Juliomys ossitenuis, Costa, Leonora P., Pavan, Silvia E., Leite, Yuri L. R. & Fagundes, Valéria, 2007

Costa, Leonora P., Pavan, Silvia E., Leite, Yuri L. R. & Fagundes, Valéria, 2007, A new species of Juliomys (Mammalia: Rodentia: Cricetidae) from the Atlantic forest of southeastern Brazil, Zootaxa 1463, pp. 21-37 : 23-32

Juliomys ossitenuis sp. nov.

Fig. 1 , Table 1

Holotype. MN 69752, an adult female, collected on 26 May 1992 by Leonora Pires Costa (original field number LC 23), at Fazenda Neblina, Parque Estadual da Serra do Brigadeiro, 20 km W Fervedouro, Minas Gerais, Brazil, 20°43'S 42°29'W, elevation 1300 m ( Fig. 2 , locality 5). The holotype consists of skin, skull, and liver tissue fixed in ethanol.

Paratypes. MN 69753, an adult female collected by L. P. Costa (original field number LC 25), and UFMG 3174, a subadult male collected by Yuri L. R. Leite (original field number YL 31), both from the type locality and collected on 26 May 1992, consisting of skin, skull, and liver tissue fixed in ethanol; UFMG 3173, an adult female from Fazenda do Itaguaré, 16 km SW Passa Quatro, Minas Gerais, Brazil 22°28'S, 45°05'W, elevation 1500 m ( Fig. 2 , locality 8), collected by L. P. Costa (original field number LC 9) on 30 October 1991, consisting of skin, skull, and liver tissue fixed in ethanol; MZUSP 33170, an adult female, and MZUSP 33171, an adult male, both from Sítio Até Que Enfim, Caucaia do Alto, São Paulo, Brazil, ca. 23°41'S 47°02'W, elevation 900 m ( Fig. 2 , locality 14), collected by Meika A. Mustrangi (original field numbers MAM 139 and MAM 141, respectively) on 20 and 21 August 1993, consisting of skin, skull, partial skeleton. Liver tissue samples fixed in ethanol are cataloged as MVZ 199262 (MAM 139) and 199263 (MAM 141), and the cyt b sequence of MAM 141 ( MZUSP 33171 and MVZ 199263) was reported by Smith and Patton (1999) and is in GenBank (accession AF108689 ).

Etymology. From the Latin words ossi (bone) and tenuis (slender), in reference to the delicate skull and postcranial skeleton of this species.

Diagnosis. Small-bodied sigmodontine rodent with short and soft pelage, dark orange-brown above and cream-white below; nose conspicuously orange, rump and inner pinna with shades of orange ( Fig. 1 ); tail slightly longer than head and body, faintly bicolored, with a small tuft at the tip; hands and feet short and broad, covered with light-orange hairs; skull small and delicate; very shallow zygomatic notch, very large sphenopalatine vacuities, and small posterolateral palatine pits; supraorbital ramus of stapedial artery present (carotid circulation pattern 1 of Voss 1988); mandible small and delicate; molars pentalophodont, ectolophid/ ectostylid of m1–m2 well-developed.

MN 69752 MN 69753 UFMG 3173 UFMG 3174 MZUSP 33170 MZUSP 33171

holotype (F) paratype (F) paratype (F) paratype (M) paratype (F) paratype (M) Description based on the holotype and five paratypes. Dorsal pelage orange-brown composed of ca. 9 mm-long over hairs, gray colored at the base and orange at the tip, and ca. 12 mm-long guard hairs, gray at the base, brown in the middle and yellow distally, gradually turning white toward the tip. Hairs around the nose short, orange, contrasting with the rest of the body ( Fig. 1 ). Over hairs on the rump vivid orange at the tip, contrasting with the rest of the body. Lateral over hairs lighter at the tip than dorsal over hairs. Ventral surface very distinct from the sides with hairs bicolored, gray at the base and cream at the tip, gradually shortening from the chest toward the chin, with cream portion getting proportionally longer. Pelage becomes sparser, shorter, and completely cream at the chin and throat ( Fig. 3 ). Orange tipped hairs visible in the inguinal region around the tail base. Tail pelage sparse at the tail base, gradually becoming denser toward the tip, where a short (ca. 3 mm) tuft is visible. Tail hairs reach 2–3 scales proximally and 3–6 scales distally, with three hairs emerging from each scale. Tail hairs brown or golden. Golden hairs predominant on the ventral surface of the tail, especially toward the base, giving a general lighter tone to this region and a faintly bicolor aspect to the tail. Mystacial vibrissae short and grayish-white anteriorly, and long and dark with silver tips posteriorly, extending beyond the posterior border of the ears. Supercilliary and genal vibrissae thinner, darker, and shorter than mystacial, and not surpassing the posterior border of the ears. Ears small, covered mainly with brownish hairs externally and yellowish hairs internally, with a distinct tuft of orange hairs at the internal base. Hands and feet short, light-orange, covered with white to golden hairs and sprinkled with a few brownbased and golden-tipped hairs dorsally. Ungual tufts grayish-white, reaching or slightly surpassing the claws. Hallux much shorter than other pedal digits; six tubercles on the ventral surface of the foot: thenar, hypothenar and four interdigital. Eight mammae arranged in four pairs: two inguinal, one postaxial and one pectoral.

Skull slender ( Fig. 4 ) with a short (less than 1/3 of the skull length) and narrow rostrum (ca. 1/5 of the skull width). Nasals slightly longer than rostrum, projecting anteriorly beyond the anterior margin of the premaxillae, and reaching or passing the suture between the maxillae and the lacrimals posteriorly. Zygomatic arches slender, slightly convergent anteriorly; jugals present. Zygomatic plate narrow and zygomatic notch shallow; zygomatic spine absent, and nasolacrimal capsule evident. Supraorbital foramen usually present, but sometimes absent or weakly developed on one side of the skull. Frontals narrow, entire molar toothrows and the maxillary root of the zygomatic arch visible in dorsal view. Interorbital region hourglass shaped, margins slightly angled, supraorbital crests absent. Dorsal surface of the skull moderately depressed mainly along the anterior part of the interfrontal suture, and reaching the posterior borders of the nasals. Hamular process of the squamosal thin and situated anteriorly, making the subsquamosal foramen smaller than the postglenoid. Interparietal broad, almost reaching the squamosal laterally. Paroccipital process weakly developed, auditory bullae large and inflated. Incisive foramen long, usually reaching the anterior border of the first molars, with slightly concave lateral margins. Mesopterygoid fossa wide and long, anterior margin biconcave and reaching the midline of the third molars ( Fig. 4 ). Palate short and wide (ca. 1/4 of skull width), with two longitudinal grooves punctuated by minute palatine foramina, varying in number (1–3) on each side of the skull, and a pair of small posterolateral palatine pits. Sphenopalatine vacuities well-developed, larger on the basisphenoid. Parapterygoid plate wide and triangular, posteriorly wider than the mesopterygoid fossa, and with minute perforations scattered anteriorly. Posterior opening of the alisphenoid canal small, transluscent groove indicating the passage of the supraorbital ramus of the carotid artery across the squamosal and alisphenoid present, and sphenofrontal foramen visible in most specimens (carotid circulatory pattern 1 of Voss 1988). Trough for buccinator-masticatory branch of maxillary nerve evident. The alisphenoid strut may be absent or present, making the foramen ovale and the buccinator-masticatory foramen confluent in some, but not all specimens. This trait varies even among specimens from the same population, and sometimes the strut is well-formed on one side of the skull and only a small spine projects from the alisphenoid on the other side.

Mandible slender ( Fig. 5 ), ramus shallow, and condyloid process well-developed, projecting above a small sickle-shaped coronoid process, and beyond the angular process posteriorly. Angular notch deeper near the angular process. Capsular process of lower incisor alveolus protruding noticeably from the lateral surface of the dentary, posterior to the coronoid process and below the sigmoid notch. Inferior masseteric crest welldeveloped, converging anteriorly with the superior masseteric crest below m1.

Upper incisors opisthodont, with dark-yellow enamel on the external surface; ungrooved. Upper molar toothrows parallel, molars pentalophodont ( Fig. 6 ). Occlusal surface rectangular in M1, squarish in M2, and triangular in M3. M1 30% longer than M2; M3 is the smallest upper tooth. Anteromedian flexus and anteroflexus deep, sharply separating even-sized anterolabial and anterolingual conules. Anteroloph and mesoloph of M1–M3 well-developed, and posteroloph of M1–M2 relatively small. Paraflexus, metaflexus, and hypoflexus of M1–M2 conspicuous; protoflexus of M2 minute. Lower molars almost rectangular; m1 20% longer than m2 or m3; m3 narrower than m2. Procingulum of m1 small, anteromedian flexid visible only in young specimens, anterolophid and protolophid weakly-developed. Mesolophid and posterolophid of m1–m3 well-developed. Ectolophid and ectostylid of m1–m2 conspicuous, reaching the labial margin of the tooth ( Fig. 6 ).

Postcranial skeleton of two paratypes (MZUSP 33170, 33171) available. Vertebrae 68–70: cervical 7, thoracic13, lumbar 6, sacral 4, caudal 38–40; ribs 13 (seven attached to the sternum).

Comparisons. The three species of Juliomys can be easily recognized by a suite of external and skeletal characters: Juliomys ossitenuis shares many external features with J. pictipes and many skull features with J. rimofrons . In general, J. ossitenuis is smaller than J. rimofrons and J. pictipes , the last being the largest of all ( Table 2 ). J. ossitenuis shares with J. pictipes the conspicuous orange rump and nose, although this trait is more evident in the latter. J. rimofrons , on the other hand, lacks the orange nose, but has an orange rump, not as intensely colored as in the other congeners. J. rimofrons has longer, denser and darker pelage than the other two ( Fig. 3 ). The dorsal hairs are darker in J. ossitenuis than in J. pictipes , which has the most colorful nose and rump among the three. The ventral pelage of J. ossitenuis is darker than that of J. pictipes and much lighter than that of J. rimofrons ( Fig. 3 ), although there is a considerable variation among populations of J.

ossitenuis , with some individuals of the southern part of the distribution with more whitish ventral pelage than those from the north. The basal gray portion of ventral hairs in J. ossitenuis reaches 1/2 of the hair length and the tip is cream-white. This gray portion is longer in J. rimofrons , which has golden-tipped ventral hairs, and much shorter in J. pictipes , in which the ventral hair tips are whiter. In addition, the hairs on the chin are graybased in J. rimofrons , completely white in J. pictipes and most specimens of J. ossitenuis ( Fig. 3 ). The tail is markedly bicolor in J. rimofrons and J. pictipes , and faintly bicolored in J. ossitenuis . In J. rimofrons , there is a distinct mid-ventral darkish longitudinal line near the tail base. This line is present in most specimens of J. ossitenuis and a few J. pictipes , being much paler in both species than in J. rimofrons . The dorsal surface of the hindfeet is light-orange in J. ossitenuis , golden-orange in J. pictipes , and pale orange-brown in J. rimofrons . J. ossitenuis and J. pictipes share self-colored yellowish-white ungual tufts, while in J. rimofrons they are gray-based.

Character J. pictipes J. ossitenuis J. rimofrons Overall body size large small small Nose orange orange brown Juliomys ossitenuis has the smallest and most delicate skull among the three species, and J. rimofrons has the most inflated braincase ( Figs. 4 and 5 ). All three species share the dorsal depression across the suture between the nasal and the frontal, making these bones thinner in this area. In the three known specimens of J. rimofrons , there is a distinct interfrontal fontanelle (or fenestra), visible to the naked eye. This trait has never been recorded in J. pictipes , but a smaller slit is present in some specimens of J. ossitenuis (four out of six specimens collected at Estação Ecológica do Bananal, São Paulo; Fig. 2 , locality 9). J. ossitenuis and J. rimofrons share several skull characters when compared to J. pictipes , such as a narrower rostrum and zygomatic plate, narrower and hour-glass shaped interorbital region, shallower zygomatic notch, and larger and more inflated tympanic bulla. They also share the carotid circulation pattern, with the squamosal-alisphenoid groove left by the supraorbital branch of the stapedial artery extending to the sphenofrontal foramen (pattern 1 of Voss 1988). J. pictipes has a large posterior opening of the alisphenoid canal and lacks the squamosalalisphenoid groove and sphenofrontal foramen, characterizing the absence of the supraorbital branch of the stapedial artery (pattern 2 of Voss 1988). J. ossitenuis has the largest sphenopalatine vacuities, followed by J. rimofrons , while these vacuities are minute or usually lacking in J. pictipes . The parietals deeply expand onto the lateral surface of the braincase in J. ossitenuis and J. rimofrons , while in J. pictipes , the parietals extend only slightly onto the lateral surface on the squamosal (see fig. 15 in Weksler 2006). The incisive foramen is longest in J. rimofrons , shortest in J. pictipes and intermediate in J. ossitenuis . The latter has the smallest posterolateral palatine pits, and most delicate mandible. In J. ossitenuis and J. rimofrons , the condyloid process projects posteriorly, extending further than the posterior margin of the angular process. The upper molars of the three species are very similar. They are larger, with more robust cusps in J. pictipes than in the other two species, reflecting its larger overall size. The main distinction among the three is the development of the ectolophid and ectostylid of m1–m2, which is conspicuous in J. ossitenuis , small in J. rimofrons and very small or absent in J. pictipes .

There are few specimens of Juliomys with postcranial material available, and we only examined J. ossitenuis and J. pictipes . In general, the scapula, clavicle and humerus of J. ossitenuis are smaller and more delicate than those of J. pictipes ( Fig. 7 ). The spinous process and the supraspinous fossa are smaller in J. ossitenuis than J. pictipes , but the infraspinous fossa is relatively larger in the former. The deltoid tuberosity of humerus has a concave distal border in J. ossitenuis , while in J. pictipes is the distal surface of this tuberosity is almost straight ( Fig. 7 ).

Molecular phylogeny. The maximum likelihood tree ( Fig. 8 ) had a score of -Ln=2936.7 (proportion of invariable sites=0.504872; gamma shape parameter=17.217111). The parsimony analysis resulted in 84 shortest trees (length = 423 steps), with a consensus topology nearly identical to the likelihood tree of Figure 8 . All well-supported nodes on the likelihood tree were also recovered using parsimony and Bayesian inference. The tree shows a well-supported monophyletic genus Juliomys , as well as monophyletic species (bootstrap>80% and posterior probability=100%). The tree also indicates sister-group relationship among J. pictipes and J. rimofrons , but the bootstrap values for this node under both parsimony and likelihood are quite low (54% and 58%, respectively), even though the Bayesian posterior probability is high (97%). The average level of cyt b sequence divergence among the three species is similar (13.4–14.4%), being much higher than the average divergence within species (0.0–2.5%), and lower than the divergence from the outgroups (21.7%). The divergence within J. ossitenuis is higher than within J. pictipes across nearly the same geographic area. Within the J. ossitenuis clade, haplotypes from the northern part of the range are basal, followed by those from Minas Gerais (which do not necessarily form a monophyletic clade) and a well-supported clade from São Paulo, in the southernmost part of the geographic distribution.

Karyotype. The karyotype has 2n=20, NFa=36, with three large metacentrics (pairs 1, 2 and 3), three large submetacentric pairs (pairs 4, 5, and 6), and three medium-sized biarmed pairs (pairs 7 to 9). The X chromosome is a large submetacentric and the Y is a small acrocentric, both clearly distinct from the autosomes ( Fig. 9 ).

Natural history. Juliomys ossitenuis is found in both Atlantic rain and semi-deciduous (or tropical seasonal; Morellato & Haddad 2000) forests above 800 meters, including cloud forests at higher elevations. Collecting localities of specimens examined range from the state of Espírito Santo to southern São Paulo, in southeastern Brazil ( Fig. 2 and Appendix). There is a positive linear correlation between latitude and elevation of collecting localities of J. ossitenuis (r=0.9240, p<0.00001), so that higher altitudes are apparently preferred at northern latitudes. The vast majority of specimens were collected in protected areas of mature, continuous forests. J. ossitenuis is an arboreal animal with short hands and feet. The holotype and three paratypes were collected in Sherman traps placed in tree branches or vines, but several other specimens were collected in pitfall traps (R. Pardini, pers. commun.). The only reproductive data available is the record of a lactating female collected on 30 May 1991 (UFMG 3173), in the begining of the dry season.

Figures

FIGURE 1. Picture of a male Juliomys ossitenuis sp. nov. (MBML 2783) from Macieira, Parque Nacional do Caparaó, Espírito Santo, Brazil. Photograph by Pedro L. Peloso.

FIGURE 2. Collecting localities of J. ossitenuis sp. nov. (circles), J. pictipes (triangles) and J. rimofrons (star), and syntopy of J. ossitenuis and J. pictipes (square). Numbers correspond to the localities listed in the Appendix.

FIGURE 3. Dorsal and ventral views of the skins of: A, J. pictipes (UFMG 3168); B, J. ossitenuis sp. nov. (MN 69752, the holotype); C, J. rimofrons (MN 61647, the holotype).

FIGURE 4. Dorsal and ventral views of the skulls of the holotypes of: A, J. pictipes (FMNH 26814),; B, J. ossitenuis sp. nov. (MN 69752); C, J. rimofrons (MN 61647). Scale bar = 5 mm. Photograph of FMNH 26814 by Pablo Gonçalves.

FIGURE 5. Lateral view of the skulls and mandibles of the holotypes of: A, J. pictipes (FMNH 26814); B, J. ossitenuis sp. nov. (MN 69752); C, J. rimofrons (MN 61647). Scale bar = 5 mm. Photograph of FMNH 26814 by Pablo Gonçalves.

FIGURE 6. Upper left (above) and lower right (below) molar toothrows of: A, J. ossitenuis sp. nov. (MN 69752, the holotype); B, J. ossitenuis sp. nov. (MZUSP 33171); C, J. pictipes (FMNH 26814, the holotype); D, J. pictipes (UFMG 3159). Arrows point to the ectolophid / ectostylid on m 1 and m 2 of J. ossitenuis. Scale bar = 0.5 mm. Photograph of FMNH 26814 by Pablo Gonçalves.

FIGURE 7. Left humerus, scapula, and clavicle of: A, J. ossitenuis sp. nov. (MZUSP 33171); B, J. pictipes (UFMG 3168). Scale bar = 5 mm.

FIGURE 8. Phylogenetic relationships among the species of Juliomys represented by the maximum likelihood phylogram resulting from the analysis of 801 base pairs of the mitochondrial cytochrome b gene. Numbers above branches represent parsimony and likelihood bootstrap support, and Bayesian posterior probabilities, respectively. Numbers below branches correspond to average Kimura 2 - parameter genetic distances among members of the clade.

FIGURE 9. Conventional staining of the karyotype of J. ossitenuis sp. nov. (MBML 2783, male), showing 2 n = 20 NFa = 36.

Tables

TABLE 1. Body and skull measurements (mm) and weight (g) of the type series of J. ossitenuis sp. nov. (M = male, F = female, for other abbreviations, see material and methods).

Age class 3 Totl 205	2 190	3 213	2 165	3 177	3 195
Tail 110	106	116	89	103	113
HF 21 Ear 16	21 14	22 17	14 14	19 10	20 15
Weight 22	18	28	11	14	21
ONL 25.74 PL 11.61	– 10.83	26.83 12.08	21.95 9.80	23.95 10.81	24.81 11.21
PPL 9.01	8.42	9.78	7.47	8.32	8.98
MRC 3.85 M1B 1.06	3.69 1.02	3.92 1.11	3.76 1.03	3.65 1.02	3.72 1.05
PBL 3.81	3.58	3.86	3.28	3.39	3.62
TFL 7.84 DL 6.57	7.15 6.08	8.15 7.04	6.79 5.47	6.56 6.01	7.58 6.23
IFL 4.85	4.67	5.36	4.19	4.72	4.62
IFB 1.78 PB1 2.57	1.86 2.53	2.13 2.65	1.69 2.33	1.34 2.31	1.70 2.39
PB3 2.86	2.87	3.12	2.69	2.63	2.82
MFB 1.86 BIT 1.65	1.67 1.49	1.95 1.76	1.43 1.31	1.72 1.57	1.66 1.56
BW 3.79	3.75	3.98	3.71	3.70	3.79
BL 4.78 BCB 10.12	4.56 10.13	4.91 10.49	4.62 10.15	4.48 10.34	4.64 9.98
SH 7.54	7.40	7.87	6.95	7.33	7.70
RH 4.68 RB 4.33	4.42 4.25	5.16 4.87	3.99 3.74	4.22 3.90	4.53 4.38
RL 7.90	–	8.34	6.35	7.42	7.24
NL 9.15 ZPL 1.77	– 1.64	9.80 2.20	7.23 1.34	8.95 1.66	8.45 1.89
IOB 3.63	3.57	3.70	3.69	3.87	3.93
ZB 13.27 GLM 13.37	12.74 12.57	13.98 14.01	11.97 11.76	12.19 12.51	12.64 12.97
MMR 3.95	3.77	3.98	3.77	3.72	3.78
DR 2.81	2.60	2.90	2.63	2.71	2.59

TABLE 2. Summary of comparative diagnostic characters among the three species of Juliomys.

Dorsal pelage Ventral pelage	short, light orange-brown white	short, dark orange-brown cream-white	long, dark-brown light-brown
Tail	markedly bicolored	slightly bicolored	markedly bicolored
Mid-ventral dark line on tail Dorsal pelage of hindfeet	usually absent or indistinct golden-orange	usually present, faint light-orange	present, distinct orange-brown
Ungual tufts	self-colored, yellow-white	self-colored, yellow-white	gray-based
Braincase Interfrontal fontanella	robust absent	small, delicate usually absent	robust, inflated present
Zygomatic notch	deep	shallow	shallow
Interorbital region Tympanic bulla	broad, convergent anteriorly small	narrow, hourglass shaped large	narrow, hourglass shaped large
Squamosal-alisphenoid groove	absent	present	present
Sphenopalatine vacuities Lateral extension of parietals	absent or minute small	very large broad	large broad
Incisive foramen length	short	intermediate	long
Posterolateral palatine pits Mandible	large large, robust	small small, delicate	large medium
Posterior projection of condy- loid process Ectolophid/ectostylid of m1– m2	short absent or minute	long conspicuous	long small
Karyotype	2n=36, NFa=34	2n=20, NFa=36	2n=20, NFa=34