Available in: Available in: https://dof.gob.mx/nota_detalle.php?codigo=5534594&fecha=13/08/2018 (accessed on July 2019). [ Links ]

Received: October 01, 2018; Accepted: September 04, 2019

*Autor de correspondencia: <helena.bagatella@gmail.com>

Editor responsable:

Alberto González Romero

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License