Zootaxa, Rediscovery of Juliomys pictipes (Rodentia ...

Zootaxa 1758: 29–44 (2008) www.mapress.com / zootaxa/

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ZOOTAXA

Rediscovery of Juliomys pictipes (Rodentia: Cricetidae) in Argentina: emended diagnosis, geographic distribution, and insights on genetic structure ULYSES F. J. PARDIÑAS1, PABLO TETA2,5, GUILLERMO D’ELÍA3 & CARLOS GALLIARI4 1

Centro Nacional Patagónico, Casilla de Correo 128, 9120 Puerto Madryn, Chubut, Argentina [email protected] Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Avenida Intendente Cantilo s/n, Ciudad Universitaria, Pabellón II, 4º Piso, C1428EHA Buenos Aires, Argentina 3 Departamento de Zoología, Universidad de Concepción, Casilla 160-C, Concepción, Chile 4 Centro de Estudios de Parásitos y Vectores, Calle 2 nº 584, 1900 La Plata, Argentina 5 Corresponding author:[email protected] 2

Abstract Juliomys pictipes, the type species of this sylvan cricetid genus, remains poorly known. In Argentina, country where the type locality is placed, it is only known from the holotype. Here we report the first new Argentinean individuals, after a gap of 80 years; the new specimens -three in total- include one topotype and allow adding two new recording localities for the species. In addition, we refined the geographical location of their type locality and described in detail several morphological traits of this peculiar mouse, producing an emended diagnosis of both the type species and the genus. Molecular data provided in this paper reinforce the identity of J. pictipes and the reference of the southern Brazilian populations of this genus to the type species. Key words: Argentina, Brazil, Atlantic forest, Sigmodontinae, taxonomy

Resumen Juliomys pictipes, la especie tipo de este género de cricétidos selváticos, permanece pobremente estudiada. En Argentina, país en el cual se emplaza su localidad típica, es conocida solamente por el holotipo. Aquí damos a conocer los primeros nuevos ejemplares argentinos luego de un lapso de 80 años; los nuevos especímenes –tres en total- incluyen un topotipo y permiten adicionar dos nuevas localidades de registro para la especie. Adicionalmente, nosotros clarificamos la ubicación geográfica de su localidad típica y describimos en detalle diversos rasgos morfológicos de este particular roedor, generando diagnosis enmendadas tanto para la especie tipo como para el género. Los datos moleculares brindados en este artículo robustecen la identidad de J. pictipes y la referencia a la misma de las poblaciones del género que ocurren en el sudeste de Brasil. Palabras clave: Argentina, Brasil, Selva Atlántica, Sigmodontinae, taxonomía

Introduction Juliomys includes three species of arboreal mice endemic to the Atlantic forest (Costa et al., 2007). Its distribution ranges from Minas Gerais and Espírito Santo in southeastern Brazil (ca. 20ºS) to the province of Misiones, in northeastern Argentina (ca. 27º 30’S; Osgood, 1933; Costa et al., 2007). The type species of the genus is J. pictipes, originally described by Osgood (1933) as Thomasomys pictipes. For several decades, the generic placement of this form was uncertain. Pine (1980) maintained it within Thomasomys, while Musser Accepted by P. Cordeiro-Estrela: 5 March 2008; published: 28 Apr. 2008

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and Carleton (1993) assigned pictipes to Wilfredomys Avila-Pires, on the assertions of Osgood (1933) and Pine (1980) that pictipes would be closely related to T. oenax, type species of Wilfredomys. Massoia et al. (1991), in a strongly departing position, included pictipes in the synonymy of Oligoryzomys flavescens antoniae. Finally, González (2000) erected the genus Juliomys to allocate pictipes. The phylogenetic position of Juliomys within Sigmodontinae remains uncertain; Smith and Patton (1999) and D’Elía (2003) pointed out that this genus cannot be unambiguously placed into any suprageneric group less inclusive than Sigmodontinae. Recently, Steppan et al. (2004) erected within Sigmodontinae the supratribal Oryzomyalia; Juliomys belongs to this clade (see D’Elía et al., 2006). Since the description of Juliomys, the genus remained monotypic until the description of J. rimofrons by Oliveira and Bonvicino (2002). In addition, an undescribed species, referred as Wilfredomys sp. by Patton and Smith (1999) and as Juliomys sp. by Oliveira and Bonvicino (2002), was recently described as J. ossitenuis by Costa et al. (2007). The confusion on the generic placement of pictipes was partially caused by the scarcity of specimens to study until the decade of 2000. On the contrary, by now, several ecological studies suggest that J. pictipes is a relatively frequent species in some forested areas of southeastern Brazil (e. g., Vieira & Monteiro-Filho, 2003; Neri-Bastos et al., 2004; Pardini & Umetsu, 2006; Umetsu et al., 2006). However, Argentinean specimens remain elusive and until now only one specimen, the holotype of the species, is know. On the basis of recently collected Argentinean specimens, including one from the type locality, in this paper we present new data on morphology, genetic variation, habitat use, and distribution of J. pictipes. In addition, we provide emended diagnoses of Juliomys and J. pictipes.

Material and methods Two specimens were obtained by us using sherman-like traps baited with oat placed on ground in the interior of sylvan environments. In addition, one specimen housed in a collection but erroneously identified as Oligoryzomys nigripes, for which no data on the method of collection is available, was examined. Morphological descriptions follow the concepts detailed by Carleton (1980), Voss (1988), Carleton and Musser (1989), and Weksler (2006). Measurements include standard external dimensions recorded in the field by the authors or taken from museum tags, and several cranial and dental descriptors taken following Tribe (1996) in order to make comparable our data to those of Oliveira and Bonvicino (2002) and Costa et al. (2007). Acronyms for institutions and collections mentioned in the text and tables are: CIES, Centro de Investigaciones Ecológicas Subtropicales, Puerto Iguazú, Misiones, Argentina; CNP, Colección de Mamíferos del Centro Nacional Patagónico, Puerto Madryn, Chubut, Argentina; FMNH, Field Museum of Natural History Mammal Collection, Chicago, USA; MLP, Museo de La Plata, Buenos Aires, Argentina. Genetic variation and phylogenetic analyses were based on cytochrome-b (cyt-b) gene sequences. One Argentinean specimen (MLP 1.I.03.24) of J. pictipes was sequenced following the protocol detailed in D’Elía and Pardiñas (2004) and was deposited in GenBank (EU157764). The dataset was completed with all cyt-b sequences of Juliomys available in GenBank as of June 2, 2007. All specimens genetically analyzed and the source and length of their cyt-b sequence are listed in Table 1. Sequence alignment was done with the program Clustal X (Thompson et al., 1997) by using the default values for all alignment parameters and verified by eye. Observed (p) sequence divergence was estimated with PAUP* (Swofford, 2000) ignoring those sites with missing data. Aligned sequences were subjected to maximum parsimony (MP; Farris, 1982) and likelihood (ML; Felsenstein, 1981) analyses. To root the tree we included as outgroups (Nixon and Carpenter, 1993) haplotypes of Abrothrix, Akodon, Euneomys, Irenomys, Oryzomys, Phyllotis, Reithrodon, Thomasomys, and Wiedomys, type genera of the tribes of Oryzomyalia or that closely related to Juliomys (see D’Elía, 2003; D’Elía et al., 2006). In the MP analysis characters were

30 · Zootaxa 1758 © 2008 Magnolia Press

PARDIÑAS ET AL.

treated as unordered and equally weighted. PAUP* was used to perform 200 replicates of heuristic searches with tree bisection-reconnection branch swapping and random addition of sequences. Two measures of clade support were calculated. We performed 1,000 parsimony jackknife (JK; Farris et al., 1996) replications with 5 addition sequence replicates each and the deletion of one-third of the characters. Clades with < 50% of support were allowed to collapse. For each node we computed in PAUP* Bremer support values (BS; Bremer, 1994) using a command file written in TreeRot version 2 (Sorenson, 1999). ML analysis was conducted on Multiply a high-throughput phylogenomics webserver (Keane et al., 2007). Clade support was measured by 100 replicates of bootstrap. The DNA evolutionary model used (GTR+I+G with the following parameters: percentage of invariable sites = 0.48; gamma distribution shape parameter = 0.88) was selected using the Akaike Information Criterion 2 (AIC2 = 10553.498444196177) in ModelGenerator (Keane et al., 2006). Base frequencies were as follows: freq(A) = 0.30662, freq(C) = 0.31428, freq(G) = 0.11884, and freq(T) = 0.26026. Substitution rates were: A-C = 3.86, A-G = 6.28, A-T = 2.54, C-G = 0.27, C-T = 22.43, and G-T = 1. The expected transition/transversion ratio was 3.36 and the expected pyrimidine transition/purine transition ratio was 8.02. TABLE 1. Haplotypes, with their Genbank accession numbers and length, used in the genetic and phylogenetic analyses. The numbers between brackets correspond to those in the Fig. 2. Species

Accession number

Length (bp)

1

Juliomys ossitenuis

EF127518

801

2

Juliomys ossitenuis

AF108689

801

3

Juliomys ossitenuis

EF127522

721

4

Juliomys ossitenuis

EF127521

565

5

Juliomys ossitenuis

EF127520

720

6

Juliomys ossitenuis

EF127519

760

7

Juliomys ossitenuis

EF127517

792

8

Juliomys ossitenuis

EF127516

792

9

Juliomys pictipes [13]

EF127515

441

10


EF127514

801

11


EF127513

801

12


AF108688

801

13


EU157764

801

14

Juliomys rimofrons

AY029477

711

15

Juliomys rimofrons

AY029476

720

Outgroup 16

Abrothrix longipilis

U03530

801

17

Akodon boliviensis

M35691

801

18

Euneomys chinchilloides

AY275115

801

19

Irenomys tarsalis

U03534

801

20

Oryzomys palustris

DQ185382

801

21

Phyllotis xanthopygus

U86832

801

22

Reithrodon auritus

AY275129

801

23

Thomasomys aureus

U03540

801

24

Wiedomys pyrrhorhinos

AY275134

801

REDISCOVERY OF JULIOMYS PICTIPES

Zootaxa 1758 © 2008 Magnolia Press ·

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Results and discussion Available phylogenetic analyses covering the three species of Juliomys strongly support the monophyly of the genus, but disagree on the relationships among the three species. Oliveira and Bonvicino (2002) found a clade composed by J. rimofrons and J. ossitenuis, of which J. pictipes is sister. Meanwhile, Costa et al. (2007) found that J. ossitenuis is sister to a clade formed by the other two Juliomys. Our MP topology differs from these two in that J. rimofrons is sister to the clade composed by J. ossitenuis and J. pictipes (Fig. 1); while our ML topology (-ln L = 5128.511) resembles that of Costa et al. (2007). Given our results, it is clear that the topological differences among the studies are not caused only by the marked differences on taxonomic coverage (i.e, amount of Juliomys haplotypes and the included outgoups) of the different studies. The three main lineages (i.e., species) of Juliomys are genetically very distinct, and the three are relatively equidistant to each other. On average, observed differences between haplotypes of J. ossitenuis and J. pictipes is 11.7 %, between haplotypes of J. ossitenuis and J. rimofrons is 12.0 %, and between J. pictipes and J. rimofrons is 12.9 %. This fact, together with the large genetic distance between Juliomys and the other sigmodontines (19.1 % for our matrix), probably causes the differences observed in the placement of the root of the Juliomys tree. We expect that the analysis of nuclear gene sequences shed new light on the relationships among the species of Juliomys.

FIGURE 1. Strict consensus tree of the 300 most parsimonious trees (length 1048 steps, CI = 0.483, RI = 0.606) obtained in the maximum parsimony analysis of the cytochrome b gene sequences. Numbers above branches indicate parsimony jackknife (left), Bremer support (middle), and maximum likelihood bootstrap (right) values of the nodes to their right. Only jackknife and bootstrap values > 50 % are shown. * indicates that the node in question was not recovered in the maximum likelihood analyses; in that analysis J. rimofrons and J. pictipes are sister to each other but with less than 50 % of support.

Juliomys González, 2000 Type species. Juliomys pictipes (Osgood, 1933). Included species (in order of nomination). J. pictipes (Osgood, 1933), J. rimofrons Oliveira and Bonvicino, 2002; J. ossitenuis Costa, Pavan, Leite and Fagundes, 2007. Emended diagnosis. Small to medium Sigmodontinae rodents (total length ~ 200, Occipto-nasal length ~ 27) with large head, conspicuous eyes, and tail equal or slightly larger than head and body; dorsal pelage soft


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dark-brown to light-orange brown; feet rather short and broad with 6 plantar pads and scutelated surface; skull with short rostrum (< 35% Occipto-nasal length), rounded braincase, and rather posterior domed profile; nasals divergent forward; interlacrymal depression behind nasals; anterior portion of interfrontal suture with incomplete fusion or directly slit-like fontanelle; zygomatic plate nearly vertical with almost obsolete upper free border; coronal suture V-shaped; interparietal wide; occipital region reduced; mesopterygoid fossa lireshaped with anterior border located at the level of third molar protocone; robust opisthodont upper incisors; brachyodont molars with crested coronal topography and well developed anteromedian flexus/ids and mesolophs/ids; 8 mammae. Fossil record. No fossil of Juliomys is known.

Juliomys pictipes (Osgood, 1933) Holotype. FMNH 26814, adult male (skin and skull) collected by C. C. Sanborn on Sept. 6, 1926. Photographs (skull and mandible) of this individual were recently published by Costa et al. (2007: figs. 4 and 5). Type locality. “Caraguatay, Rio Parana, 100 miles south of Rio Iguassu, Misiones, Argentina” (Osgood, 1933:11). The exact location of this type locality was recently addressed by Pardiñas et al. (2007:397). These authors, taking into account the most probable route followed by C. Sanborn and the fact that he worked in Misiones’ Charles Benson property (see Field Museum of Natural History - Reports, 1927), restricted it to Puerto Caraguatay (26º 37’ S, 54º 46’ W, Department of Montecarlo, Province of Misiones). However, in a recent inspection of this area, Mr. Benitez, an old resident of the area and with a good knowledge of it, showed us (UFJP and CAG) the exact place where the original house of Mr. Benson was emplaced. The main building is now in ruins and practically subsumed by the forest. Clearly, this is not Puerto Caraguatay, instead Puerto Benson with coordinates 26º 37’ 13” S and 54º 46’ 57” W and probably Sanborn trapped around there. Despite those findings, the extreme proximity of these two localities (ca. 0.5 km), the missing of Puerto Benson as toponomy, and the ambiguity around the exact place where Sanborn worked, support our restriction of the type locality of J. pictipes to Puerto Caraguatay. Distribution (Fig. 2). J. pictipes is restricted to tropical and subtropical moist forests of the Atlantic coast in southeastern Brazil and in interior subtropical moist forests of Argentina (Osgood, 1933; Pine, 1980; Costa et al., 2007). New Argentinean specimens (Fig. 2). CIES-M 23, adult female preserved as skin in poor condition and skull, originally identified as Oligoryzomys nigripes. Collected by Silvana Montanelli in Sendero Macuco, Parque Nacional Iguazú (25º 41’ S, 54º 26’ W, Department of Iguazú, Province of Misiones). CNP 895, young female, preserved as cleaned skull, carcass in fluid and digestive, collected by Ulyses Pardiñas and Rosario Robles (original number LTU 379) in Arroyo de Salamanca, Parque Provincial “Ernesto Che Guevara” (26º 36’ 53” S, 54º 46’ 51” W, 147 m asl, Department of Montecarlo, Province of Misiones). MLP 1.I.03.24, adult pregnant female (3 fetus) preserved as complete fluid, except digestive organs, collected by Graciela Navone and Juliana Notarnicola on 28 August 2006 (original number JN 702) in Balneario de la Reserva Privada de Usos Múltiples de la Universidad Nacional de La Plata “Valle del Arroyo Cuña Pirú” (27º 05’ S, 54º 57’ W, Department of Cainguas, Province of Misiones). Emended diagnosis. The largest known species of Juliomys, characterized by the following combination of traits: body markedly bicolored light orange-brown above and white to cream-white below; tail slightly shorter than head-body length; tail bicolor except for the terminal half-inch, which is dusky all around; feet clear ochraceous-twany, the toes whitish; zygomatic notch moderately expressed; upper free border of the zygomatic plate reduced; incisive foramina short, not reaching the first upper molars; lateral expansion of frontal bones restricted; tympanic bulla small, squamosal-alisphenoid and sphenofrontal foramen absents, sphenopalatine vacuities absents or reduced to a narrow fissures, 2n = 36.



33

FIGURE 2. Recording localities of Juliomys pictipes: ARGENTINA: MISIONES: 1. Parque Nacional Iguazú; 2. Parque Provincial “Ernesto Che Guevara;” 3. Reserva Privada de Usos Múltiples de la Universidad Nacional de La Plata “Valle del Arroyo CuZa Pirú”; BRAZIL: SmO PAULO: 4. Buri; not specific locality provided; 5. Mulheres and Museros; 6. Fazenda Sakamoto, Campinho; Fazenda Sakamoto, Portão; Fazenda Intervales; 7. Fragmento Citadini; Fragmento Divisa; Três Quedas; Moacir; Paraguai; Cogumelo; 8. Floresta Nacional de Ipanema, 20 km NW Sorocaba; 9. Piedade, not specific locality provided; 10. Reserva Florestal do Morro Grande, Caucaia do Alto; 11. Riacho Grande; 12. Parque Natural Municipal da Serra do Itapety; RIO DE JANEIRO: 13. Mata do Mamede; 14. Fazenda Boa FJ; MINAS GERAIS: 15. Reserva Particular do Patrim^nio Natural do CaraHa, 25 km SW Santa Barbara; 16. EstaHão de Pesquisa e Desenvolvimento Ambiental de Peti. The grey area represents the approximate cover of the Atlantic Forest.

Description. Based on the new Argentinean specimens. A small-sized sigmodontine rodent, externally similar to Oligoryzomys nigripes, but with the head and eyes proportionally larger and with a shorter tail that is nearly equal to head and body (Fig. 3). Dorsal hairs are plumbeous gray at the base and distally reddish. Over hairs on the rump and hind legs are vivid orange at the tip, contrasting with the rest of the body. The venter is covered by bicolored hairs; each hair has a short gray base and is withish at the tip. Orange tipped hairs are visible in the inguinal region around the tail base. The philtrum, genal zone, and chin are covered by whitish hairs. Hairs around the nose are short and orange, contrasting with the rest of the body. The ears are small, covered mainly with short and sparse brownish hairs externally and mostly naked internally; the ear border is covered by short reddish hairs. Mystacial vibrissae are blackish, relatively short anteriorly, and long posteriorly, the latter largely extended beyond the posterior border of the ears. The supercilliary and genal vibrissae are thinner, blackish, and shorter than mystacial, and not surpassing the posterior border of the ears. The tail pelage is sparse, gradually becoming denser toward the tip, where a short tuft is visible. Hairs from proximal and distal halves of tail reach 2–3 scales and 3–6 scales, respectively, with three hairs emerging from each scale. Tail hairs are brown on the dorsum and rufous in the venter, except in the distal tip, which is uniformly brown. Eight mammae are present in a pregnant female examined (MLP 1.I.03.24) that are arranged in one inguinal, one abdominal, one postaxial and one pectoral pair (see Voss & Carleton, 1993). The hands and feet are short, covered with orange hairs dorsally; the fingers are covered by short white hairs (Fig. 4b). The hallux is much shorter than other pedal digits. Manal and pedal pads boulbous and enlarged, especially those of the distal phalanxes, remembering the pads of arboreal sigmodontine species of the genus Oecomys and Rhipidomys (Hershkovitz, 1960; Rivas & Linares, 2006). Three large and rounded interdigital and two large and mostly


PARDIÑAS ET AL.

ovale carpal pads are present (Fig. 4a). The plantar surface of the hind feet has six bulbous tubercles, four interdigitals and two tarsal. The interdigital ones are nearly ovale and large. The thenar pad is more rounded and smaller than the interdigital tubercles. The hypothenar pad is large and is comma-shaped. The distal edge of the thenar just reaches the proximal edge of the hypothenar and is positioned approximately midway along the sole of the foot (Fig. 4c). The skin between distal pads up to the thenar and hypothenar pad limit is covered by small and rounded scales, while the remainder of the plantar surface is smooth (Fig. 4a, c). The claws on the hind feet are short and darker in color than the skin of the pes. Ungual tufts are grayish-white and large, reaching or slightly surpassing the claws.

FIGURE 3. External aspect (lateral view) of a recently collected Juliomys pictipes from Misiones, Argentina (MLP 1.I.03.24).

The skull is robust with a short rostrum, a rounded braincase and a marked domed profile in its posterior region (Fig. 5,6A-L). The nasals diverge anteriorly, without contrasting expansions and with a slight projection anterior to the incisors, conforming a moderate tube (Fig. 5). The nasofrontal suture is straight but markedly denticulate, positioned anteriorly to the lacrimal level (Fig. 6A). A clear central depression is present in the anterior part of the interfrontal region (Fig. 6E); in addition, in this region the interfrontal suture is slightly open, contrasting with the condition of this suture posterior to the depression which appears clearly closed in adult individuals (Fig. 6B, C). Following Weksler (2006:28, character 22) the interorbital region can be typified as symmetrically constricted with squared supraorbital margins (Fig. 6B, C). The lacrimal bone is large. The coronal suture is V-shaped and the squamosal anterior-upper portion is clearly visible from above over the braincase margins (Fig. 6B). Both parietal and interparietal sutures are meandrous, and the former suture includes supernumerary middle bones (Fig. 6I). The interparietal is wide and broad (Fig. 6I). The occipital region is dorso-ventrally compressed producing a oblique position of the foramen magnum (Fig. 6H). Lateral parietal and lambdoid crests are inconspicuous (Fig. 5). The zygomatic plate is high and narrow showing a much reduced upper free border and having a masseteric tubercle well developed in their base (Fig. 6D). Contrasting with the general solid construction of the skull, the zygomatic arches, well expanded, are gracile (Fig. 5). A moderate postorbital ridge is present. The lateral portion of the parietals is reduced (Fig. 6H). Ventrally, the incisive foramina are wide and moderately long and their posterior ends almost reach the M1 anterior face (Fig. 5, 6G). The palate is bombed and finely foraminate with two posterior palatine foramina and paired posterolateral palatal pits side by side the mesopterygoid fossa anterior region (Fig. 6F). The mesopterygoid fossa is broad and has a lire-shape (Fig. 6F). The mesopterygoid roof is almost totally ossified; the sphenopalatine vacuities remain as narrow fissures (Fig. 6G). The parapterygoid fossae are broad, well ossified, and show the small posterior openings of the alisphenoid canal (Fig. 6G). The anterior ends of the parapterygoid fossae are located at the level of M3 protocones (Fig. 6F). Otic capsules are reduced and auditory meatus are clearly enlarged (Fig. 6J). The carotid canal is big and without pteriotic participation; the stapedial foramen is minute and the petrotympanic fissure absent (Fig. 6J). The tegmen tympani is well developed, superposed to the squa-



35

mosal bone, and partially filling the postglenoid foramen (Fig. 6K). The narrow hamular process is distally spatulated and directly applied on the mastoid (Fig. 6K). The mastoid capsule is small but not flattened with a large mastoid fenestra. Cranial foramina related with cephalic arterial pattern include a well developed oval foramen and a small anterior opening of the alisphenoid canal; the alisphenoid strut is absent, and the same is true for the squamosal-alisphenoid groove while the trough for the masticatory-buccinator nerve is shallow but well expressed (Fig. 6G, K). These traits coupled with the absence of the sphenofrontal foramen characterizing the carotid circulatory pattern 2 of Voss (1988).

FIGURE 4. Manus and pes of Juliomys pictipes from Misiones, Argentina (MLP 1.I.03.24): a. Manus, palmar surface; b. Pes, dorsal surface (note the bicolor condition); c. Pes, plantar surface.

The mandible is robust and short (Fig. 7A–B). The anteriormost point of the diastema is well below the alveolar plane (Fig. 7A). The mental foramen is scarcely visible from lateral view. Both upper and lower


PARDIÑAS ET AL.

ridges of masseteric crest are clearly expressed; the same is true for the capsular projection of the incisor. The angular process is short with respect to the condyloid process (Fig. 7B).

FIGURE 5. Lateral, dorsal and ventral views of the skull of Juliomys pictipes (CIES-M 23) from Misiones, Argentina (scale = 5 mm).

Upper incisors are robust and deep, opisthodont, with bright orange frontal enamel. Both upper and lower molars are brachyodont, crested and with the main cusps slightly alternate. M1 (Fig. 6L): subrectangular in outline; main cusp slightly alternating; procingulum almost wide as the remainder portion of the tooth; deep and penetrating anteromedian flexus with their fund engulfed producing two conules being the lingual smaller than labial one; anteroloph and mesoloph transverses in orientation with their labial tips spatulated and showing medium point-connections to the anterior structures (anterolabial conule and paracone, respectively) like displaced paralophules; short posteroloph transverse in orientation; very wide and penetrating protoflexus, subequal in morphology to hypoflexus; protostyle and enterostyle present, the latter with a short enteroloph (developed also in the young individual CNP 895). M2: subcuadrangular in outline; gross morphology very similar to the M1 comparable portion; main cusp something more alternating than M1. M3: about 0.7 of the M2 length; anteroloph conspicuous. Lower molars are crested and the main cusp slightly alternating. m1: procingulum wide; anteromedian flexid well developed producing subequal conulids; anterolophid transverse in orientation with tendency to fusion to anterolingual conulid; protoflexid externally obliterate by a sharp anterolabial cingulum; mesolophid narrow but independent and clearly developed well projected lingually; broad hypoflexid showing a small but marked ectostylid. m2: quadrangular in outline and subequal to the m1 comparable portion; mesolophid well developed; ectolophid plus ectostylid. m3: almost large as m2 (0.9);



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hypoflexid flanqued by oblique proto- and hypoconid walls resulting in a triangular outline, with their fund oriented to a bifid structure composed by fused mesolophid plus entoconid; annular posterofossetid. We examined the stomach gross anatomy of one juvenile specimen (CNP 895). The morphology is of the type unilocular hemiglandular (see Carleton, 1973); in this morphology the glandular epithelium from the antrum extends to the corpus, near the esophagus opening (Fig. 8). Measures of the thick intestine and caecum are 3.5 and 1.8 cm, respectively. Measurements. See Table 2. TABLE 2. External and craniodental measurements of Argentinean specimens of Juliomys pictipes. Age classes were defined according to the criteria of Costa et al. (2007). MLP 1.I.03.24

CIES-M 23

CNP 895

FMNH 26814a

3

3

1

3

Total length

205

185

154

197

Tail length

95

95

82

97

18/20

-

18/19.5

-/21

Age class

Hind foot without/with claw Ear length

a

15

-

13

12 (dry)

Weigth (in grams)

-

22

8.5

-

Occipto-nasal length

-

24.82

-

26.30

Palatal length

-

9.34

8.34

-

Postpalatal length

-

9.36

7.91

9.00

Molar row–crown length

-

3.92

3.74

3.90

First molar breadth

-

1.08

1.06

-

Palatal bridge length

-

3.82

3.74

-

Temporal fossa length

-

7.77

6.90

-

Diastema length

-

6.03

5.07

6.50

Incisive foramen length

-

4.43

3.65

4.30

Incisive foramen breadth

-

1.76

1.67

-

Palatal breadth at first molar

-

2.43

1.83

-

Palatal breadth at third molar

-

2.50

2.38

-

Mesopterygoid fossa breadth

-

1.75

1.69

-

Breadth across incisor tips

-

1.66

1.51

-

Bullar width

-

3.28

3.23

-

Bullar length

-

4.11

3.26

-

Braincase breadth

-

11.88

10.64

12.30

Skull height

-

7.86

6.97

-

Rostral height

-

4.68

4.26

-

Rostral breadth

-

4.15

3.87

-

Rostral length

-

6.86

-

-

Nasal length

-

8.04

-

9.00

Zygomatic plate length

-

2.29

1.71

2.50

Zygomatic breadth

-

13.23

-

14.40

Interorbital breadth

-

4.19

3.76

4.50

Greatest length of mandible

-

12.63

11.47

-

Mandibular molar row–alveolar length

-

4.02

3.90

-

Depth of ramus

-

3.08

3.00

-

Holotype; measurements taken from Osgood (1933:12)


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FIGURE 6. Selected cranial traits in adult (except noted) Juliomys pictipes (CIES-M 23). A. Rostrum in dorsal view: note the inconspicuous zygomatic notches and broad zygomatic root; B. Interorbital region: the arrow indicates incomplete fusion in the anterior part of the interfrontal suture; C. Interorbital region in a juvenile specimen (CNP 895); D. Rostrum in lateral view: note the almost absence of upper free border in the zygomatic plate; E. Interfrontal depression; F. Mesopterygoid fossa; G. Palatal and postpalatal region of a juvenile specimen (CNP 895): note the complete ossification of the mesopterygoid fossa roof; H. Temporal region; I. Braincase; J. Auditory capsule: note the extension of the meatus; K. Squamosal-alisphenoid region; L. Upper first molar detail: note the crested corona and the well developed mesoloph. Abbreviations: acl = anterior opening alisphenoid canal, bu = auditory capsule, cc = carotid canal, d = interfrontal depression, f = frontal, fo = foramen ovale, i = interparietal, m = maseteric tubercle, M1 = first upper molar, M2 = second upper molar, M3 = third upper molar, ma = meatus, mb = trough for masticatory-buccinator nerve, mf = mesopterygoid fossa, ms mesoloph, mt = mastoid, mx = maxilla, na = nasal, oc = occipital, p = lateral portion of the parietal, pa = parapterygoid fossa, pm = premaxilla, ppp = postpalatal posterolateral pit, pr = parietal, r = zygomatic root, sb = supernumerary bone, sq = squamosal, t = tegmen tympani, zp = zygomatic plate.

Habitat. All specimens were collected in the Interior Atlantic Forest of the Misiones Province, Argentina. This biotic unit, also known as “Selva Paranaense,” is part of the South American Atlantic Forest macroregion (Plací & Di Bitetti, 2005). Three of four specimens were collected in the vicinity of watercourses of the Paraná river basin. One individual from Sendero Macuco, Parque Nacional Iguazú, was collected in a mature forest of “Laurel and Guatambu” (Martínez-Crovetto 1963), where the predominant arboreal species were Matayba elaeagnoides, Balforoundendron riedelianum, Sorocea ilicifolia, Cordia ecaliculata, and Prumus sphaerocarpa. Dense underbrush vegetation at Sendero Macuco includes the bamboos Merostachys clausseni and Chusquea ramossisima. The individual CNP 895 was collected ca. 2 km of the type locality. The rainforest in this area is highly disturbed by human activities, including wood extraction and timber plantations. In fact, the small provincial park “Ernesto Che Guevara” (18 ha), where the specimen was trapped, constitutes



39

FIGURE 7. Selected mandible traits in adult Juliomys pictipes (CIES-M 23). A. Anterior region of the horizontal ramus: note the depressed position of the diastema anterior point with respect to the alveolar plane; B. Ascending ramus region: note the short angular process. Abbreviations: cp = capsular projection, m1 = first lower molar, m2 = second lower molar, m3 = third lower molar, me = mental foramen, ml = maseteric crest, lower ridge, mu = maseteric crest, upper ridge.


PARDIÑAS ET AL.

FIGURE 8. Stomach of Juliomys pictipes (CNP 895): internal view of the dorsal half. Abbreviations: p: pilorous; ia: incisura angularis; e: esophagus; ce: cornified squamous epithelium; co: corpus; bf: bordering fold; ge: glandular epithelium; a: antrum.

one of the last patches of forests in this area. The mean height of the trees in this place is 10-12 m, with a discontinuous dosel. The vegetal community is dominated by the Lauraceae Ocotea spp. and Nectandra spp. and other tree species like Inga sp., Luehea divaricada, Fagara hyemalis, Peltophorum dubium, and Balfourodendron riedelianum. Vegetation in the underbrush includes dense communities of bamboo Chusquea ramosissima. Finally, the individual MLP 1.I.03.24 was caught in a riverine forest of Ocotea acutifolia and Nectandra megapotamica. The mean hight of the trees in this place is ca. 20 m, with a discontinuous dosel. Other tree species present there include Luehea divaricada, Chrysophyllum marginatum, Balfourodendron riedelianum, Bastardiopsis densiflora, Inga affinis and Peltophorum dubium. At this place, the specimen was caught in dense underbrush of the bamboo Merostachys clausseni. Genetic variation. Only five cytochrome-b sequences of J. pictipes are available; these specimens were collected in one Argentinean and three Brazilian (one in Minas Gerais and two in São Paulo States) localities. Observed genetic variation among these cyt-b haplotypes is moderate; it ranges form 0.3 to 2.3%. In addition, there is not a pattern of isolation by distance. The most distinct haplotype is the one recovered at the Minas Gerais locality and not the one from the Argentinean locality that is the most apart of the four (see Fig. 1). Comparisons involving the haplotype from Minas Gerais and the other J. pictipes haplotypes range from 1.6 to 2.3%, while comparisons between the Argentinean haplotype and the others range from 0.4 to 1.6%. Future studies involving more haplotypes, especially from intermediate localities will test the pattern of genetic structure described here, and explain its biological meaning if any. Conservation status. D'Elía et al. (2006) categorized J. pictipes in Argentina as data deficient. Due to the lack of primary data about J. pictipes natural history and the fragmentary knowledge about its distribution we prefer to maintain this category for the populations in Misiones Province. Globally, J. pictipes was treated by Baillie (1996) as Lower risk, least concern.



41

Final considerations Comparisons among the three recognized species of Juliomys indicate trenchant differences both in morphology as well as karyology and ecological preferences (see discussions in Oliveira and Bonvicino, 2002:315; Costa et al., 2007:29). Juliomys pictipes departs from rimofrons and ossitenuis in several anatomical traits, being the most contrasting ones: carotid circulatory pattern, sphenopalatine vacuities, extension of incisive foramina, condyle morphology, and otic capsules morphology. The diploid complement of J. pictipes (2n = 36; Bonvicino and Otazu, 1999) also differs radically with respect of both rimofrons and ossitenuis (2n = 20; Costa et al., 2007:33). In addition, rimofrons and ossitenuis appear to be species restricted to altitude environments (> 800 m) whereas pictipes is widely distributed in lowlands. Given the nature of these differences it may be pertinent to erect a new genus to encompass rimofrons and ossitenuis; however, we note that none of our phylogenetic analyses (see above) place these two species as sister to each other. Even when Juliomys pictipes survives in small patches of both primary and old growth secondary forests, it appears to be a rare sigmodontine in southeastern Atlantic forest assemblages (24 to 28ºS). This could be an explanation of the registered gap –roughly 80 years- between the first capture of this species (1926) and our findings. In fact, the Cuña Pirú region was sampled by the authors and colleagues during several years extracting more than 700 specimens of small mammals (see Pardiñas et al., 2003) but only one J. pictipes. However, several lines of evidence suggest that the rarity of J. pictipes in Misiones province is partially an artifact. First, morphological traits displayed by J. pictipes suggest it is an arboreal species. As most of the trapping effort conducted in Misiones has been done with traps set on ground, the chances of capturing J. pictipes are reduced. Second, the main source of information about the small mammal assemblages from Misiones province are osteological remains recovered from owl pellets of Tyto alba (e.g., Massoia, 1993). This owl mainly preys in open environments, where J. pictipes does not live. Third, probably several specimens –especially the fragments recovered from owl pellets- have been wrongly identified as belonging to other similar –in size and external morphology-, abundant and widespread sigmodontines like Oligoryzomys spp. Therefore, to assess the real abundance and distribution of J. pictipes, as well as those of other presumably arboreal and poorly known sigmodontines as Rhagomys rufescens and Abrawayaomys ruschii, the restudy of these owl pellet samples seems necessary. In addition, intense trapping in both substrate and canopy is much needed.

Acknowledgements This contribution was possible thanks to the effort of several people and institutions which freely provided materials, help, data, or funds; all of these are deeply acknowledged by the authors. Graciela Navone and Juliana Notarnicola trapped the specimen from Cuña Pirú. Marcela Lareschi, Juliana Notarnicola, and Rosario Robles enthusiastically helped during the field trip to Caraguatay area. Mr. Benitez and the staff of Parque Provincial “Ernesto Che Guevara” gave useful data and assistance in order to locate the place of “Mr. Benson house.” Silvina Fabbri and Karina Schiaffino permited us the study of specimens housed at CIES. Carolina Abud gathered the DNA sequence of Juliomys working in Enrique Lessa’s lab (Universidad de la República, Uruguay). Finally, Darío Podestá took many of the photographs used in this study. Trappings in Misiones province were authorized by Ernesto Krausuck (Ministerio de Ecología). This research was funded by Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 6179 to U. Pardiñas).

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