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Rodentia: Cricetidae), with the Description of Two New Species

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Rodentia: Cricetidae), with the Description of Two New Species Revista Mexicana de Mastozoología Nueva época Issn: 2007 - 4484 PHYLOGEnETIC RElATIonsHIPs oF Calomys sorellus CoMPlEX (RoDEnTIA: CRICETIDAE), WITH THE DEsCRIPTIon oF TWo nEW sPECIES HORACIO ZEBALLOS1, R. EDUARDO PALMA2, PABLO A. MARQUET2,3, AND GERARDO CEBALLOS4 1 Instituto de Ciencias de la Naturaleza, Territorio y Energías Re- novables, Pontificia Universidad Católica del Perú, Av. Universitaria 1801, San Miguel, Lima 32, Perú 2 Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Alameda 340, Santiago 6513677, Chile 3 Instituto de Ecologia & Biodiversidad (IEB), Casilla 653, Santiago, Chile 4 Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, Mexico D.F. 04510, México Autor de correspondencia: Horacio Zeballos; correo electrónico: [email protected] ABSTRACT We reviewed the phylogenetic relationships of forms assigned to Calomys sorellus based on the Cyto- chrome b gene sequences and morphological comparisons. We present the first description of the evolutionary relationships within the C. sorellus species complex. The results show a clade with species from lowlands of Eastern of Andes and other clade with Andean species which contains: C. musculinus, C. sorellus and C. lepidus which would be species complex. One of the new species occurs in the Ati- quipa Lomas in the coastal desert of southern Peru, and other on the occidental slope of southern Peru in Arequipa and Moquegua. These new species are based upon considering their phenotypic characte- ristics (size, coloration, pelage), geographic distribution, and molecular phylogeny. Key words: New species, rodent, Sigmodontinae, biodiversity, Peru. RESUMEN Revisamos las relaciones filogenéticas de las formas asignadas a Calomys sorellus basados en secuencias nucleotídicas del gen mitocondrial Citocromo b así como de caracteres morfológi- cos. Los resultados muestran un clado que agrupa a las formas de las tierras bajas al este de los Andes y a un clado andino, compuesto por: Calomys musculinus, Calomys sorellus y Calomys lepidus que serían complejos de especies. C. sorellus estaría compuesto por al menos cinco es- pecies, tres de ellas previamente fueron definidas como subespecies, a las que agregamos dos especies nuevas. Una de ellas habita en las lomas de Atiquipa en la costa desértica del sur del Perú, y la otra en las vertientes occidentales de los Andes del sur del Perú en Arequipa y Mo- quegua. Estas nuevas especies están definidas por sus diferencias morfológicas y moleculares y por su tamaño corporal, pelaje y distribución geográfica. Palabras clave: Especie nueva, roedor, Sigmodontinae, biodiversidad, Perú. REVISTA MEXICANA DE MASTOZOOLOGÍA Nueva época, 2014, Año 4 Núm. 1 • 1 Introduction Oliver Pearson (pers. comm.) captu- red one individual of the Calomys genus in the Sigmodontine rodents are one of the most di- coastal region of Arequipa, without assigning it verse groups of mammals in the world inhabi- to any species. We collected additional speci- ting almost all terrestrial environments of South mens in the same locality. At first glance, those America (Catzeflis et al., 1992; Wilson and Ree- specimens did not appear to be similar to any der, 2005). The tribe Phyllotini, one of the most species of the Calomys species already descri- diverse groups in this subfamily, includes two bed. Therefore, to define the identity of those very diverse genera, Phyllotis and Calomys. specimens we carried out analyses of phyloge- The genus Calomys inhabits a large region bet- netic relationships. So, in this paper we analyze ween Venezuela and Argentina in the Andean molecular and morphological traits of the genus highlands and the eastern lowlands and is re- Calomys in Peru to evaluate its phylogenetic re- lated to the oldest forms of the Sigmodontine lationships and species composition. radiation (Baskin, 1978). Most of these species inhabit the eastern lowlands of the Andes. Ca- MATERIALS brera (1961) and Ellerman (1941) recognized AND METHODS 10 to 15 species in this genus, but the number was reduced to four by Hershkovitz (1962). Study area However, two of these species Calomys lau- The Calomys specimens we used in cha and Calomys callosus, have been consi- this study included all its geographic range in dered a species’ complex (Massoia et al., 1968; Peru (Figure 1). The distribution range of Ca- Pearson and Patton, 1976; Williams and Mares, lomys in Peru extends along the Puna from the 1978; Reig, 1986; Corti et al., 1987; Olds, 1988; northern Andes to the southern international Bonvicino and Almeida, 2000) and a recent re- border with Bolivia and Chile. The genus is also visions of the genus have recognized at least known form a small area on the southern coast 13 species within it (Salazar-Bravo et al., 2001; of the Arequipa department where the seasonal Bonvicino et al., 2010; Musser and Carleton, fog input supports the development of rich ve- 2005; Almeida et al., 2007; González-Ittig et al., getation along hills know as “Loma formations” 2007; Haag et al., 2007). (Figure 1). In the Peruvian Andes two species of Calomys have been recognized. Calomys le- Morphological characteristics pidus occurs in the highlands of the Andes We reviewed 240 Calomys specimens above 3,000 m, from central Peru to northwes- which are stored in the following collections: the tern Argentina (Pearson, 1951; Cabrera, 1961; Bolivian Collection of Fauna (CBF) in La Paz, Bo- Heshkovitz, 1962; Steppan, 1995). The second livia; the Museum of Natural History at the Uni- species, Calomys sorellus, is endemic to Peru, versidad Nacional Mayor de San Marcos (MUSM) where it is widely distributed along the Andes in Lima, Peru; and the Scientific Collection of from the northern most part of the country to Museum of Natural History of the Universidad the Peruvian Andes around Titicaca Lake (Pa- Nacional de San Agustin (MUSA) in Arequipa, checo, 2002). In the northern part of its range, Peru (Appendix 1). We followed the terminolo- C. sorellus lives above 2,000 m whereas in the gy for cranial and dental morphology described Andean regions of southern Peru it occurs over by Hershkovitz (1962), Carleton and Musser 3,300 m (Cabrera, 1961; Heshkovitz, 1962; (1989), Voss 1988, and Steppan (1995). Ex- Pearson, 1951; Steppan, 1995), and its occu- ternal and cranial measurements (Tables 1, 2) rrence in western Bolivia is also very likely (An- were recorded in millimeters (mm) and weight in derson, 1997). Three subspecies of C. sorellus grams (g). Body measurements were obtained have been recognized: C. s. sorellus, C. s. frida, from the skin label; tail length was subtracted and C. s. miurus. from total length to obtain the head-and-body 2 • REVISTA MEXICANA DE MASTOZOOLOGÍA Nueva época, 2014, Año 4 Núm. 1 LORETO LORETO LORETO LOLROERTEOTO LORLEOTROETO AMAZONAS CAJAMARCA SOUTH SAN MARTIN AMERICA AMAZONAS CAJAMARCA AMAZONAS AMAAMZAOZNOANSAS CAJAMAAMRACZAONAS CACJAAJMAAMRAZOCRANCAS SOUTH CAJAMARCA CALJAA LMIBAERRCTAAD SAN MARTIN AMERICA SSOOUUTTHH SAN MARTIN SOSUOTUHTH SASNA NM AMRATRITNIN AAMMEERRICIICAA SANS MANA RMTAINRTIN AMAEMREICRAICA LA LIBERTAD LA LIBERTAD LAL AL ILBIEBRETRATDAD LA LLIABA ELNRICBTAESRDHTAD HUANUCO UCAYALI HUANUCO ANCASH PASCO ANCASH HUANUCO ANACNACSAHSH HUHAUNAUNCUOCO ANCAANSCHASH HUAHNUUACNOUCO UCAYALI UCAYALI UCUACYAAYLAILI PASCO UCAUYCAALYI ALI LIMA JUNIN PASCO PAPSACSOCO CALLAO PASPCAOSCO MADRE DE DIOS LIMA JUNIN CALLAO LIMA JUNIN LILMIMAA JUJNUINNIN MADRE DE DIOS LIMALIMA HUANCAVELJIUCNAJINUNIN CALLAO CUSCO CACLALLALOAO MADRE DE DIOS CALCLALOLAO MAMDARDER ED ED ED IDOISOS MADMRAED DRE DIEO DSIOS HUANCAVELICA APURIMAC AYACUCHO CUSCO ICA HUANCAVELICA HUHAUNACNACVAEVLEILCIACA HUANCAVELICA CUSCO HUANCAVELICA CUCSUCSOCO CUSCCUOSCO PUNO FIGURE 1. MAP OF SPE- AYACUCHO APURIMAC ICA CIES DISTRIBUTION OF APURIMAC AYACUCHO APAUPRUIRMIAMCAC AYAAYCAUCCUHCOHOAPURIMAC ICAAYAACYUACCHUOCHO APURIMAC Calomys FROM PERU: ICIACA ICAICA AREQUIPA PUNO C. sorellus (BLACK LAGO TITICACA PUNO SQUARES); C. miu- PUPNUONO Altimetria PUNPOUNO rus (WHITE CIRCLES); m.s.n.m. AREQUIPA MOQUEGUA LAGO TITICACA AREQUIPA C. frida OF CUSCO ARAERQEUQIUPIAPA 0 - 2,000 AREQUIPA LAGO TITICACA AREQUIPA LALGAOG OT ITITCIACCAACA (BLACK TRIANGLES); C . Altimetria LAGLOA GTIOT ICTIATCICAACA 2,000 - 4,000 TACNA frida OF PUNO (WHITE m.s.n.m. Altimetri0a 75 150 300 Km Al>tAi 4ml,t0ie0mt0AreAilatlirtmiiameetrtiraia MOQUEGUA SQUARES C. achaku 0 - 2,000m.s.n.m. ); mm.s.s.n.n.m.m. MOQUEGUA m.sm.n.s.m.n.m. MOMQOUQEUGEUGAUA MOQMUOEQGUUEAGUA (WHITE TRIANGLES, TYPE 2,000 - 4,000 0 0- 2-- ,20,,00000 0 - 02 ,-0 020,000 TACNA WHITE STAR AND C . 2,0000 - 4,00705 150 300 Km ); > 4,000 2,20,00 0- 4- ,40,000 TACNA 2,0020,0 -0 04 ,-0 040,000 TATCANCANA chinchilico BLACK 0 75 150 300 Km TACTNAACNA ( > >4 ,40,,00000 00 7755 115500 33000KKmm > 4>,0 040,000 0 0 7575 151050 30300K0mKm STAR). REVISTA MEXICANA DE MASTOZOOLOGÍA Nueva época, 2014, Año 4 Núm. 1 • 3 length (HB). Other measurements included: To- Prism 310 (Applied Biosystems) at the labora- tal length (T); tail length (TL); hind foot length tory of Molecular Diversity, Pontificia Universi- (HF); EL, ear length (EL); and weight (W). Cra- dad Católica de Chile. Sequences were aligned nial measurements corresponded to: Condyle- using the Clustal X 1.83 program (Thompson et Incisive Length; (CIL); LN, Nasallength (NL); al., 1997), checked visually, and edited with the Breadth of Braincase (BB); Breadth of Rostrum programs BioEdit 7.0 (Hall 1999) and DnaSP (BR); Zygomatic Breadth (ZB); Least Interorbi-
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