Marmosa (Micoureus) budini, Thomas, 1920

MARMOSA (MICOUREUS) BUDINI THOMAS, 1920

Marmosa budini Thomas, 1920: 195 . Type locality ‘ Altura de Yuto , Rio San Francisco.’

Marmosa constantiae constantiae : Tate, 1933: 75 (part); name combination.

Marmosa constantiae budini : Tate, 1933: 76; name combination.

aHolotype (BMNH 20.1.7.134) of Marmosa (Micoureus) budini (young adult).

bHolotype (BMNH 3.7.7.157) of Marmosa (Micoureus) constantiae (mature adult).

Marmosa constanciae budini : Olrog, 1960: 404; incorrect spelling.

Marmosa constanciae Mares et al., 1981: 160 ; name combination and incorrect spelling.

M [icoureus]. constantiae : Gardner & Creighton, 1989: 4 (part); name combination.

Marmosa (Micoureus) cinerea budini : Anderson et al., 1993: 14; name combination.

Micoureus constantiae budini : Anderson, 1997: 9 (part); name combination.

Micoureus constantiae constantiae View in CoL : Anderson, 1997: 9 (part); name combination.

Type information: The holotype is deposited in the Natural History Museum, BMNH 20.1 .7.134, (original number 714), adult male (young adult), with skin and skull in good condition, collected on 23 July 1919 by E. Budin, ‘ Rio San Francisco , Altura de Yuto,’ Jujuy, Argentina, 500 m elev. (Supporting Information, Fig. S1) .

Geographic distribution: This species occurs from the central region of Bolivia (Chaparé Province, Cochabamba; Ñuflo de Chaves Province, Santa Cruz) to north-western Argentina (Tucumán Province), extending to the east in the central-eastern portion of Paraguay (Department of San Pedro) and central-western portion of Mato Grosso do Sul State (Aquidauana) in Brazil ( Fig. 5). According to our records, the species does not occur in sympatry with any other Micoureus species .

Habitat: The distribution of Marmosa budini extends across multiple ecoregions ( Olson et al., 2001), such as Cerrado, Chaco (savannic and humid), Pantanal, Parana / Paraiba interior forests, Bolivian Yungas, Andean Yungas, south-western Amazonian moist forests, Chiquitania dry forests and Bolivian montane dry forests.

Emended diagnosis: Dorsal fur usually long (8–13 mm) and woolly, with light greyish-brown to olivaceous coloration; ventral coloration yellowish-cream, with narrow lateral bands of grey-based hairs the never join in the midline of the venter; caudal scales arranged in spiral series, with number of hairs varying from four to seven per scale on the dorsum of the tail and from three to six per scale on the venter, which decrease in number as they advance to the distal part of the tail; posterior margins of nasals rounded or squared, never w-shaped; developed supraorbital ridges, only laterally projected; temporal ridges moderately convergent; interparietal bone narrow anteriorly and medially, with posterior region abruptly expanding laterally; well-developed palatine fenestrae; cochlear fenestra exposed in ventral view; incipient posterior accessory cusp in the canine may be present, especially in females; upper molars with complete posterior lingual cingulum and inferior molars with complete labial cingulid.

Morphological description: Marmosa budini is a small-sized species when compared to others of the subgenus Micoureus , with head and body length ( HBL) 122 to 221 mm and tail longer than HBL ( Table 8); rostrum lighter than the dorsum of the head, covered with yellowish buffy-based and black-tipped hairs;

aHolotype ( BMNH 5.11.1.25) of Marmosa (Micoureus) demerarae (young adult).

bHolotype ( BMNH 20.7.14.41) of Marmosa (Micoureus) limae (mature adult).

cHolotype ( BMNH 20.7.14.39) of Marmosa (Micoureus) domina (mature adult).

dJunior synonyms of Marmosa (Micoureus) demerarae .

well-defined facial mask, wider in the upper region ( Fig. 6A); cheeks yellowish-cream; seven to eight genal vibrissae (generally eight), three of which are long and black, and the remaining short and yellowish; dorsal hairs 8–13 mm long; dorsal fur olivaceous greyish-brown, somewhat lighter on the laterals of the body; ventral fur yellowish-cream, with lateral grey-based hairs restricted to the thorax and abdomen; ventral grey-based bands never joining at the midline of the venter ( Fig. 7); mammary formula unknown; medial and lateral carpal tubercles present in mature adult males; body fur at the base of the tail 14–27 mm; tail light to dark brown, part-coloured, usually with the half distal portion depigmented; tail scales arranged in spiral series; from the posterior margin of each scale emerges four to seven hairs on the dorsum of the tail and three to six hairs on the venter (the number of scale hairs decrease distally along the tail); prehensile ventral surface of the tail tip on average 35 mm long.

Craniodentally, M. budini has a short and broad rostrum when compared to other species of subgenus Micoureus herein examined ( Tables 6, 7); long nasal bones that extend beyond the lacrimal bones, with rounded to squared posterior margins, never w-shaped; developed supraorbital ridges, only laterally projected; temporal ridges moderately convergent ( Fig. 8A); interparietal bone narrow anteriorly and medially, with posterior region abruptly expanding laterally ( Fig. 9A); two lacrimal foramina exposed in lateral view; infraorbital foramen aligned with the third upper premolar; jugal extends over the squamosal to form the zygomatic process of the squamosal; anterior margin of incisive foramina usually aligned with the third upper incisive and posterior margin aligned with the upper canine; palatine fenestrae present, consisting of two well-developed rounded perforations ( Fig. 10A); tympanic process of alisphenoid globular, without anteromedial process ( Fig. 11); cochlear fenestra exposed in ventral view; mental foramina aligned with either the first lower premolar or the first lower molar; upper canine lower when compared to other species of Micoureus , with or without incipient posterior accessory cusp, generally in a 52% absent, 48% small and laminar (N = 219); the specimen UFMT 3428 exhibits secondary foramen ovale.

b 66% absent, 34% small and acute (N = 50); the specimens MPEG 40200 and MPEG: PSA210 exhibit secondary foramen ovale.

females; crowns of upper second to five incisors (I2–I5) triangular, longer in I5; upper molars with complete posterior lingual cingulum; lower molars with complete labial cingulid ( Fig. 12A, C).

Comparison with other Micoureus species: Marmosa budini differs from the other species of Micoureus morphologically analysed in this report by having a smaller body size ( HBL: 122–221 mm and LT: 173– 255 mm; Table 8); supraorbital ridges only laterally projected (versus laterally and dorsally projected; Fig. 8); interparietal bone narrow anteriorly, with medial and posterior region abruptly (versus moderately to gradually) expanding laterally ( Fig. 9); palatine fenestrae consisting of two well-developed rounded perforations (absent in other species; Fig. 10); upper molars with complete posterior lingual cingulum (also observed in some upper molars of M. regina ) and lower molars with complete labial cingulid ( Fig. 12).

Externally, Marmosa budini has a dorsal fur that is as long as that of M. demerarae (8–13 mm) and M. constantiae (8–14 mm), longer than that of M. regina (8 mm) and shorter than that of M. paraguayana (11–15 mm). It also differs from the other species by exhibiting denser body fur and from M. regina by having woolly (vs. smooth) body fur. Body fur at the base of the tail is short in M. budini (20.6 ± 3.4 mm, N = 30) and M. regina (up to 20 mm), whereas it is moderately longer in M. constantiae (33.7 ± 8.3 mm, N = 237) and M. demerarae (35.8 ± 5.8 mm, N = 59) and much longer in M. paraguayana (44.1 ± 8.5 mm, N = 10; Table 8).

The facial mask is well-defined, with wider upper region in M. budini and M. regina , whereas it is not well-defined in M. constantiae and M. paraguayana . Although the facial mask is also well-defined, with a wider upper region in M. demerarae , it differs from the previous species by exhibiting a sharpened posterior margin ( Fig. 6). The ventral fur is yellowish-cream in Marmosa budini , with narrow lateral bands of grey-based hairs that never unite on the midline of the venter ( Fig. 7A). On the other hand, the ventral fur varies from yellowish-cream to yellowish-buff in M. constantiae ( Fig. 7B, C) and it is yellowish-cream in the M. regina , with lateral bands of grey-based hairs that may or may not join in the midline of the chest or abdomen in the former species and may broaden (but never join medially) in the abdomen in the latter species. Finally, M. paraguayana and M. demerarae ( Fig. 7D) has a yellowish-cream and yellowish-cream to yellowish-buff ventral coloration, respectively, with dark grey-based hairs throughout the venter, except the chin.

The part-colour pattern of the tail is present in all species. Usually, M. budini exhibits the distal half of the tail fully depigmented, with the ventral region slightly lighter in the proximal direction; M. paraguayana exhibits the distal two-thirds of the tail completely depigmented; in M. demerarae , the tail varies from completely pigmented to depigmented in the most distal part, presenting a speckled pattern; finally, M. constantiae has a tail that varies from strongly depigmented in its two-thirds’ distal portion to slightly depigmented only in the ventral portion of the distal half, this last pattern being less common.

The caudal scales are arranged in a spiral and vary only in the amount of hairs associated with them. In M. budini , the amount of hairs on each scale varies from four to seven dorsally and from three to six ventrally. In M. paraguayana , the number of hairs per scale varies from three to five dorsally and from three to four ventrally. The other species herein analysed always has three hairs per scale in both dorsum and venter of the tail. In all species examined, the number of hairs per scale decreases as they advance to the distal part of the tail.

In relation to the skull, Marmosa budini has moderately convergent temporal ridges, differing from M. demerarae and M. constantiae that have moderately to strongly convergent temporal ridges, usually forming a sagittal crest in the latter species ( Fig. 8). By contrast, M. paraguayana has parallel temporal ridges. Marmosa budini has a globular tympanic process of the alisphenoid that is similar in M. paraguayana and M. demerarae , but distinct from M. regina whose process is slightly compressed ( Fig. 11). This character varies in M. constantiae , which has the two patterns cited above. The anteromedial process of the tympanic process on the alisphenoid is absent in M. budini and M. regina , usually absent in M. demerarae and M. constantiae and present in M. paraguayana (small and laminar). The cochlear fenestra is exposed in ventral view in M. budini and M. regina , usually exposed in M. demerarae and M. constantiae and not exposed in M. paraguayana . In some cases, the non-visualization of the cochlear fenestra is associated with the expansion of the mastoid bone or the tympanic process of petrosal. Dentally, M. budini , M. constantiae and M. demerarae may have an incipient posterior accessory cusp on the upper canine, especially the females.

Intraspecific morphological variation: Specimens of M. budini from Argentina (Salta and Jujuy) have a lighter dorsal coloration in relation to the specimens from Bolivia. The tail coloration does not follow a defined pattern and can present depigmentation for up to 80% of the tail length. This was observed throughout the geographic distribution of the species, although most of the specimens examined only had depigmentation on the distal half of the tail. Young individuals may present ventral fur with salmon tones. The specimen MHNKM 2085 (male, young adult) collected in Bolivia (Cordillera Province, Tierra Nuaves) does not present palatine fenestrae.

Reproduction information: Mammary formula unknown. Three adult females (mature adults, BMNH 8.4 .4.3, BMNH 26.12 .4.86 and MHNKM 2933 ), collected in the provinces of Santa Cruz and Cordillera in Bolivia, were captured with seven to 10 young attached to the nipples in the months of November and December .