Phyllotis nogalaris Thomas, 1921

Jayat, J. Pablo, Ortiz, Pablo E., González, F. Rodrigo & D’Elía, Guillermo, 2016, Taxonomy of the Phyllotis osilae species group in Argentina; the status of the “ Rata de los nogales ” (Phyllotis nogalaris Thomas, 1921; Rodentia: Cricetidae), Zootaxa 4083 (3), pp. 397-417 : 406-413

Phyllotis nogalaris Thomas, 1921

( Figs. 3 , 6 and 7 )

Phyllotis nogalaris Thomas, 1921 . Ann. & Mag. Nat. Hist., 9 (8): 611.

Phyllotis osilae nogalaris Pearson, 1958 . Univ. Cal. Publ., Zool., 56 (4): 427.

Holotype. Adult male. B.M. 21.11.1.22 . Original number 1472 (col. E. Budin).

Type locality. “Higuerilla, 2000 m ”, Jujuy, Argentina ( Thomas 1921); restricted by Pardiñas et al. (2007) to Pampichuela , Valle Grande , Jujuy (23°32' S, 65°02' W, 1735 m) ( Fig. 5 ).

Emended diagnosis. A member of the tribe Phyllotini distinguishable from all other species of Phyllotis by the following combination of state characters: size large for the genus (mean values in mm for adult specimens [age classes 3–5]: length of head and body, 128; tail length, 140; condyle-incisive length, 29.46; maxillary tooth row length, 5.75; Table 1 ); fur dense and soft, richly colored; dorsal coloration uniform, obscure buffy brown but with notorious blackish eye rings; flanks with a striking yellowish-orange fringe extended from cheeks to the rump; venter buffy white with a ochraceous pectoral streak; tail relatively dark and bicolored along most of its length with the exception of the entirely blackish distal end; skull heavily built, with the rostrum relatively long and broad; nasals extending beyond the level of the lacrimal bones; large lacrimals; zygomatic notches broad and deep; interorbital region narrow and pinched, hour-glass shaped, without sharply squared posterior margins; zygomatic plate relatively broad; zygomatic arches well expanded; mesopterygoid fossa relatively broad and with a median spine; incisors whitish-yellow; molars hypsodont and robust, relatively long and broad.

Description. Dorsal coloration dark buffy brown and heavily streaked with black hairs. Head of the same general color than dorsum but with conspicuous blackish eye rings. Sides of the body yellowish-orange (this coloration pattern constitute a fringe extending from cheeks to rump). Venter buffy white, with a mid-ventral yellowish-orange pectoral streak. Chin and throat lighter than belly, including some hairs entirely white in the chin. Ears of the same color than dorsum. Manus and pes covered by dense and short white hairs. In both fore and hind feet the ungual white tufts surpass the end of the claws. Tail relatively dark, with the ventral surface strongly paler than dorsum, but with the distal tip entirely blackish, and with a small tuft of hairs.

The skull of P. nogalaris looks more strongly built than those of the other species of the P. osilae group ( Fig. 3 ). Rostrum broad and elongated, with nasals extending beyond the level of the lacrimal bones. Lacrimals comparatively well developed. Zygomatic notches deep and broad. Zygomatic plate relatively broad and high (see Tables 1 and 2), with a straight anterior border. Interorbital region narrow, hour-glass shaped, and pinched. Braincase broad, without evident temporal and lambdoidal crests. Posterior ends of the incisive foramina surpass the anterior face of M1. Mesopterygoid fossa wide in the context of the P. osilae species group, bearing a welldeveloped median spine on the palatine. Two posterolateral palatal pits are adjacent to the anterior margin of the mesopterygoid fossa. Parapterygoid fossae well developed and moderately excavated. Hamular process delicate and distally attached to the mastoidal capsule. Auditory bullae with a short and broad bony eustachian tube. Mandibular condyle slightly lower than coronoid process, extending posteriorly just behind the angular process. Capsular projection moderately developed. Upper and lower ridges of the masseteric crests joining anteriorly at the level of the protoflexid of m1 and extending approximately to the mental foramen.

Upper incisors orthodont, with the anterior enamel whitish-yellow. Molars relatively hypsodont, with tendency to lamination, and the primary cusps slightly alternate ( Fig. 6 ). M1 with a procingulum antero-posteriorly compressed, without anteromedian flexus. Lingual flexi transverse and labial flexi oblique respect to the longitudinal axis of the molar. M2 is “S” or “Z”-shaped, with a deep and oblique mesoflexus, and without anteroflexus. M3 with a deeply excavated hypoflexus, sometimes forming a lake. Lower incisors more delicate and yellowish than the upper ones. Young specimens with vestigial anteromedian flexid, and well developed anteroflexid and posteroflexid in m1. Anterolabial cingulum well developed, coalescing with the protoconid in adult specimens, and isolating the protoflexus. Protoflexid and posteroflexid of m2 reduced in young specimens. The m3 is large, slightly smaller than m2.

Phyllotis nogalaris has 13 thoracic ribs and 7 cervical, 13 thoracic, 8–9 lumbar, and 27–34 caudal vertebrae (N = 5 specimens).

Morphologic variability. Studied specimens of Phyllotis nogalaris are uniform in external and skull characters, although minor variation exists. The development of the lateral yellowish-orange sides and the midventral yellowish-orange pectoral streak varies among specimens. In the skull we observe variation in the width of the zygomatic plate and the development of the median spine on the palatine. Similarly, some specimens show a slightly more developed mandibular capsular projection.

Comparisons. Phyllotis nogalaris can be distinguished from P. osilae (as represented by specimens from southern Peru and central Bolivia, from where the nominal subspecies P. osilae osilae and P. osilae phaeus come) by its notably larger size in almost all external and skull measurements (see Pearson 1958; Hershkovitz 1962) ( Table 1 ), more obscure and colored skin, presence of a well-defined yellowish-orange lateral fringe ( Fig. 7 ), lacrimals more developed, broader braincase, deeper and broader zygomatic notches, noticeably more developed median spine on the palatine, broader bony eustachian tubes, molars more robust and hypsodont ( Fig. 3 ), and noteworthy genetic divergence ( Table 5).

Several external and cranial features differentiate Phyllotis nogalaris from P. anitae and P. alisosiensis . P. nogalaris is clearer in general coloration, less dark-grayish in the dorsum and less ochraceous or cinnamon in the venter ( Fig. 7 ). Young specimens of P. anitae have the digits and the distal dorsum of manus and pes white but the proximal dorsum dark, and the tail is only slightly bicolored. The nasolacrimal capsules and the zygomatic notches are less developed in P. anitae and P. alisosiensis . P. anitae and P. alisosiensis also have molars with stronger degree of hypsodonty, which differentiate these species from P. nogalaris ( Fig. 3 ; see also Fig. 4 in Ferro et al., 2010). Genetic divergence between P. nogalaris and P. anitae is 11.0 % and between P. nogalaris and P. alisosiensis is 11.2 %.

P. tucumanus s.s. is broadly distributed in southernmost NWA, occupying many different habitats. Across its distribution, this form is morphologically highly variable ( Fig. 4 ). Specimens coming from high altitudinal grasslands are easily differentiated from P. nogalaris in the skin coloration pattern, being notably clearer and with weaker tinges; but in populations from the humid eastern slopes, in the ecotone area between the high altitude grasslands and Yungas forest, skins are similar to those of P. nogalaris . Notwithstanding, P. nogalaris has broader rostrum and braincase, and a proportionally narrower interorbital constriction. Additionally, molars of P. nogalaris are notably more robust, laminated and hypsodont.

Skins of P. nogalaris and representatives of Phyllotis coming from the Centinela range ( Phyllotis tucumanus form 2) are practically indistinguishable at first glance, sharing the intense and dark general hue. However, in P. nogalaris the fur is dense and softer, with longer hairs and with a greater prevalence of black guard hairs, making the fur comparatively more grayish. Instead, in P. tucumanus form 2 the general coloration is more ochraceous, and the hairs are shorter and less dense. Morphometric values for the skull of these two forms are also similar ( Table 2 and Fig. 4 ), but some characters allow differentiating them. Phyllotis nogalaris has narrower and shallower zygomatic notches, lacrimals somewhat larger, and a well-developed median spine in the mesopterygoid fossa always present. Furthermore, the zygomatic plate of P. tucumanus form 2 shows a tiny spiny process on the free upper border, feature not seen in the examined series of P. nogalaris . All the specimens referred to P. tucumanus form 2 come from small patches of high altitude grassland intermingled with forests of Alnus acuminata on an isolated eastern range, separated for more than 100 km of Yungas and Chaco lowland forested areas from the Zenta range, where P. nogalaris distributes (see Fig. 5 ).

Compared to the sympatric P. tucumanus form 3, P. nogalaris has a more dense fur, with longer and darker hairs, more contrasting eye-ring, more orange flanks, and more ochraceous venter. Furthermore, P. nogalaris is in average larger in most of the analyzed morphometric variables, with the molar series and the interlacrimal distance conspicuously longer. Notwithstanding, P. nogalaris has a proportionally narrow zygomatic plate and short incisive foramina. Although both forms were registered at the same locality, they occupy different microhabitats, with P. nogalaris being trapped exclusively on humid and forested patches and P. tucumanus form 3 only caught in open environments dominated by dense grasslands interspersed with rocky outcrops.

Specimens referred to P. tucumanus form 4 (coming from Rodeo Pampa, northernmost Salta province) have the clearest skin among the species here studied. Compared with P. tucumanus form 4, the fur of P. nogalaris is denser, having longer hairs, more colored by a higher prevalence of black guard hairs, showing a more developed eye ring, and more conspicuous lateral and pectoral orange fringes. The tail is darker in P. nogalaris , having a blackish ventral distal end, feature not seen in P. tucumanus form 4. The skull of P. nogalaris is clearly more robust, with a broader rostrum, more flared zygomatic arches and more inflated braincase. In P. nogalaris the zygomatic notch is in general broader and deeper, lacrimals are more robust, and nasals extend further back than in P. tucumanus form 4. Many other anatomical structures are more developed in P. nogalaris , including a larger tympanic bulla, a broader mesopterygoid fossa, and larger, more robust and hypsodont molars. However, P. tucumanus form 4 shows a comparatively broader interorbital constriction, a relatively broader zygomatic plate, and a more robust tympanic hook. Populations of these species also occupy different environments, with Phyllotis tucumanus form 4 occurring in open areas of highland grasslands and P. nogalaris found only in forested patches.

Other species of Phyllotis that do not belong to the P. osilae species group and are present in NWA, as P. xanthopygus and P. caprinus , are clearly distinguishable from P. nogalaris in external, cranial, dental and genetic characters, and they will not be compared here (see Pearson, 1958 for morphologic comparison).

Distribution. Phyllotis nogalaris was only known from a few localities in Jujuy province at the southern end of the Zenta range, on the Cordillera Oriental orographic system (e.g., Pearson, 1958; Díaz & Barquez, 2007). Here we record the species for Salta province, in central areas of the same mountain range. Some authors mentioned nogalaris (as a subspecies of P. osilae ) for additional areas. Jayat & Pacheco (2006) and Jayat et al. (2007) assigned specimens from Centinela range to nogalaris but these belong to a putative undescribed form (see below). Díaz & Barquez (2007) assigned specimens from dry Puna environments, above 3700 m, to nogalaris ; several of these specimens were later re-identified by Jayat et al. (2007) as P. xanthopygus . Díaz & Barquez (2007) also referred two specimens from El Duraznillo, Jujuy province, to nogalaris . We have not examined those specimens but the environmental characteristics of El Duraznillo are similar to that of areas where P. nogalaris was in fact collected. Heinonen & Bosso (1994) suggested the possibility that specimens of Phyllotis from Selva Montana environments of the Calilegua National Park belong to nogalaris .

Natural history. Phyllotis nogalaris preferentially inhabits the upper-forested belts of the Yungas, from the Selva Montana at 1200 m to the Bosque Montano-Pastizales de Neblina transition at almost 3100 m. Thomas (1921) nominated P. nogalaris because the type specimens were caught in areas with “nogales” ( Juglans australis ). However, other records come from alder forests ( Alnus acuminata ) and Polylepis woodlands intermingled with high altitudinal grasslands (e.g., Festuca , Pennisetum , Stipa ). Specimens from Quebrada Alumbriojo were obtained from Polylepis woodlands on a humid ravine near a mountain stream; understory was characterized by rocky outcrops and grasslands mixed with several species of ferns. Specimens from Abra de Ciénaga Negra were also obtained on forested areas, but situated on more humid easternmost slopes of Zenta range, where Alnus acuminata was the dominant tree species.

None of the seven specimens (three males and four females) caught in Quebrada Alumbriojo in June showed signs of reproductive activity, and only one was molting. Two males captured at Abra de Ciénaga Negra in November were molting and showed semi-scrotal testes.

Comments. Even after removing Phyllotis nogalari s, data at hand suggest that specimens currently assigned to P. osilae in NWA may encompass more than one biological species. Our sampling includes haplotypes from several localities of Argentina, Bolivia, and Peru ( Fig. 5 ). Results show deep genealogical diversity that is mostly geographically structured and that is congruent with the observed pattern of morphological variation. Haplotypes recovered from specimens from southern Peru and northern Bolivia, which can be assignable to P. osilae , form a well-supported clade ( Fig. 2 ) sister to a clade formed by haplotypes of individuals from southern Bolivia and all NWA ( P. tucumanus s.l., Fig. 2 ); haplotypes of both clades diverge on average by 6.4 %. Given this result and the geographic segregation of both clades, even when noting that in our sampling there is a gap between both clades, it seems reasonable to limit P. osilae to the northern clade. This suggestion implies that P. osilae does not occur in Argentina.

The name tucumanus , coined by Thomas (1912) as Phyllotis darwini tucumanus on the base of specimens collected at Cumbres de Mala Mala, Tucumán province, is available for the southern clade ( Fig. 2 ). The name P. lutescens Thomas , also included in the synonymy of P. osilae ( Musser & Carleton 2005; Steppan & Ramirez, 2015), has priority over tucumanus ; but this name is based on specimens from Cochabamba, Bolivia, a locality distant from the known distribution of the southern clade. In this context, the southern clade could be referred as P. tucumanus s.l. We refer as to P. tucumanus s.s. one of the four morphologically distinct subclades ( Figs. 2 and 4 ) that composes the large P. tucumanus s.l. clade. The three other forms, here referred as P. tucumanus form 2, P. tucumanus form 3, and P. tucumanus form 4 (see appendix and Fig. 2 ) show deep genetic divergences ( Table 5) and clear differences in morphologic and morphometric characters among them and respect to P. osilae and P. nogalaris . Notwithstanding the noteworthy pattern of morphologic and genetic variation, we consider that a geographically larger sample as well as other genes (i.e. nuclear markers) must be analyzed before these unnamed forms are formally recognized.

The taxonomic status of Phyllotis alisosiensis , recently described on base of a small sample from the upper montane forest of the Yungas on the Aconquija range, Tucumán ( Ferro et al. 2010), needs re-evaluation. This nominal form is genetically and morphologically very similar to P. anitae , which ranges in the same area and inhabits the same Yungas environment. Sequenced specimens from these nominal forms diverge in less than 1.3%, a value well below the average observed genetic divergence for other pairs of species of Phyllotis and in line to intraspecific values ( Table 5). The few morphological characteristics that differentiate both forms must be taken with caution given the limited number of specimens in which both nominal forms were based and because the type material of each form belong to different age classes. A more detailed examination about the likely synonymy of these nominal forms is also under development (Jayat et al., in prep.).

Biogeography. The complex picture showed by our research for populations from NWA of the Phyllotis osilae species group may seem surprising. The diversity here uncovered may be the result of the tight association of the P. osilae species group with the high altitude grasslands and their ecotones ( Fig. 5 ). These grasslands form isolated patches at the top of the mountain ranges, in which populations of Phyllotis would have differentiated prompted by the cyclical grassland expansions and retractions related to climatic events that these systems undergone during the late Cenozoic ( Ortiz et al. 2011 and references therein). A similar scenario has been suggested for other species at the light of paleontological (e.g., Ortiz et al. 2000; Ortiz & Pardiñas, 2001), phylogenetic and phylogeographic analyses (D’Elía et al. 2008).

More in general, the complex physiographic and environmental features of NWA coupled with its unique biogeographic history surely have constituted a major driving force for the striking sigmodontine diversity of the region. A recent account mentioned at least 50 species for this relatively small area ( Jayat et al. 2011a), many of which are environmentally restricted and thus, confined to narrow distributional ranges (e.g., Jayat et al. 2007, 2008a; Mares et al. 2008; Teta et al. 2011). However, as shown in the present study, considerable uncertainties still remain regarding such basic subjects as species boundaries, identity and distribution, while most of the area and environments still are to be appropriately surveyed ( Jayat et al. 2011a, b). We expect that during the next coming years a significant improvement in the knowledge of NWA small mammal assemblage will be accomplished, with the recognition of new entities and the synonymy of others (e.g., as preliminary indicated here for P. xanthophygus and its associated form caprinus ; Fig. 2 ).

Figures

FIGURE 2 Genealogical relationship of 56 haplotypes recovered from specimens of Phyllotis and eight haplotypes of representatives of the other eight phyllotine genera obtained in a Bayesian analysis (see text for details). Numbers at branches indicate Bayesian posterior probability values (left to the diagonal) and Maximum Likelihood Bootstrap proportions (right to the diagonal). A less-than sign (<) indicates that the given clade receives less than 50 % of Bootstrap support in the Maximum Likelihood analysis. A dash (-) indicates that in the Maximum Likelihood analysis that clade was not recovered. For haplotypes retrieved from Genbank, catalogue and accession numbers are shown in haplotype labels. For haplotypes generated by us catalogue numbers are shown in haplotype labels and accession numbers in the Appendix.

FIGURE 3. Dorsal, ventral, and lateral views of skulls in three species of the Phyllotis osilae species group: P. nogalaris (JPJ 2186; a, d and g), P. o. osilae (AMNH M- 16503, holotype; b, e and h), and P. anitae (JPJ 924; c, f and i). Scale bar = 10 mm.

FIGURE 4. Individual specimen scores based on log-transformed values of 20 cranial measurements, projected onto the first and second principal components extracted from analysis of young specimens (age classes 2 and 3, n = 74) of Phyllotis nogalaris and 4 forms of P. tucumanus in Northwestern Argentina: P. nogalaris (white squares), P. tucumanus s. s. (black squares), P. tucumanus form 2 (white diamonds), P. tucumanus form 3 (white triangles), and P. tucumanus form 4 (white circles). Character loadings and percentage of variance explained by each of three PCs in Table 3.

FIGURE 5. Map of central Andes in South America. A. Collection localities of the sequenced specimens of the Phyllotis osilae species group used in this study. Stars indicate type localities of the nominal forms of this species group. B. Collection localities and approximate distribution of the species in the Phyllotis osilae species group as recognized in this study.

FIGURE 6. Left upper (a) and left lower (b) molar rows in a young specimen (age class 2) of Phyllotis nogalaris.

FIGURE 7. Dorsal, lateral, and ventral views of skins in three species of the Phyllotis osilae species group: P. o. osilae (MACN 50.352; a, b and c), P. anitae (JPJ 924; d, e and f), and P. nogalaris (MACN 26378; g, h and i).