Caluromys lanatus

DidelphisLinnaeus, 1758:54. Part. DidelphysSchreber, 1778:532. Part, unjustified emendation of DidelphisLinnaeus, 1758. SariguaMuirhead, 1819:429. Part, vide Allen (1900:186). MicoureusLesson, 1842:186. Part. PhilanderBurmeister, 1856:74. Type species Philander cayopollinBurmeister, 1856 (= Didelphis philanderLinnaeus, 1758), by subsequent designation (Hershkovitz 1949:12). Preoccupied by PhilanderBrisson, 1762 and PhilanderTiedemann, 1808. GambaLiais, 1872:330. Part. CuicaLiais, 1872:330. Part. Micoureus: Ihering, 1894:11. Part. Caluromys J. A. Allen, 1900:189. Type species Didelphis philanderLinnaeus, 1758 by original designation. Replacement name for PhilanderBurmeister, 1856. Micoureus: Matschie, 1916:269. Part, not MicoureusLesson, 1842. MallodelphysThomas, 1920:195, footnote. Type species Didelphis lanigeraDesmarest, 1820 by original designation. Described as a subgenus of Philander sensu Burmeister (1856). CalaromysMiranda-Ribeiro, 1936:324. Incorrect subsequent spelling of Caluromys J. A. Allen, 1900. MallodelphisMiranda-Ribeiro, 1936:328. Incorrect subsequent spelling of MallodelphysThomas, 1920; considered a valid genus. CalurosmysÁvila-Pires, 1964:11. Incorrect subsequent spelling of Caluromys J. A. Allen, 1900. Order Didelphimorphia, family Didelphidae, subfamily Caluromyinae. A key to the 3 species of Caluromys, C. derbianus (Waterhouse, 1841), C. lanatus (Olfers, 1818), and C. philander (Linnaeus, 1758), follows: Total length 587–760 mm, ears whitish to pink; forelimbs and feet creamy white; gray patch between shoulders usually present; undersides buffy white to golden tawny; proximal 30–50% of tail with dorsal hair ------------------------------------------------------------------------------- C. derbianus Total length 410–730 mm; ears pinkish tan to brownish; forelimbs and feet red-brown to grayish; gray patch between shoulders rarely present; undersides orange or yellowish white to grayish; proximal 10–70% of tail with dorsal hair ------------------------------------------------------------------------------- 2 Total length 510–730 mm; proximal 50% of tail haired dorsally, up to 20% of tail haired ventrally; naked ventral surface of tail base covered with hard raised tubercles; pouch has lateral skin folds joined posteriorly and opens anteriorly ------------------------------------------------------------------------------- C. lanatus Total length 410–690 mm; pelage extending onto tail to ca. same length dorsally and ventrally, at maximum to 33% of total length of tail; naked ventral surface of tail base covered with smooth flat scales; pouch has separate and deep lateral skin folds and opens along midline ------------------------------------------------------------------------------- C. philander [Didelphys] lanataIlliger, 1815:107. Nomen nudum. D[idelphys]. lanataOlfers, 1818:206. Type locality “Paraguay;” restricted to Caazapá, Paraguay, by Cabrera (1916:516); based on Azara's (1801) “Micouré laineux.” Didelphis lanigeraDesmarest, 1820:258. Type localities “dans le Caapeza, á cinquante lieues de la cité de l'Assomption, Paraguay” and “dans les champs du village de Sainte-Marie de la Foi, Paraguay;” restricted to “Caazapá, Paraguay” by Cabrera (1916:516); based on Azara's (1801) “Micouré second” or micouré laineux.” Didelphys lanigera: Waterhouse, 1841:98. Name combination. Micoureus lanigera: Lesson, 1842:186. Name combination. Didelphys ochropusWagner, 1842:359. Type locality “Barra;” (Cabrera 1958:3) Barra do Rio Negro, Amazonas, Brazil. D[idelphys]. ornataTschudi, 1845:146. Type locality “der mittleren und tiefen Waldregion,” Peru. Didelphys [Philander] lanigera: Thomas, 1888:339. Part; name combination. Philander cicurBangs, 1898:161. Type locality “Pueblo Viejo, Colombia, altitude 8000 ft.” P[hilander]. ornatus: Bangs, 1898:162. Name combination. [Didelphys (Philander)] cicur: Trouessart, 1898:1238. Name combination. [Didelphys (Philander) laniger] ochropus: Trouessart, 1898:1238. Name combination; in synonymy of Didelphys (Philander) laniger derbiana. [Didelphys (Philander) laniger] ornata: Trouessart, 1898:1238. Name combination. Caluromys cicur: Allen, 1900:189. Name combination. Caluromys laniger: Allen, 1900:189. Name combination for Didelphis lanigeraDesmarest, 1820. Caluromys derbianus ornatus: Allen, 1900:189. Name combination. [Caluromys] ochropus: Thomas, 1901:196. Name combination. C[aluromys]. l[aniger]. cicur: Thomas, 1901:196. Name combination. [Caluromys] ornatus: Thomas, 1901:196. Name combination. [Didelphys (Philander) laniger] ornatus: Trouessart, 1905:855. Name combination and incorrect gender concordance. P[hilander]. l[aniger]. cicur: Thomas, 1913:358. Name combination. P[hilander]. l[aniger]. ornatus: Thomas, 1913:358. Name combination. Philander laniger jivaroThomas, 1913:360. Type locality “Sarayacu on the Pastasa River,” Pastaza, Ecuador. Philander laniger: Cabrera, 1916:514. Name combination. Micoureus ochropus: Matschie, 1916:269. Name combination. Micoureus ornatus: Matschie, 1916:269. Name combination. Micoureus juninensisMatschie, 1917:283. Type locality “Chanchamayo in der Nähe von La Merced, Provinz Junin, Peru, in her Höhe von 1000 m.” Micoureus meridensisMatschie, 1917:285. Type locality “von Briceno in der Montana de la Sierra bei Merida in Venezuela in der Höhe von 2500 m.” Micoureus cahyensisMatschie, 1917:288. Type locality “Am Rio Cahy in Rio Grande do Sul,” Brazil. Micoureus bartlettiMatschie, 1917:288. Type locality “Chamicaros-Fluß, südlicher Nebenfluß des Marañon zwischen Huallaga and Ucayali,” Loreto, Peru. Micoureus nattereriMatschie, 1917:291. Type locality “von Caissara, Matto Grosso,” Brazil. [Philander laniger] ochropus: Cabrera, 1919:33. Name combination. Mallodelphis lanigera ochropus: Miranda-Ribeiro, 1936:355. Name combination. Mallodelphis lanigera hemiuraMiranda-Ribeiro, 1936:355. Type locality unknown. Mallodelphis lanigera vitalinaMiranda-Ribeiro, 1936:355. Type locality “Barra do Paraopéba, Minas Geraes,” Brazil. Mallodelphis lanigera nattereri: Miranda-Ribeiro, 1936:356. Name combination. Mallodelphis lanigera modestaMiranda-Ribeiro, 1936:356. Type locality “Mato Grosso, provavelmente Pantanal,” Brazil. Caluromys laniger ochropus: Tate, 1939:163. Name combination. [Caluromys laniger] meridensis: Tate, 1939:163. Name combination. [Caluromys laniger] jivaro: Tate, 1939:163. Name combination. Caluromys laniger ornatus: Sanborn, 1949:277. Name combination. P[hilander]. lanata: Hershkovitz, 1951:552. Name combination. Philander calmensisVieira, 1955:347. Incorrect subsequent spelling of Micoureus cahyensisMatschie, 1917. Caluromys lanatus cicur: Cabrera, 1958:2. Name combination. Caluromys lanatus lanatus: Cabrera, 1958:2. Name combination. Caluromys lanatus ochropus: Cabrera, 1958:3. Name combination. Caluromys lanatus ornatus: Cabrera, 1958:3. Name combination. Content as above. Caluromys lanatus has 4 subspecies (Cabrera 1958): C. l. cicur (Bangs, 1898:161); see above; meridensis (Matschie) is a synonym. C. l. lanatus (Olfers, 1818:206); see above; cahyensis (Matschie), hemiura (Miranda-Ribeiro), lanigera (Desmarest), modesta (Miranda-Ribeiro), and nattereri (Miranda-Ribeiro) are synonyms. C. l. ochropus (Wagner, 1842:359); see above; vitalina (Miranda-Ribeiro) is a synonym. C. l. ornatus (Tschudi, 1845:146); see above; bartletti (Matschie), jivaro (Thomas), and juninensis (Matschie) are synonyms. Fur of C. lanatus is long, dense, and woolly; with a reddish brown dorsum that is brightest red over shoulders, forearms, and hind legs; with an underside orange to yellowish; and with reddish brown feet. In contrast, C. derbianus has a pale gray patch between shoulders, creamy white forelimbs and feet, and buffy white to golden tawny venter. C. philander has uniform red-brown to grayish upperparts and forelimbs, and C. philander also differs from C. lanatus in having a tail furred to the 1st one-third of its length dorsally and ventrally, whereas C. lanatus has up to 50% of its tail length furred dorsally and 20% of it furred ventrally. Caluromys lanatus is a medium-sized opossum with long, dense, and soft guard hairs and a tail ca. 140% of length of head and body (Fig. 1). Dorsal color is reddish brown to pale brown mixed with gray and grades to orange on shoulders, forelimbs, hind limbs, and top of head; rarely, individuals have a gray patch between shoulders. Head is grayish, and face has a prominent median dark stripe from between ears to nose, brown to orange eye rings, naked ears that are pinkish tan, and whitish cheeks. Ventral surface of body is yellowish white laterally and grayish at midline. Feet are reddish brown to dark gray. All digits have well developed pads and claws, except for thumb of hind feet. Tail is furred dorsally for one-half of its length and ventrally for one-fifth of its length. Terminal portion of tail is naked (usually whitish yellow mottled with brown spots) and fully prehensile. Pouch of females is developed only when carrying young; young are more grayish than adults (Eisenberg and Redford 1999; Emmons and Feer 1997; Patton et al. 2000; Vieira 1949). External measurements (range, in mm or g) of 26 adults of both sexes: length of head and body, 201–319; length of tail, 330–446; length of hind foot, 30–51; length of ear, 30–41; and body mass, 310–520 (Emmons and Feer 1997; Patton et al. 2000; Redford and Eisenberg 1992). An adult Caluromys lanatus from Salto Caxias Dam, Paraná State, Brazil Caluromys l. cicur from Magdalena Valley, Colombia, is grayish brown dorsally, with gray sides, and sometimes completely gray ventrally, whereas C. l. lanatus from Paraguay is pale brown, with tail lacking brown spots (Emmons and Feer 1997). C. l. ochropus from Amazonia has a markedly red-brown dorsal color (Patton et al. 2000), and is larger than C. l. lanatus from central and southern ranges (Costa and Patton 2005; Patton et al. 2000; Vieira 1949). Skull (Fig. 2) has a short and robust rostrum, small paraoccipital process that never surpasses occipital condyle, reduced lambdoidal and sagittal crests, well developed postorbital processes, small palatine foramina, dorsal projection of superior portion of zygomatic that reduces size of orbit, no foramen ethmoidale, and a small foramen rotundum (Pérez-Hernández 1985). C. lanatus also has a rostral process of the premaxillae, but lacks a palatal process, resulting in insertion of upper canine in maxillary bone. Nasal bones are wider posteriorly than anteriorly with tips extending anteriorly above or beyond I1, thereby obscuring nasal orifice in dorsal view. C. lanatus lacks maxillopalatine, palatine, and maxillary fenestrae, and a transverse canal foramen. Mandible has 2 mental foramina and an angular process that is obtuse and weakly inflected (Voss and Jansa 2003). Dorsal, ventral, and lateral views of cranium and lateral view of mandible of an adult male Caluromys lanatus (MZUSP [Museu de Zoologia da Universidade de São Paulo mammal collection] 4532) from Igarapé Grande, Rio Juruá, Amazonas, Brazil, collected by A. M. Ollala (field number 1981) on 15 January 1937. Greatest length of skull is 61.64 mm Means and parenthetical ranges of cranial measurements (in mm) of 8 adults of both sexes are: length of condyloincisive, 59.5 (56.5–62.8); breadth of zygomatic, 34.8 (32.7–37.1); width of braincase, 20.6 (19.4–22.3); breadth of interorbital constriction (taken posterior to postorbital processes), 8.4 (7.6–9.2); length of rostrum, 22.8 (21.7–24.0); length of nasal bones, 25.8 (22.2–27.1); width of rostrum, 13.0 (12.3–13.8); length of palate, 31.9 (30.5–33.4); width of palate, 17.7 (17.1–18.2); breadth of mastoid, 23.3 (21.4–25.6); length of basioccipital, 8.7 (8.2–9.2); depth of cranium, 18.9 (16.6– 21.1); length of molar row, 9.8 (9.2–10.1); and length from C to M4, 20.6 (18.2–22.2—Patton et al. 2000). Caluromys lanatus ranges from east of the Andes in central Colombia, western and southern Venezuela, eastern Ecuador, Peru, and Bolivia to western, central, and southern Brazil, northeastern Argentina (Missiones), and eastern and southern Paraguay (Fig. 3; Costa 2003; Costa and Patton 2005; Eisenberg 1989; Eisenberg and Redford 1999; Emmons and Feer 1997; Gardner 2005; Patton et al. 2000). Elevational range is 0– 2,600 m (Alberico et al. 2000). Distributions of 4 subspecies are: C. l. cicur, eastern Colombia and western Venezuela; C. l. lanatus, Paraguay and Brazil, from Mato Grosso to São Paulo states; C. l. ochropus, Orinoco and Amazon basins to eastern Brazil; and C. l. ornatus, Peru and Ecuador, east of the Andes (Cabrera 1958; Pérez-Hernández 1989). Geographic distribution of Caluromys lanatus in South America, 1, C. l. cicur; 2, C. l. lanatus; 3, C. l. ochropus; 4, C. l. ornatus. Square is type locality in Caazapá, Paraguay. Cross is Lagoa Santa, Brazil, with Pleistocene–Holocene remains of C. lanatus (Cartelle 1999; Winge 1893). Map redrawn with modifications from Costa (2003), Eisenberg (1989), Eisenberg and Redford (1999), Emmons and Feer (1997), and Lambert et al. (2005) Remains of C. lanatus occur in Pleistocene–Holocene cave deposits of Lagoa Santa, Minas Gerais, Brazil (Cartelle 1999; Winge 1893). Female C. lanatus have abdominal and inguinal mammae confined to the pouch region (Voss and Jansa 2003). Dental formula is i 5/4, c 1/1, p 3/3, m 4/4, total 50. Crowns of I2–I5 are asymmetrical with longer anterior than posterior cutting edges. Upper canine is simple and without accessory cusps. P1 is very small, without prominent occlusal features, and situated directly behind upper canine. A gap occurs between P1 and the much larger P2. P2 is taller than P3, which has well-developed anterior and posterior cutting edges. M1 is wider than M4. Molar dentition is weakly carnassialized and weakly dilambdodont. Upper molars lack ectoflexus. A continuous shelf occurs along anterior margin of crowns of M1–M3. Mandibular teeth have distinct lingual cusps in i1–i4, a p2 taller than p3, a deciduous p3 with a complete tricuspid trigonid, a labially salient hypoconid in m3, and a large and well-developed entoconid in m1–m3 (Redford and Eisenberg 1992; Voss and Jansa 2003). Occlusal area of molars is reduced (Cáceres 2000). Caluromys lanatus has a relatively large braincase and long tail, which are associated with its high degree of arboreal activity (Cáceres 2000; Eisenberg and Wilson 1981). The protein transthyretin occurs in plasma (Richardson et al. 1996). C. lanatus has a large hind gut and caecum, a small stomach, and a short small intestine (Cáceres 2005). The large hind gut and caecum are associated with a diet mainly of plant material (Chivers and Hladik 1980; Crowe and Hume 1997; Schieck and Millar 1985), and the small stomach chamber is associated with a frugivorous diet (Hildebrand 1995). Digestive tract anatomy is specialized for consumption of fruits, gums, and twigs. Penis of C. lanatus is postscrotal, forming an evident sigmoid flexure, and partially located in preputial sac when in nonerected state. Two muscles, ischiocavernous and bulbospongiosus, situated outside pelvic cavity, comprise bulk of penis musculature. These muscles join in radix penis, where paired levator muscles are encased and insert by a single tendon. Paired penis retractor muscles arise in sublumbar region and insert on both sides of dorsal curvature of sigmoid flexure. Glans is same length as penis, bifid, deeply cleft, and with elliptical tips lacking a diverticulum. Urethra ends in body–glans transition, with 2 urethral grooves extending for different lengths along medial surfaces of each glans tip. When erected, penis projects through cloaca, with preputial opening ventral to anus (Nogueira et al. 1999). Urogenital and rectal openings are closely juxtaposed and share a common mucosa (Voss and Jansa 2003). A median cylindrical structure is located between uterine cervices and the origin of lateral vaginal canals. An incomplete, thin, and perforated vaginal septum forms a short common vagina with lining markedly folded. A rudimentary pseudovaginal canal has lateral vaginal canals that form closed loops (Reig et al. 1987). In Brazil, 2 females with pouch young were trapped at Rio Juruá, Amazon Basin, during June and November. Postlactating females were trapped in February, March, and October in the same region (Patton et al. 2000). In Brazil, modal estrous cycle length was 27–29 days, and females cycle throughout the year (Bucher and Fritz 1977). Litter size is 1 or 2 young in the Amazon Basin (Patton et al. 2000) and 3 or 4 in southern range of distribution (Monteiro-Filho and Cáceres 2005). Females develop a pouch only when carrying young (Emmons and Feer 1997). Body mass of young averaged 3.5 g in October 1998 at a seasonal forest in southern Brazil, and sex ratio was male-biased (1.00:0.22; n = 3 litters—N. C. Cáceres, in litt.). Caluromys lanatus occurs in small, secondary forest fragments in Amazonian rain forest (Malcolm 1995) and in disturbed, fragmented forests in southern Brazil (Quadros et al. 2000). C. lanatus was trapped mostly in canopy and subcanopy, from 5 to 15 m high (Eisenberg and Redford 1999; Malcolm 1991b; Patton et al. 2000). C. lanatus occurs in dense multistratal rain forest (terra firme and várzea); in gallery, mangrove, semideciduous, transitional, and xerophitic forests; and in dense savanna (Carmignotto 2004; Gargaglioni et al. 1998; Gribel 1988; Moreno-Bejarano and Álvarez-León 2003; Patton et al. 2000; Talamoni and Dias 1999). In its southern range, C. lanatus occurs in more seasonal forests when compared to its northern range. Continuous distribution of C. lanatus from southern Brazil to the Amazonian rain forest occurs along the southern Cerrado and Pantanal biomes (Carmignotto 2004). Phylogeography of Atlantic and Amazon rain-forest populations shows a closer relationship between the seasonal Atlantic forest and the southwestern Amazon populations (Costa 2003). C. lanatus is parapatric with C. philander and C. derbianus, and is replaced by C. philander in eastern Brazil (Eisenberg and Redford 1999; Emmons and Feer 1997). Sympatry with C. philander occurs in northern and central Brazil (central Amazonia, north of Mato Grosso, Goiás and Minas Gerais states), Guyana, and eastern Bolivia (Carmignotto 2004; Eisenberg 1989; Malcolm 1991a; Patton and Costa 2003; Patton et al. 2000). No contact occurs with C. derbianus in northwestern South America (Eisenberg 1989; Eisenberg and Redford 1999). In central Brazil, Peru, and Ecuador, C. lanatus is a nectar consumer and probable pollinator of Pseudobombax tomentosum and Quararibea cordata (Gribel 1988; Janson et al. 1981). The caecum of 1 individual contained hundreds of small seeds of Ficus luschnatiana in southern Brazil (Cáceres 2000, 2005). C. lanatus consumed fruits of Cecropia and in southern Brazil and Cáceres C. lanatus and et al. 1999). C. lanatus on a diet and (Bucher and Fritz 1977). was and was in central State, Brazil 1999). and but C. lanatus was never trapped in high 1999). C. lanatus is but in usually at 1977). 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J. and Costa during of the and 2 the for and was by of A.