Marmosops (Sciophanes) woodalli ( Pine, 1981 )

Ferreira, Claudilívia, Oliveira, Ana Cristina Mendes De, Lima-Silva, Luan Gabriel & Rossi, Rogério Vieira, 2020, Taxonomic review of the slender mouse opossums of the “ Parvidens ” group from Brazil (Didelphimorphia: Didelphidae: Marmosops), with description of a new species, Zootaxa 4890 (2), pp. 201-233 : 225-227

Marmosops (Sciophanes) woodalli ( Pine, 1981)

Marmosa parvidens woodalli Pine, 1981: 62 .

Marmosops pinheiroi: Voss et al. 2001: 49 (part); name combination.

Holotype. USNM 393532 consists of skin and skull of an adult female collected on 14 June 1968, Ronald H. Pine field no. 5054.

Type locality. Nova Área Experimental, Utinga (1º27’S, 48º29W; the wooded area surrounding the Belém waterworks), Pará, Brazil .

Geographic distribution. It occurs on the right bank of the Xingu River , including the Marajó Island in the state of Pará, extending east to the state of Maranhão and south to the state of Tocantins, Brazil ( Figure 5 ) .

Amended diagnosis. Dorsal coloration usually dark brown; tail length (LT: 92–158 mm) relatively longer in relation to head and body length ( HBL: 70–120 mm); ventral coloration white, with narrow lateral bands of graybased and white-tipped hairs arranged irregularly, which may or may not join on the throat and/or mid-chest and usually do not extend to the inner surface of the hind limbs; supraoccipital rounded in dorsal view (due to its con-vex shape); M3 with posterior portion of the stylar shelf more labially designed than the anterior portion (occlusal view); upper molars with preprotocrista and anterolabial cingulum seperated, not forming a continuous shelf along the anterior margin of the tooth crown; metaconule of the upper molars undeveloped; and talonid of the m4 usually tricuspid.

Morphological description. Marmosops woodalli has head body size ranging from 70 to 120 mm and a longer tail (LT: 92–158 mm; Tables 4 and 5 ); dorsal hairs 6–9 mm long; dorsal fur smooth, usually dark brown, being slightly lighter laterally; rostrum lighter than the top of the head, presenting grayish brown coloration, with some gray hairs; mask around the eyes blackish, with conspicuous posterior portion (except in UFMT 3975; UFPA-M 371, 384; MPEG 40177, 40178, 40181); cheeks with both white hairs and gray-based and white-tipped hairs; hands covered dorsally with whitish hairs; tail bicolor, brown dark (54%, n=79) or grayish-brown (46%, n=79); tail scales arranged in a spiral, each with three hairs inserted in the posterior margin; the central hair of the triplet clearly thick-er and more pigmented than the lateral ones; white venter, with narrow lateral bands of gray-based and white-tipped hairs arranged irregularly, which may or may not join on the throat and/or mid-chest and usually do not extend to the inner surface of the hind limbs (83.3%, n=88); hands with lateral spoon shaped carpal tubercle in adult males.

Craniodentally, M. woodalli exhibits zygomatic process of the squamosal widely overlapped dorsally by the jugal; lacrimal foramina may be exposed or not exposed in lateral view (less common); supraorbital margin slightly rounded with non-prominent crest; long nasal bones (extending slightly behind the lacrimal) and generally wider posteriorly than anteriorly (71.4%, n=49); supraoccipital with rounded shape in dorsal view, due to its markedly convex shape; paraoccipital process long and narrow; tympanic process of the alisphenoid with ventral surface oval or globose; cochlear fenestrae exposed in ventral view (except in UFMT 1251, 1258; MZUSP: AS 30; MPEG 40183, MPEG: SBER 02, 11, 15); palatine fenestrae absent, but diminutive perforations are present in the palatine and/or maxillary bones in 45% of the specimens (n=70); C1 with anterior and posterior accessory cusps in males and females; M3 with posterior portion of the stylar shelf more labially projected than the anterior portion (in oc-clusal view); upper molars with preprotocrista and anterolabial cingulum separated, not forming a continuous shelf along the anterior margin of the tooth crown (except in UFPA-M 376; MPEG 40167, 40296, MPEG: CAX 098, 293, MAR 428); metaconule of upper molars slightly developed; lower canine (c1) premolariform, (with posterior accessory cusps) subequal in height with first lower premolar (p1) (except in UFMT 3719, 3718, 3966; MZUSP: AS 30; MPEG: MAR 222, 428, 485, 1294; in which c1 is slightly higher than p1); m2 paraconid usually higher than the entoconid of m1 (70%, n=70); and talonid of the m4 usually tricuspid (83%, n=70; except in UFPA-M 382, 429; MNRJ 75117, 75121, 75122, 75139; UFMT 765; MPEG 40378, 40380; MPEG: CAX 293, MAR 589, PEB 12).

Geographic variation. Specimens of M. woodalli from the Cerrado biome (states of Maranhão and Tocantins) exhibit lighter dorsal fur (reddish brown) than specimens from forested areas (dark brown). In addition, specimens from the right margin of the Tocantins River have larger body size ( HBL = 110.1 ±17.8 mm) than those from the left bank ( HBL = 102.8±17.6 mm), and Student´s t tests showed that females from the right margin exhibit larger CBL, PL, MTR, UMS, WM4, BRC, BRJ, LMS, Lm4, and smaller TBO, while males exhibit larger PL, MTR, UMS, PPB, WET, POC, LMS, and Lm4 ( Table S5 ).

Comparisons with M. parvidens and other species of the “Parvidens” group ( Table 6). Comparisons between M. woodalli , M. marina and M. pinheiroi (s.s.) are provided above. Marmosops woodalli can be discriminated from M. parvidens by exhibiting dark brown dorsal coloration (versus slightly reddish brown); white (versus cream) ventral fur; lateral bands of gray-based hairs on the venter narrow and irregularly arranged, joining or not on the throat and/or mid-chest (versus usually absent, never joining together; Figure 4A and D ); rounded supraoc-cipital ( Figure 9A ), due to its markedly convex shape in dorsal view (versus slightly convex); tympanic process of the alisphenoid with ventral surface oval or globose (versus usually globose); posterior portion of the stylar shelf of the M3 more labially projected than the anterior portion (versus anterior and posterior portions equally projected labially); preprotocrista and anterolabial cingulum separated, not forming a continuous shelf on the anterior margin of crown of the upper molars (versus united, forming a continuous shelf on the anterior margin of crown the upper molars; Figures 7 B-C); and small accessory cusp between the metaconid and the entoconid of lower molars absent ( Figure 8 A-B).

Habitats and sympatry. Marmosops woodalli is geographically distributed in the Babaçu Forests of Maranhão, Xingu/Tocantins-Araguaia Humid Forests, Tocantins-Araguaia/ Maranhão Humid Forests, Marajó Várzea Forests, and Tropical Dry Forests ecoregions (sensu Olson et al. 2001). One specimen collected in Itapecuru Mirim, state of Maranhão, Brazil ( MPEG 45528), was associated to disturbed forest (secondary vegetation) according to its tag information. There is no record of sympatry between M. woodalli and other Marmosops species.

Natural history data. Mammary formula 4–1–4 = 9. Pregnant females were recorded in October, in Primavera, state of Pará, Brazil. In this locality, M. Aragona captured four specimens in live-traps (Sherman), three of which set on the ground (three individuals – UFMT 3975, 3978, and UFMT: TC 189) and one in the understory ( UFMT 3966); two other individuals were captured in pitfall-traps.

Specimens examined (n=165). BRAZIL - Maranhão: Bacabeira , 3°0’S, 44°19’W, 1 F, 1 M ( UFPA-M 966 , 980 ) ; Ferrovia Norte Sul , 5°35’S, 47°26’W, 1 M ( MZUSP: AS 30 ) ; Itapecuru Mirim , 3°24’S, 44°21’W, 1 M ( MPEG 45528 ) ; Miranda do Norte , 3°31’38”S, 44°30’46”W, 1 M ( UFPA: EFC 08-03 ) . Pará: Barcarena , 1°30’S, 48°37’W, 12 M, 2 F ( UFPA-M 345 , 368 , 369 , 371-374 , 376 , 377 , 379 , 380 , 381 , 382 , 384 ) ; Belém, Agropalma , 1°19’S, 48°28’W, 4 F, 2 M ( MPEG: AGPM 06 , 11 , 33 , 38 , 109 , 152 ) ; Canaã dos Carajás , 6°32’S, 49°51’W, 1 M ( MZUSP: CA 20 ) ; Caxiuanã , 1°55’S, 51°22’W, 9 M, 3 F, 4? ( MPEG 40167 , 40169 , 40171 , 40172 , 40298 ; MPEG: MAR 222 , 428 , 589 , 683 , 1294 ; CAX 098, 186, 209, 293, 360, 407) ; Estrada de Ferro Carajás , 6°16’S, 50°34’W, 7 M (UFPA-M 423, 426, 429, 458, 459, 487, 521) ; Chaves, Fazenda Tauari, Ilha de Marajó , 0°39’S, 50°11’W, 5 M, 2 F ( MPEG 40388 , 40389 , 40390 ou 40392 (double), 40391, 40393, 40394, 40395) ; Linha de Transmissão do Tucurui-Xingu (Jurupari), 3°42’0”S, 49°41’59”W, 2 M, 1 F ( MZUSP: LTBM 02 , 09 ; LTC 24 ) ; Marabá , 5 M, 3 F ( UFPA-M 257 , 347 , 355 , 356 , 358 , 382 , 1824 , 1907 ) ; Marabá, Flona Tapirapé , 5°49’0”S, 50°30’60”W, 3 F, 7 M, 7? ( MPEG 40174- 40179 , 40181 , 40183 ; MPEG: PSA 065 , 087 , 154 ; UFMT 1241, 1245, 1247, 1251, 1252, 1258) ; Melgaço, Estação Científica Ferreira Penna , 1°41’33”S, 50°28’43”W, 5 M, 4 F, 4? ( MPEG 40375-40378 , 40380 , 40381-40384 , 40385- 40387 ; MPEG: EPM 095 ) ; Parauapebas , 6°4’S, 49°54’W, 1 M ( MPEG 38941 ) ; Peixe-boi , 01º05’53”S 47º19’54”W, 2 F, 1 M ( MPEG: PEB 06 , 12 , 25 ) ; Primavera , 0°57’S, 47°6’W, 7 M, 6 F, 2? ( UFMT 765 , 3703 , 3704 , 3716 , 3718 , 3719 , 3964 , 3966 , 3975 , 3977-3979 , 3981 ; UFMT: TC 178 , 189 ) ; São Felix do Xingu , 7°1’S, 52°21’W, 5 M, 3 F ( MPEG 42460 , 42721 , 42723 , 42725 , 42726 , 42728 , 42730 , 42793 ) ; Santa Barbara , 1°12’26”S, 48°16’14”W, 6 M, 1 F ( MPEG: SBER 01 , 02 , 07 , 11 , 15 , 17 , 32 ) ; São Geraldo do Araguaia 6°23’S, 48°33’W, 2 M ( MNRJ 75242 , 75244 ) ; Senador José Porfírio , 3°51’S, 51°51’W, 6 M ( MPEG 41851 , 41862 , 42447 , 42458 , 42459 , 42460 ) ; Tucu-ruí, 3°42’S, 49°42’W, 1 F, 1 M ( MPEG 12296 , 12297 ) ; Nova Área Experimental, Utinga, Belém , 1º27’S, 48º29’W, 1 F ( USNM 393532 , photograph of the holotype) ; Utinga, Parque Ambiental de Belém , 1°25’33”S, 48°26’39”W, 6 M, 9 F, 1? ( MPEG 8787 , 12701 , 12960 , 15257 , 38654 , 38657 , 38658 , 38666 , 38667 , 38669 , 38671 , 39695 , 39697 , 39698 , 39706 ; MPEG: PAB 017 ) ; Viseu , 1°10’58”S, 46°17’32”W, 1 M ( MPEG: VIS 45 ) . Tocantins: Goiatins , 7°47’53”S, 47°16’40”W, 2 M, 1 F ( MNRJ 75121 , 75122 , 75136 ) ; Ribeiro Gonçalves , 7°47’48”S, 47°16’47”W, 1 M, 2 F ( MNRJ 75117 , 75139 , 75140 ) .

Others specimens examined: Marmosops parvidens (n=34). BRASIL - Amazonas: Balbina , 1º53’S 59º28’W, 2 F ( MZUSP 22940 ; MPEG 22141 ) ; Urucará , 2º23’S, 57º38’W, 2 M ( MPEG 40065 , 40068 ) . Pará: Floresta Estadual Faro (Flota Faro), left bank of Rio Nhamundá , 1°16’44”S, 58°2’24”W, 2 F, 4 M, 1? ( MPEG 39959 , 39963 , 30075 , 39976 , 39982 , 39984 ; MPEG: CN 080 ) ; Óbidos, Flota Trombetas, 0°58’S, 55°31’W, 3 M, 4? ( MPEG 40401 , 40403 , 40404 ; MPEG: CN 182 , 186 , 207 , 210 ) ; Oriximiná, Porto Trombetas , 1º49’S 56º30’W, 6 M, 6 F ( MPEG 39802 , 39807 , 40070 , 40074 , 42404 , 42422 , 42364 , 42372 , 42405 , 42424 , 42437 , 42441 ) ; Terra Santa , 2°6’S, 56°29’W, 2 M, 1 F ( MPEG 40081-40083 ) . GUYNA: “Hyde Park, 30 miles up the Demarara River,” Demerara-Mahaica ( FMNH 18545 , photograph of the holotype) .

Figures

FIGURE 4. Dorsal and ventral pelage of Marmosops species: A, M. marina sp. nov. (UFMT 4078 ♁, Holotype); B, M. parvidens (MPEG 39976 ♁); C, M. pinheiroi (UFPA 40026 ♁); D, M. woodalli (MPEG 40388 ♁). Scale bar 50 mm.

FIGURE 5. Distribution (polygons) and collection localities (symbols) for Marmosops species of the “Parvidens” group in- cluded in this report: M. parvidens (yellow circles); M. pinheiroi (stricto sensu; green circles); M. woodalli (red circles); M. marina sp. nov. (blue circles); sympatry between M. parvidens and M. pinheiroi (s. s.; crosses); type localities (stars). The ranges of M. parvidens and M. pinheiroi were partially based on Voss et al. (2001; 2013) and Díaz-Nieto & Voss (2016). The range of M. woodalli was partially based on Nascimento et al. (2015).

FIGURE 7. Occlusal view of upper molars M2–M4 of Marmosops species. A, M. marina sp. nov (UFMT 1427, Paratype ♁); B, M. parvidens (MPEG 40403 ♁); C, M. woodalli (MPEG 38667 ♁). Abbreviations: alci, anterolabial cingulum; prprcr, preprotocrista. Note the presence of a continuous shelf along the anterior margin of crown of the upper molars formed by the preprotocrista and the anterolabial cingulum in both M. marina and M. parvidens, which is narrow in the former (constriction indicated by arrows) and wide in the latter species. This condition is absent in M. woodalli. Scale bar 1.65 mm.

FIGURE 8. Lingual view of left lower molars m1–m3 of Marmosops species. A, M. woodalli (UFMT 3719 ♁); B, M. parvidens (MPEG 40404 ♁). The arrow indicates a small accessory cusp between the metaconid and the entoconid. Abbreviations: mecd, metaconid; encd, entoconid. Scale bar 1 mm.

FIGURE 9. Dorsal view of the braincase of Marmosops species. A, M. woodalli (UFMT 3966 ♁); B, M. pinheiroi (MPEG 40017 ♁). Abbreviations: ip, interparietal; par, parietal; sup, supraoccipital. Note the rounded and markedly convex shape of the supraoccipital in M. woodalli and the slightly convex shape of this bone in M. pinheiroi. Scale bar 5 mm.