Gracilinanus microtarsus ( Wagner, 1842 )

Lóss, Simone, Costa, Leonora Pires & Leite, Yuri L. R., 2011, Geographic variation, phylogeny and systematic status of Gracilinanus microtarsus (Mammalia: Didelphimorphia: Didelphidae), Zootaxa 2761, pp. 1-33 : 23-28

Gracilinanus microtarsus ( Wagner, 1842)

Didelphys microtarsus Wagner, 1842: 359 . Type locality: “Ypanema” (= Floresta Nacional de Ipanema, 20 km NW Sorocaba, São Paulo, Brazil, 23°26'7"S 47°37'41"W 701 m; see Costa et al. 2003) (locality 53, Figure 11 ). Type specimen: the lectotype designated by Tate (1933) is Vienna 48A, collected by Johann Natterer on October 2nd, 1891, cataloged at the Naturhistorisches Museum, Vienna, Austria. According to Tate (1933), the description was apparently based upon at least three specimens (Vienna 48, 48A and 48B), and Hershkovitz (1992) mentioned a series of eight specimens under the number 48, citing Pelzeln (1883).

Marmosa herhardti [incorrect original spelling] Miranda-Ribeiro, 1936: 382. The corrected original spelling is Marmosa ehrhardti Miranda-Ribeiro, 1936 , according to the ICZN (1999, Article 32.5), since the author was naming this species after Mr. Ehrhardt ( Miranda-Ribeiro 1936, page 382). Type locality: “Humboldt” (currently Curupá), Santa Catarina, Brazil 26°26’S 49°14’W, 62 m (locality 80, Figure 11 ). Type specimen: the lectotype was designated by Miranda-Ribeiro (1955:416) under the number MN 1266 (skin and skull). It is a young male collected on December 23rd, 1915, bought from Mr. Ehrhardt (field number 1). Paralectotypes: MN 1264 and 1265, collected on December 25th, 1915; MN1262, collected on September 18th, 1916; MN 1259, 1261, 1263, and 1266, collected on December 23rd, 1915. All bear the same field number (15), and were bought together with the lectotype. There are cases of ambiguous associations among skins and skulls of the type series, as remarked by Langguth et al. (1997).

Geographic distribution. Gracilinanus microtarsus occurs in eastern Brazil, in the states of Bahia, eastern Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina, and northern Rio Grande do Sul ( Figure 11 ). Recent records ( Pereira & Geise 2007; Geise & Astúa 2009) extended the northern most limit of its distribution to two localities in the central region of Bahia: Lençóis, at Chapada Diamantina (locality 1) and Mucugê. It is found in areas ranging from sea level to 1,800 m, occurs mainly in the Atlantic forest biome, but also in Cerrado formations bordering the Atlantic Forest. Gracilinanus microtarsus occurs in sympatry with Gracilinanus agilis at Lagoa Santa, Parque Estadual do Rio Preto, Belo Horizonte (localities 32, 29, and 36, respectively), Felício dos Santos, and Diamantina, all in Minas Gerais State. Specimens identified as “large microtarsus ” are distributed in some localities in Rio de Janeiro and São Paulo, being sympatric with phenotype “small microtarsus ” at Teresópolis, Rio de Janeiro (locality 22). Specimens of “ ehrhardti ” occur in Paraná, Santa Catarina, and Rio Grande do Sul. Specimens of “small microtarsus ” are the most widespread, representing the remaining distribution.

Emended description. External morphology ( Figure 12 ): ventral margin of rhinarium with two shallow grooves on each side of median sulcus; eyes surrounded by mask of dark fur extending to muzzle and ears, and contrasting in color with paler fur of cheeks and rostrum; pale spot above eye absent; dark mid-rostral stripe absent; ears large, translucent, yellow-orange at the base and brown toward the tip; tragus large; rostral pelage similar to the cheeks, paler than the dorsal pelage; gular gland present in adult males and females; dorsal fur ca. 10 mm-long, soft, with two color bands, dark gray at the base and varying from brown-light to brown-reddish distally; dorsal guard hairs ca. 12 mm; ventral fur self-colored, cream-yellowish from mouth to the chin or to the lower pectoral region; ventral fur of arms gray-based, yellow-tipped; manus covered by short cream hairs dorsally; manual digits III and IV subequal and longer than adjacent digits (II and V); manual claws shorter than fleshy digital pads; central palmar surface of manus sparsely tubercular; lateral carpal tubercles present in adult males; radius crest well developed in adult males; pedal digit IV longer than adjacent digits III and IV; pedal epithelium covered by short hairs dorsally, varying from cream to light-brown; pouch absent; mammary complement 6–1–6 = 13, with six teats on each side of the venter, from thoracic to inguinal portion, and one central teat on inguinal region; cloaca present; tail bicolored, dark above and paler below, or unicolored; tail hair brown; caudal scales in distinctly annular series; three hairs of equal thickness projecting from the posterior margin of each caudal scale; naked prehensile surface at distal end of tail present.

Skull and mandible ( Figure 13 ): rostral process of premaxillae present; palatal process of premaxillae contacts C1 alveolus on each side; nasal tips extend anterior to I1; postorbital processes of frontal absent or indistinct; temporal margin present, poorly or well developed; interorbital region varying from convergent anteriorly to straight; sagittal crest absent; incisive foramen reach posterior edge of canines, or extend beyond posterior edge of canines in some specimens; maxillopalatine fenestrae large, relative size equal to or larger than three molars; palatine fenestrae present; posterolateral palatal foramen not extending lingually to M4 protocone; posterolateral palatal foramen smaller than palatine fenestrae; maxillary and alisphenoid not in contact on orbital floor; transverse canal foramen present; extracranial course of mandibular nerve enclosed by anteromedial strut of alisphenoid bulla; ectotympanic suspension direct; paroccipital process small and rounded; alisphenoid tympanic process inflated, with alisphenoid bulla strut originating on the medial portion or apex of alisphenoid; dorsal margin of foramen magnum formed by supraoccipital and exoccipitals; two mental foramina on lateral aspect of each hemimandible.

Dentition: unworn crowns of I2–I5 simetrically rhomboidal, slightly increasing in breadth from front to back (I2 ≤ I5); unworn C1 usually without accessory cusps; P1 present, smaller than posterior premolars; P2 distinctly taller than P3; P2 and P3 with anterior and posterior cutting edge; upper molars strongly dilambdodont and highly carnassialized, increasing in width (transverse dimension) from front to back (width M1 <width M4); ectoflexus deep on M1 and M2, and shallow or absent on M3; preprotocrist and anterolabial cingulum joined to form a continuous shelf along the margin of M3; distinct lingual cusp on lower incisors; c1 procumbent, usually with small posterior accessory cusp; p2 distinctly taller than p3; m3 hypoconid salient labially; entoconid large and developed on m1-m3; hypoconulid similar to entoconid.

Post cranium: deltoid tuber on humerus well developed in adult males and poorly developed in females; medial epicondyle well developed, surpassing the coronoid fossa in males, but not in females; astralagus and calcaneus joined.

Remarks. Until few years ago, two synonyms were recognized under G. microtarsus . The first, G. guahybae ( Tate, 1931) , was described as a subspecies of G. microtarsus from “ Ilha de Guayba” (= Guaíba), Rio Grande do Sul, Brazil. This subspecies was part of this genus until systematic revision by Voss et al. (2005) allocated it to the new genus Cryptonanus . The second synonym, G. ehrhardti , is based on a new species described by Miranda- Ribeiro (1936) and it was considered as such until Cabrera (1958) suggested that it should become a junior synonym, since it was indistinguishable from G. microtarsus using morphological characteristics and geographic distribution. Voss et al. (2005) referred to the nominal taxon G. e h r h a rd t i as incertae sedis because they did not examine specimens of the type-series, catalogued at the Museu Nacional, Rio de Janeiro, Brazil. As we discussed above, our results led us to consider G. ehrhardti a junior synonym of G. microtarsus .

Intraspecific variation. Gracilinanus microtarsus exhibits marked intraspecific variation, treated here as three phenotypes, as described in material and methods. Specimens of “large microtarsus ” exhibit self-yellow ventral pelage from mouth to lower thorax, and gray-based hair with yellow tips from lower thorax to tail base. Specimens of “small microtarsus ” and “ ehrhardti ” have gray-based hairs from chin to tail base. In addition, “ ehrhardti ” shows unicolored tail, while specimens of the other two phenotypes have bicolored tail.

Among cranial differences observed on Gracilinanus microtarsus phenotypes, most are present at the interorbital region ( Figure 14 ). The temporal margin is poorly developed, the interorbital edge is angular, without crests or with poorly developed crest in specimens of “small microtarsus ” and “ ehrhardti ”. Specimens of “large microtarsus ” show temporal margin projecting over interorbital edge as a prominent crest, extending through parietal and ending at the supraorbital edge. This characteristic is more evident in adult male specimens. Specimens of “large microtarsus ” show straight interorbital region, while in “small microtarsus ” and “ ehrhardti ” the interorbital region is convergent anteriorly. Specimens of “small microtarsus ” and “large microtarsus ” have small incisive foramen, reaching the posterior edge of canines, while in “ ehrhardti ” the foramen is moderately large, extending beyond the posterior edge of canines, but not surpassing the anterior edge of first deciduous premolar. The alisphenoid tympanic process is inflated, with alisphenoid bulla strut originating on the medial portion of alisphenoid in “small microtarsus ” and “ ehrhardti ”. In specimens of “large microtarsus ”, the alisphenoid tympanic process is moderately inflated, oval, and its strut originates at the alisphenoid apex ( Figure 5 A–D ).

Comparisons. G. microtarsus and G. agilis can be distinguished by some characteristics described by Costa et al. (2003). Given their similarity, specimens are often misidentified by collectors in the field. When compared to G. microtarsus , G. agilis has yellow ventral pelage, with gray-based hairs restricted to the lower pectoral and abdominal area, narrower blackish mask surrounding the eyes, gradual color change between muzzle and dorsum, and posterolateral palatal foramen larger than the palatine fenestrae. P2 and P3 have similar sizes in G. agilis , but P2 is distinctily taller than P 3 in G. microtarsus ( Figure 5 E–G).

Sexual dimorphism. Adult males from some localities (1—Lençóis, state of Bahia; 18—Pedra Roxa, Caparaó, state of Espírito Santo; 58, 61—Ibiúna, 57—Piedade and 53—Ipanema, state of São Paulo) show well-developed radius crest, and a triangular shaped ulnar tubercle developed on the pisiform. Females show a flat radius, with no ossified protuberance and no tubercle on the psiform. Males show deltoid tubercle and medial epicondyle more developed than females.

Natural history. Gracilinanus reproduces during periods of high rainfall, from October to March ( Passamani 2000), or from September to March ( Martins et al. 2006a). Partial semelparity has been registered in males, according to Martins et al. (2006b). Tate (1933) suggested that his “ Microtarsus Group” has terrestrial habits, with short claws and small hindfeet. Ecological studies using live-traps at different forest layers revealed that animals of the genus Gracilinanus are preferentially arboreal ( Grelle 2003; Vieira & Monteiro-Filho 2003; Vieira 2006) and feed on the ground, when food is scarce in the understory. Astúa de Moraes (2004) documented the use of arboreal strata by Gracilinanus , and observed scapular modifications that might be related to the arboreal locomotion.

Although commonly documented as insectivore, studies on food habits suggest that the genus has an omnivorous diet (Vieira & Astúa de Moraes 2003; Martins & Bonato 2004, Santori & Astúa de Moraes 2006; Araújo et al. 2010), and other studies have confirmed the presence of seeds, some of them with elevated germination success ( Leite et al. 1996; Vieira & Izar 1999). In addition to feeding on insects and fruits, they eat arachnids and mollusks ( Martins & Bonato 2004).

The food-niche width of males and females of G. microtarsus vary according the seasons of the year. Between sexes, the average food-niche widths were similar in the trimesters corresponding to the warm–wet season, but were significantly different in the trimesters corresponding to the cool–dry season, becoming broader in the males and narrower in the females ( Martins et al. 2006c). Physiological information on this species can be found in Cooper et al. (2009).

Much remains to be learned about the taxonomy, distribution and natural history of Gracilinanus microtarsus . The species is poorly represented in museum collections, and this can be attributed to its low density at some localities along its distribution and to inadequate methods of capture. Studies based on nuclear DNA, and on increasing numbers of specimens analyzed, covering its geographic distribution would be useful to re-evaluate the results observed in G. microtarsus and the taxonomic decisions proposed here.

Figures

FIGURE 11. Map of eastern Brazil showing known records of Gracilinanus microtarsus based on specimens examined. Localities are keyed to numbered entries in the Appendix. The symbols represent: (●) “ small microtarsus ”, (․) “ large microtarsus ” and (˔) “ ehrhardti ”.

FIGURE 12. Dorsal and ventral views of skins of Gracilinanus microtarsus. A and C, MZUSP 29159 (“ small microtarsus ”, male, age class 5), B and D, UFMG 2536 (“ large microtarsus ”, male, age class 6. Scale = 10 mm.

FIGURE 13. Dorsal and ventral cranial views (above), and lateral cranial and mandibular lateral views (below) in Gracilinanus microtarsus (“ large microtarsus ”, male, age class 6) (UFMG 2536). Scale = 5 mm.

FIGURE 14. Dorsal (above) and ventral (below) cranial views of “ small microtarsus ” (left, MZUSP 29164, male, age class 5), “ large microtarsus ” (middle, UFMG 2536, male, age class 6), and “ ehrhardti ” (right, MNHCI 4322, male, age class 5). Scale = 5 mm.

FIGURE 5. A – D Ventral and lateral view of left tympanic region of “ small microtarsus ” (A and C, MZUSP 29159) and “ large microtarsus ” (B and D, UFMG 2535), illustrating morphological differences of the alisphenoid tympanic process in adult males. Scale = 2 mm; E – G Lateral cranial view of C 1 - P 3 in G. microtarsus (“ small microtarsus ”) (E, MZUSP 29159), G. agilis (“ midwest ”) (F, UFMG 2487) and Cryptonanus sp. (G, FURB 9362) illustrating taxonomic differences in the relative height of P 2 versus P 3 in adult males. Scale = 1 mm; H – I Ventral view of the carpus, manus, radius, and ulna in Gracilinanus microtarsus showing differences on lateral carpal tubercle (lct). Specimens of “ small microtarsus ” (H, MZUSP 31009) and “ large microtarsus ” (I, MZUSP 30717), both adult males. Scale = 2 mm; J – K Anterior view of humerus in “ large microtarsus ” (J, MZUSP 30641) and “ small microtarsus ” (K, MZUSP 29161), showing variation in deltoid tuber (dt) and medial epicondyle (me) in adult males. Scale = 2 mm; L – M Lateral view of the carpus, manus, radius, and ulna in Gracilinanus microtarsus showing differences on radius crest (rc). Specimens of “ large microtarsus ” (L, MZUSP 30717) and “ small microtarsus ” (M, MZUSP 31009), both adult males. Scale = 2 mm.