Rhipidomys ochrogaster J.A. Allen, 1901

Pacheco, Víctor & Peralta, María, 2011, Rediscovery of Rhipidomys ochrogaster J. A. Allen, 1901 (Cricetidae: Sigmodontinae) with a redescription of the species, Zootaxa 3106, pp. 42-59 : 43-56

Rhipidomys ochrogaster J.A. Allen, 1901

Type locality. “Inca Mines [= Santo Domingo Mine], about 200 miles northeast of Juliaca, on the east side of the Andes, on the Inambary River [Río Inambari].” Department of Puno, Peru.

Distribution. Only known from the Yungas of southeastern Peru, Department of Puno, in the Río Inambari drainage ( Allen, 1901; Tribe, 1996), and the Río Tambopata drainage (this work), from 1220 m to 1942 m ( Fig. 1 ).

Revised diagnosis. A large-sized, long-tailed species of Rhipidomys with orange-brown dorsal fur and pale orange or melon ventral fur; tail dark, considerably longer than head and body, and with long terminal pencil; broad hind foot with metatarsal patch extending onto first phalanges of toes. Skull moderately large, with rather narrow and pointed rostrum, broad interorbital region and broad, rounded braincase; supraorbital shelf well developed and divergent backward; postorbital ridges absent or weak; primitive (pattern 1) carotid circulation (large stapedial foramen, squamosal-alisphenoid groove visible but not strong, and sphenofrontal foramen); and narrow zygomatic plate.

Description. External morphology. A large-sized Rhipidomys with orange-brown dorsal pelage and relatively long hairs (cover hairs: 11–13 mm, guard hairs: 14–17 mm), pale-orange ventral pelage moderately countershaded ( Fig. 2 ). The dorsal coloration is Color 26 Clay (color codes follow Smithe, 1975), washed with Color 28 Olive Brown; ventrally the pelage is Color 24 Buff, and the margins are Color 39 Cinnamon. The chin is whitish. Ventral hairs lack a gray-based band except on the chest. A middorsal stripe and a pectoral streak are lacking. Ears are small and dark with a very narrow antitragus; an auricular patch behind the ears is absent; the orbicular ring is dark but narrow. The anus is not protruded.

Genal, superciliary, and mystacial vibrissae are present. Mystacial vibrissae are very long, extending back far beyond the pinna. Genal and superciliary vibrissae are long and also projected backward far beyond the pinna when appressed to the body. Ungual tufts on the manus cover the claws. The metacarpal region is dark brown flecked with white hairs. The claws of the manus are curved with open bases; the thenar and hypothenar pads are both large and similar in size; digit II is longer than digit V. Pes long and relatively broad, with long ungual tufts that cover the claws; the metatarsal patches are dark brown (Color 27 Drab), flecked with golden hairs, and extending to first phalanges of toes; the terminal portion of toes and sides of the feet are pale orange to cream ( Fig. 3 a). Six plantar pads are present; the thenar and hypothenar are well developed, the first is larger than the second; the hypothenar is located directly behind the pad IV, and overlaps the thenar and pad I ( Fig. 3 b). Pad region of the plantar surfaces are squamated. Digits on the pes are long, digit I extends to halfway along the second phalange of digit II, and digit V to the base of the claw of digit IV ( Fig. 3 a, b). The tail is uniformly dark, longer than head and body length (130% in our specimen and 148% in the holotype), and terminates in a long pencil of hairs of 17 to 23 mm in length ( Fig. 3 c). The base of the tail is not densely haired. Hairs along the shaft extends over 2.5 rows of scales; and one centimeter covers 13 or 14 rows of the tail. There are three pairs of mammae in inguinal, abdominal and pectoral position (sensu Pacheco, 2003).

Cranial morphology. Skull is relatively large (greatest length 36.61 and 38.16 mm in the holotype and our specimen respectively) with a convex braincase profile ( Fig. 4 ). Rostrum relatively narrow and pointed with reduced gnathic process; nasals are long, narrow, and tapering posteriorly to a point posterior to premaxillary-maxillary-frontal joint. Zygomatic notches are shallow; interorbital region is moderately broad, with base of molars visible from dorsal view; supraorbital shelf is prominent and divergent backward, the anterior half is also expanded; postorbital ridge is absent or weak; braincase broad and rounded. Premaxillary-maxillary-frontal joint placed behind zygomatic notch. Zygomatic plate is vertical and narrow, almost as broad as the length of M1. Zygomatic arches with rounded profile but narrow anteriorly, and do not dip to the plane of molar ridges. Anterior orbital bridge is moderately high. Lacrimals are small, elongated, and without posterior process; frontals are broad, flat, and without a medial depression; fronto-parietal suture is rounded or triangular; a rhomboid interparietal is longitudinally longer than half the length of parietals. Parieto-occipital suture is about a third of the parietal breadth. Incisive foramina is long and broad, with posterior margins rounded, and extend backward to a place between M1 procingulum; septum is long and narrow, close to half the length of incisive foramina. Diastema shape is concave; M1 are placed posterior to the base of zygomatic plate. Palate length is short and broad, extending to M3 but not reaching the hypoflexus of M3. Posterolateral palatal pits are small and placed at both sides of mesopterygoid fossa. Maxillary pits are large and placed at level of M1 procingulum. Sphenopalatine vacuities are closed or represented by small slits; maxillary base of molars are rectangular. Mesopterygoid fossa is broad with sides parallel; medial posterior process of palate is very small. Parapterygoid fossa is triangular, deep, and without vacuities; posterior alisphenoid channel and foramen ovale are large; middle lacerate foramen is conspicuous, extends from basisphenoid to near the tegmen tympani; posterior margin of squamosals lacks a notch; alisphenoid strut is present and robust; anterior alisphenoid channel is small. Carotid circulation pattern 1 as determined by Voss (1988): large stapedial foramen, squamosal-alisphenoid groove visible but not strong, and sphenofrontal foramen. Internal carotid canal is relatively small and bounded by basioccipital and Eustachian tube, but not the periotic. Tegmen tympani are large and robust and sinus groove are present. Jugal is robust, maxillary and squamosal endings do not overlap. Ectotympanic ring is open, dorsal margin of ectotympanic do not reach the petrosal; ventral margin of ectotympanic has a small leaf-process. Postglenoid foramen is very small and hidden by the hamular process; subsquamosal fenestra is placed posterior or dorsal to postglenoid foramen, and with its posterior margin opened. Lambdoid ridge is absent, the occipital condyle is at the same level of braincase; paraoccipital process is conspicuous and not bifurcated; ethmoid foramen is placed dorsal to M2; ethmoturbinals are moderate in size; sphenopalatine foramen is bordered by palatine bones; optic foramen is relatively large and dorsal to M3. Bullae are small and not globose; Eustachian tube is long and tubular; anterior process is broad and short, with two spines that may or may not reach the alisphenoids; basioccipital is very broad; mastoids lack perforation. Lamina of malleus is very narrow and not deep, processus brevis of incus is long, conical, and relatively robust; orbicular apophysis is short and massive.

Dental morphology. Incisors deep, moderately opisthodont, with wearing surface facing caudally; upper and lower molar cusps are slightly alternated; tooth design and topography are bunodont and brachyodont; molar hypoflexus and paraflexus do not overlap ( Fig. 5 ). Labial cingulum on upper molars are well developed. Procingulum breadth of M1 is less than the breadth across the protocone and paracone. Anteromedian flexus is well defined and separates a smaller anterolingual conule from the anterolabial conule. M1 anteroloph is present and perpendicular to the mure; anterolophule is present and fills the anteroflexus; paraloph is perpendicular to the mure; mesoloph is perpendicular to the cingulum; hypoflexus is distinct and triangular in shape; protostyle and enterostyle are present; paralophule well developed reaching mesoloph. M2 protoflexus is present and small, paraflexus and anteroloph are complete; M2 paraloph obliquely oriented to the mure; hypoflexus and posteroflexus of M2 distinct: paralophule also distinct. M3 topography is crenulated, with a distinct hypoflexus and a low metacone. The procingulid of m1 is divided by the anteromedian flexid into two subequal conules. The m1 presents a well developed lingual cingulid, and a cingulid shelf on the anterolabial margin of the procingulid; protolophid and anterolophid are present; mesolophid and entolophid are perpendicular to murid; posterolophid and posteroflexid are long and narrow; ectolophids are absent; anterolabial cingulum of m2 and m3 are conspicuous.

Mandible and other features. Masseteric crests level with the anterior edge of m1; mental foramen large and placed close to the diastema; capsular process not developed and forming a shelf; mandibular bone not deep, with the ventral margin shallow. Coronoid process short, triangular, slightly ventral to the condylar process; condylar process long, robust, and extending posterior to the angular process. Hyoid basihyal lacks medial process.

The morphology of the stomach conforms to the unilocular-hemiglandular pattern sensu Carleton (1973); and it is similar to the illustration of Thomasomys cinereus in Carleton (1973: fig 4b). The stomach content analysis revealed a great abundance of seed and insects. Seeds belonged to the species Piper sp. 1 and Piper sp. 2 (Arias, E., pers. comm.); while insects were represented by only one species of army ants of the genus Labidus (Azorsa, F., pers. comm.). Seeds represented about 30% and the army ants 70% of items in 10 randomly selected fields (Arias, E., pers. comm.). The gall bladder is absent. No endoparasites were observed.

Comparisons. This section is based on characteristics presented by Tribe (1996), Patton et al. (2000) and by our own examination. Compared to Rhipidomys leucodactylus , R. ochrogaster may be distinguished externally by the bright orange-brown dorsal pelage coloration instead of a dark-brown; ventral fur is pale orange instead of white or light yellowish, and with gray-based hairs only on the chest versus throughout all venter; dorsal hairs are longer, 11–13 mm versus 6–10 mm; metatarsal patch coloration extends into the first phalanges of toes versus extending the entire toes ( Patton et al., 2000); tail with a terminal tuft of hairs from 17 to 23 mm long versus about 25 mm in our samples of R. leucodactylus , although it might reach 40 mm in the last taxon ( Tribe, 1996); scales cover 13 or 14 rows per 10 mm longitudinally versus 12 rows. R. ochrogaster is also distinguished from R. leucodactylus in several cranio-dental characteristics ( Figs. 6 , 7 ). The braincase is broad and rounded versus narrow and more elongated, and the rostrum is narrow versus broad ( Tribe, 1996). The mesopterygoid fossa is narrow versus broad. The carotid circulatory pattern is primitive (stapedial foramen, internal groove on the squamosal and alisphenoid, and sphenofrontal foramen present) versus the derived condition ( Tribe, 1996); and orbicular apophysis is short versus long and digit-like ( Fig. 9 ). Rhipidomys ochrogaster is also generally smaller in several skull measurements ( Table 1 ): Greatest length of skull, Condyloincisive length, Condylomolar length, Length of orbital fossa, Diastema length, Length of incisive foramina, and Length of maxillary toothrow; and narrower in Breadth of incisive foramina, Breadth of rostrum, Breadth of palatal bridge, Breadth of nasals, and Zygomatic breadth. It is also shorter in Breadth of zygomatic plate and Depth of incisors.

Rhipidomys ochrogaster is also distinct from R. gardneri by the bright orange-brown dorsal fur coloration instead of yellow brown; ventral fur is pale orange instead of whitish, and with gray-based hairs only on chest versus on the throat and chest ( Patton et al. 2000) or throughout all venter (this work); dorsal hairs are longer, 11–13 mm versus 5–10 mm; dark metatarsal patch extends into the first phalanges of toes versus not extending onto the toes ( Patton et al., 2000); tail with moderate scales, 13 or 14 per 10 mm longitudinally versus 16 on average ( Patton et al. 2000), and the terminal tuft of hairs in the tail is longer, 17–23 mm versus 6–14 mm. In the skull, the braincase in R. ochrogaster is broad and rounded versus narrow and more elongated, and the rostrum is narrow versus broad ( Tribe, 1996); the zygomatic notch is shallow versus deep, and the mesopterygoid fossa lacks a medial spine on the anterior border versus present ( Patton et al., 2000); the carotid circulatory pattern is primitive (stapedial foramen, internal groove on the squamosal, and sphenofrontal foramen present) versus the derived condition ( Tribe, 1996); processus brevis of incus is robust and conspicuous versus weak and slender ( Fig. 9 ). Also, R. ochrogaster exhibit a distinctly narrow nasal bone (4.18 versus 4.62 in average) and a narrow zygomatic plate (2.93 versus 3.58 in average) in comparisons to R. gardneri ( Table 1 ).

Characters R. leucodactylus R. gardneri R. ochrogaster

AMNH 16481a MUSM 35095 a External measurements of the holotype taken from Allen (1901). Cranial measurements of the holotype taken by the senior author; b measurement taken from dry skin

Upper and lower molars of R. ochrogaster are very similar to those of R. leucodactylus and R. gardneri ( Fig. 8 ), except that anteromedian flexus and flexid are deeper in R. leucodactylus and R. gardneri than in R. ochrogaster ( Tribe, 1996) . This author also mentioned that R. ochrogaster have upper molars with well developed paralophule/ mesostyle, but these structures are also present in the other two species. R. ochrogaster and R. leucodactylus lack enteroloph and ectolophids on upper and lower molars respectively, but these structures are frequently seen in R. gardneri ( Fig. 8 ).

Natural history. The habitat of the collection site is characterized by a forest of slender trees that reach approximately 15 m in height, a dense understory, and a forest floor covered to a depth of at least 3 cm with soil litter ( Fig. 10 ). The trap line was set on a steep slope, dominated by woody plants and herbaceous patches of fern, grass and sedge. Plant species present in this habitat are Ilex sp. ( Aquifoliaceae ), Viburnum sp. ( Adoxaceae ), Miconia sp. ( Melastomataceae ), Myrsine sp. ( Myrsinaceae ), Myrcia sp. ( Myrtaceae ), Clusia sp. ( Clusiaceae ), Cecropia sp. ( Urticaceae ), and Clethra sp. ( Clethraceae ). This habitat corresponds to the Yungas ( Tovar Narváez et al., 2010) or the humid eastern montane forests ( Young and Leon, 1999). The capture took place at the beginning of the dry season (May–November). During the fieldwork the weather was sunny and clear with sporadic rains.

Rhipidomys ochrogaster was collected in the same trap line with the species Oligoryzomys destructor (Tschudi) , Neacomys spinosus (Thomas) , Lenoxus apicalis J. A. Allen , Oxymycterus juliacae J. A. Allen , and Akodon baliolus Osgood. The recognition of the last two taxa follow Pacheco et al. (2011) who consider them as valid species.

Figures

FIGURE 1. Collecting localities of Rhipidomys ochrogaster in Peru, Puno department: (1) Inca Mines (= Santo Domingo) in the valley of Río Inambari; 69 ° 41 ' W, 13 ° 51 ' S; (2) Yanacocha, in the valley of Río Tambopata; 69 º 15 ' 20.4 '' W, 14 º 11 ' 37.5 " S; 1942 m.

FIGURE 2. External appearance of Rhipidomys ochrogaster (MUSM 35095): (A) lateral view, (B) dorsal view, and (C) ventral view. Scale is 20 mm.

FIGURE 3. Hind feet and tail of Rhipidomys ochrogaster (MUSM 35095): (A) dorsal view of left foot, (B) ventral view of left foot, and (C) terminal part of the tail showing a well developed pencil. Scale is 10 mm.

FIGURE 4. Dorsal, ventral and lateral views of cranium and mandible of Rhipidomys ochrogaster (MUSM 35095). Scale is 10 mm.

FIGURE 5. Occlusal view of molar rows of Rhipidomys ochrogaster (MUSM 35095): (A) left upper molars, (B) right lower molars. Scale is 1 mm.

FIGURE 6. Dorsal and ventral view of the skull of three species of Rhipidomys: (A) R. gardneri (MUSM 14472), (B) R. leucodactylus (MUSM 12987), and (C) R. ochrogaster (MUSM 35095). Scale is 10 mm.

FIGURE 7. Lateral view of the skull and mandible of three species of Rhipidomys: (A) R. gardneri (MUSM 14472), (B) R. leucodactylus (MUSM 12987), and (C) R. ochrogaster (MUSM 35095). Scale is 10 mm.

FIGURE 8. Occlusal view of upper and lower molar rows of three species of Rhipidomys: (A – D) R. gardneri (MUSM 14472), (B – E) R. leucodactylus (MUSM 12987), and (C – F) R. ochrogaster (MUSM 35095). Scale is 1 mm.

FIGURE 9. Lateral view of braincase and an enlargement of the auditory bullae region of three species of Rhipidomys: (A – B) Rhipidomys gardneri (MUSM 14472), (C – D) R. leucodactylus (MUSM 12987), and (E – F) R. ochrogaster (MUSM 35095). Scale is 10 mm. pop = paraoccipital process, pb = processus brevis of incus, oa = orbicular apophysis.

FIGURE 10. Mountain forest habitat near Yanacocha town where Rhipidomys ochrogaster was collected in our study. Photograph by M. Peralta.

Tables

TABLE 1. External and cranial measurements (in millimeters) of Rhipidomys leucodactylus, R. gardneri, and R. ochrogaster from Peru. Measurements are given in mean ± standard deviation, with range and sample size.

Head and body length	176 ± 11.53 (163–185) 3	171 ± 9.165 (161–179) 3	154	152.1
Total length	404.7 ± 11.68 (392–415) 3	356.33 ± 7.09 (350–364) 3	382	350.6
Length of tail	228.67 ± 6.50 (222–235) 3	185.33 ± 8.50 (177–194) 3	228	198.5
Length of foot	36.67± 2.52 (34–39) 3	34.66 ± 3.51 (31–38) 3	35	34.5
Length of ear	19.7 ± 5.09 (15–25.1) 3	19.33 ± 0.577 (19–20) 3	19b	21
Greatest length of skull	41.4 ± 1.2 (40–43) 10	40.4 ± 1.41 (38.2–41.77) 6	36.61	38.16
Condyloincisive length	38.5 ± 1.3 (37–41) 10	36.77 ± 1.31 (34.92–38.33) 6	34.34	34.51
Condylomolar length	25.1 ± 0.7 (23.9–26.3) 10	24.04 ± 0.72 (23.22–25.07) 6	22.72	23.15
Length of orbital fossa	13.7 ± 0.4 (13.1–14.2) 10	13.38 ± 0.52 (12.7–14.06) 6	11.99	12.66
Length of nasals	14.9 ± 0.7 (14–15.7) 10	14.00 ± 0.61 (13.05–14.83) 6	14.23	14
Diastema length	11.2 ± 0.7 (10.5–11.6) 10	10.62 ± 0.49 (9.8–10.93) 6	9.63	9.46
Length of incisive foramina	8.5 ± 0.3 (8.2–9.4) 10	7.57 ± 0.79 (6.1–8.35) 6	7.95	7.62
Length of maxillary toothrow	6.7 ± 0.3 (6.3–7.1) 10	6.21 ± 0.17 (5.93–6.31) 6	6.31	6.13
Breadth of incisive foramina	3.44 ± 0.2 (3.1–4) 10	3.32 ± 0.16 (3.19–3.62) 6	2.88	3.13
Breadth of rostrum	7.4 ± 0.4 (7–8.1) 10	6.17 ± 0.54 (5.57–6.9) 6	5.89	6.25
Breadth of palatal bridge	4.4 ± 0.3 (4–4.7) 10	3.75 ± 0.36 (3.26–4.31) 6	3.72	4.03
Breadth of first upper molar	1.8 ± 0.1 (1.6–1.9) 10	1.67 ± 0.05 (1.61–1.75) 6	1.77	1.81
Breadth of nasals	4.9 ± 0.4 (4.4–5.6) 10	4.62 ± 0.24 (4.35–4.96) 6	4.23	4.12
Least interorbital breadth	6.2 ± 0.5 (5.6–6.9) 10	6.26 ± 0.21 (6.03–6.61) 6	5.81	6.1
Zygomatic breadth	22 ± 0.8 (20.6–22.9) 10	20.94 ± 0.68 (20.2–21.72) 6	19.68	20.48
Braincase breadth	16.8 ± 0.5 (16.3–17.4) 10	16.49 ± 0.42 (15.78–16.92) 6	16.41	17.02
Breadth of zygomatic plate	3.7 ± 0.2 (2.9–4) 10	3.58 ± 0.18 (3.23–3.73) 6	2.92	2.94
Depth of incisor	2.3 ± 0.1 (2.1–2.4) 10	2.22 ± 0.18 (1.95–2.41) 6	1.95	2.03
Height of braincase	11.5 ± 0.4 (10.4–12) 9	11.05 ± 0.26 (10.73–11.37) 6	11.38	11.3
Weight	159 ± 3.61 (155–162) 3	144 ± 12.86 (126–155) 5	-	129