Marmosops pakaraimae, Voss & Lim & Díaz-Nieto & Jansa, 2013

Voss, Robert S., Lim, Burton K., Díaz-Nieto, Juan F. & Jansa, Sharon A., 2013, A New Species of Marmosops (Marsupialia: Didelphidae) from the Pakaraima Highlands of Guyana, with Remarks on the Origin of the Endemic Pantepui Mammal Fauna, American Museum Novitates 2013 (3778), pp. 1-28 : 6-16

Marmosops pakaraimae , new species

Figures 2 –6

HOLOTYPE: The holotype ( ROM 115129 ; original number F46739 ) consists of the skin, skull, postcranial skeleton, and preserved tissues of an adult male collected by Burton K. Lim and Deirdre M. Jafferally on 26 February 2003 at “Second Camp” (5°17′N, 60°45′W, 800 m above sea level) on Mount Roraima , Cuyuni-Mazaruni Region, Guyana.

DISTRIBUTION: Known from five localities, of which three are in the Pakaraima Highlands of western Guyana and two are in the adjacent highlands of eastern Venezuela (fig. 1). Recorded elevations at these localities range from 800 to about 1500 m above sea level.

DESCRIPTION: A small species of Marmosops (measurements in table 4) with all the diagnostic qualitative traits of the genus ( Voss and Jansa, 2009: 134–137). Body pelage dark brown (near Dark Umber) middorsally but indistinctly paler laterally; superficially whitish ventrally (the ventral coloration contrasting abruptly with the brownish flanks), but hairs of throat, chest, and abdomen uniformly gray-based (only the apex of the chin, the oral margins, and the scrotum have self-white fur). Gular gland apparently absent. Manus covered dorsally with pale hairs in some specimens (e.g., ROM 114698), but metacarpals distinctly darker than digits in others (e.g., ROM 115129); lateral carpal tubercles large and spoon shaped ( Voss et al., 2001: fig. 20) in all examined adult males; forearm with both proximal and distal antebrachial vibrissae (Díaz-N. et al., 2011: fig. 5b). Mammary formula unknown (no female specimens examined). Scrotal epithelium unpigmented and covered with short self-white hairs. Hind foot covered dorsally with pale hairs; hypothenar and fourth interdigital plantar pads separate (with discontinuous dermatoglyphs; Díaz-N. et al., 2011: fig. 4B). Tail substantially longer than combined length of head and body (mean LT/HBL × 100 = 150%), dorsal surface dark (probably grayish in life) from base to tip, but ventral surface indistinctly paler (especially near the base).

Nasal bones long (extending well behind the lacrimals) and much wider posteriorly than anteriorly. Interorbital region very broad, the supraorbital margins rounded (without distinct beads); postorbital processes absent. Lacrimal foramina concealed from lateral view inside anterior orbital margin; fenestra in squamosal-parietal suture consistently present and large; subsquamosal foramen anteroposteriorly elongated (exposing the petrosal well behind the sulcus for the prootic sinus; Díaz-N. et al., 2011: fig. 6B). Premaxillary rostral process long and well developed; incisive foramina short, not extending posteriorly behind canines; palatine fenestrae absent.

Upper canine (C1) short, with both anterior and posterior accessory cusps. Second upper premolar (P2) slightly but consistently taller than third upper premolar (P3); P3 oblique (not in line with C1–P2, its anterior base lingual to the posterior base of P2). Upper third molar (M3) anterolabial cingulum narrowly continuous with preprotocrista (anterior cingulum complete). Lower canine (c1) premolariform (procumbent, with posterior accessory cusp) and small, subequal in height to lower first premolar (p1); anterolingual accessory cusp (Díaz-N. et al., 2011: fig. 9B) absent. Unworn fourth lower molar (m4) talonid with three distinct cusps (hypoconid, hypoconulid, and entoconid).

MORPHOLOGICAL COMPARISONS: Marmosops pakaraimae closely resembles M. parvidens and M. pinheiroi , both of which also occur in the Guiana Region (north of the Amazon and east of the Orinoco-Rio Negro; Voss et al., 2001: fig. 98). These three species share many qualitative morphological traits including (1) small size, (2) spoon-shaped lateral carpal tubercles in adult males, (3) two antebrachial vibrissae, (4) an anteroposteriorly elongated subsquamosal foramen, (5) no palatine fenestrae, (6) upper canines with both anterior and posterior accessory cusps, (7) P2 slightly but consistently larger than P3, and (7) a premolariform c1 that is subequal in height to p1. Although some of these traits occur in other congeneric species ( Voss et al., 2001; Voss and Jansa, 2009; Díaz-N. et al., 2011), no extralimital (non-Guianan) species of Marmosops exhibits all of them, and spoon-shaped lateral carpal tubercles seem to occur uniquely in these three taxa. Additionally, we recovered this species triplet as a strongly supported monophyletic group in a multigene phylogenetic analysis of the entire genus (Díaz- Nieto et al., in prep.), so diagnostic morphological comparisons (summarized in tables 5 and 6) are appropriately restricted to just these forms.

Marmosops pakaraimae averages larger than M. parvidens in all measured external dimensions except ear length (table 5), and the two species differ strikingly in dorsal pelage coloration (dark brown in pakaraimae versus a paler, somewhat dusty reddish-brown in parvidens ; fig. 2). The difference in ventral pelage coloration (fig. 3) is even more striking: whereas pakaraimae has almost completely gray-based ventral fur, all examined specimens of parvidens have a continuous streak of self-whitish fur that extends from chin to groin. Marmosops pakaraimae is consistently larger than M. parvidens in all measured craniodental dimensions, especially in five variables (CBL, LIB, LPB, MTR, LM) that exhibit nonoverlapping variation between our all-male samples of these species (no female specimens of pakaraimae are known). Side-by-side comparisons of representative skulls (figs. 4–6) reveal that pakaraimae has a visibly broader interorbital region but relatively smaller orbits than parvidens . In qualitative aspects of craniodental morphology, however, these species are notably similar, both having lacrimal foramina that are mostly concealed from lateral view inside the anterior orbital margin ( Voss et al., 2001: fig. 25A), short upper canines, upper third molars with narrowly complete anterior cingula, and tricuspid m4 talonids.

Marmosops pakaraimae also averages larger than M. pinheiroi in external dimensions (except ear length), and the two species differ in dorsal pelage color (dark brown in pakaraimae versus paler brownish-gray in pinheiroi ). The ventral fur of pakaraimae is also more extensively gray-based than the ventral fur of pinheiroi , which usually includes a narrow, discontinuous midventral streak of self-white hairs. Marmosops pakaraimae is also larger on average than M. pinheiroi in craniodental measurements, especially in three dimensions (LIB, LPB, and LM) that exhibit nonoverlapping variation in our samples. Visual comparisons of representative skulls (figs. 4–6) reveal similar proportional differences between pakaraimae and pinheiroi to those previously noted between pakaraimae and parvidens , namely that pakaraimae has a broader interorbit but smaller orbits. Unlike pakaraimae and parvidens , the lacrimal foramina are more prominently exposed laterally ( Voss et al., 2001: fig. 25B), C1 is taller, M3 never has a complete anterior cingulum, and m4 usually has a bicuspid talonid in pinheiroi .

REMARKS: Of the six Venezuelan specimens that Voss et al (2001: 50) identified as Marmosops pinheiroi , two can confidently be reidentified as M. pakaraimae based on the diagnostic criteria explained above; one of these is AMNH 176353 (from ca. 1500 m on Churi-tepui) and the other is USNM 385046 (from 1032 m in the Sierra de Lema). Two other specimens appear to be good examples of M. pinheiroi ; both of these (AMNH 130568, 130570) are from 460 m at the base of Auyán-tepui. The remaining specimens (AMNH 130521, from 1100 m on Auyántepui; and AMNH 176352, apparently from the lower slopes of Churi-tepui) might be M. pakaraimae but have slightly shorter molar rows and somewhat narrower interorbits than our Guyanese material, and we are not confident of this identification.

Pine (1981: 62) reported two specimens that he identified as Marmosa parvidens pinheiroi from 85 km SSE El Dorado, Bolívar, Venezuela. One of these is USNM 385046, a paratype of Marmosops pakaraimae , but we were not able to examine the other specimen (USNM 385045), which has been returned to Venezuela and is now in the Museo de la Estación Biológica de Rancho Grande in Maracay (where it has been recataloged as EBRG 3945). Although we assume that USNM 385045 is another example of M. pakaraimae , we are not currently able to confirm this identification personally.

NATURAL HISTORY: All of our Guyanese specimens of Marmosops pakaraimae were livetrapped at or near (<2 m above) ground level in primary evergreen premontane forest. In the physiognomically defined classification of Grubb (1977), the dominant vegetation at these capture sites shares characteristics with both Lowland Rain Forest and Lower Montane Rain Forest (fig. 7): most (but not all) trees were unbuttressed, vascular epiphytes were sometimes (but not always) abundant, and thick-stemmed woody climbers (lianas) were infrequent but not completely absent. An abundant leaf litter was present, and tree trunks, roots, and boulders were often covered with moss. Soils were waterlogged at some sites and the canopy was more open than is commonly the case in primary forest at lower elevations; most of the trees were of moderate height (ca. 20 m tall). One specimen of M. pakaraimae was taken on the inclined trunk of a tree, but the rest were trapped on more or less horizontal surfaces.

According to Handley (1976: 74–75), the natural vegetation at 85 km SSE El Dorado (in the Sierra de Lema of eastern Venezuela) was “[d]ense, moist, luxuriant [premontane] forest (12–24 m high) ... festooned with orchids, ferns, mosses, and other epiphytes.” The ground at this locality was described as wet and rocky, “with little cover except for abundant moss-covered boulders and fallen trees.” The specimen tag attached to the skin of USNM 385046 bears the inscription “Live trap in forest on ground.” No habitat information accompanies the specimen from Churi-tepui.

SPECIMENS EXAMINED: Marmosops pakaraimae (N = 8): Guyana — Cuyuni-Mazaruni, Mt. Roraima (ROM 115129, 115148, 115254); Potaro-Siparuni, Mt. Ayanganna (ROM 114698), Mt. Wokomung (ROM 115841, 115845). Venezuela — Bolívar, 85 km SSE El Dorado (USNM 385046), Churi-tepui (AMNH 176353).

Marmosops parvidens (N = 24): Brazil — Amazonas, Boca Rio Paratucu (AMNH 93970), 80 km N Manaus (USNM 579985–579989); Pará, Ilha do Taiuna (AMNH 97333). French Guiana —Paracou (AMNH 267344, 267347, 267348, 267353, 267359, 267361; MNHN 1995- 929, 1995-933, 1995-939), River Arataye (USNM 548439). Guyana — Demerara-Mahaica, Hyde (LEFT) FIG. 6. Lateral views of skulls. Top to bottom: Marmosops pakaraimae (ROM 115129, holotype), M. parvidens (AMNH 267359 [skull], 267353 [mandible]), and M. pinheiroi (AMNH 267345). All views about ×3. Park (FMNH 18545 [holotype]), Upper Takutu-Upper Essequibo, Karanambo (ROM 97938). Surinam — Brokopondo, Brownsberg Nature Park (ROM 113997, 114009, 114144); Nickerie, Kayser Gebergte Airstrip (FMNH 93169); Sipaliwini, Bakhuis Transect 13 (ROM 117348).

Marmosops pinheiroi (N = 32): Brazil — Amapá, Serra do Navio ( USNM 461459 [holotype], 461460, 461462–461465) ; Pará , 52 km SSW Altamira ( USNM 549294 ) , Belém ( USNM 545543 ) , Utinga ( USNM 393529–393532 , 393534 ) . French Guiana — Paracou ( AMNH 266423 , 267341 , 267342 , 267345 , 267346 , 267349 , 267352 , 267357 ; MNHN 1995-931, 1995-932) . Guyana — Potaro-Siparuni, Canopy Walkway ( ROM 119852 ) , 10 km NW Kurupukari ( ROM 108920 ) , Kabukalli Landing ( ROM 111558 , 111663 ) . Surinam — Brokopondo, Finisanti ( FMNH 95320 ) ; Nickerie, Sipaliwini Airstrip ( CM 63506 ) ; Sipaliwini, Bakhuis Transect 9 ( ROM 116974 ) . Venezuela — Bolívar, Auyántepui ( AMNH 130568 , 130570 ) .

Phylogenetic Analysis

We aligned 21 ingroup and 2 outgroup cytochrome- b sequences ranging in length from 421 to 1149 bp, resulting in a data matrix that contained 17.9% missing entries. There is no significant departure from base-compositional stationarity among individuals in these data (χ 2 = 36.764, df = 66, P = 0.999). The five maximum-likelihood replicates produced identical topologies and lnL values (-4100.189), maximum-parsimony analysis produced 312 equally short trees (each of 579 steps), and Bayesian analysis produced a posterior distribution that converged on a single optimum topology (as evidenced by the “compare” plot of AWTY) with mean lnL value of -4133.336. All of these analyses yielded congruent topologies, of which we present the Bayesian maximum-credibility tree (fig. 8) with accompanying nodal support statistics from all three methods.

All three species of Marmosops recognized on the basis of morphology in this report were recovered as robustly supported clades, and a sister-group relationship between M. pakaraimae and M. parvidens was also strongly supported. Uncorrected mean sequence divergence within each of these species ranges from 0.1% (in M. pakaraimae ) to 3.3% (in M. pinheiroi ), whereas uncorrected mean interspecific distances range from 6.9% (between M. pakaraimae and M. parvidens ) to 12.1% (between M. parvidens and M. pinheiroi ; table 7). Some relatively shallow and weakly supported phylogeographic structure can be seen within M. pakaraimae and M. parvidens , but analyzed sequences of M. pinheiroi were recovered as strongly supported haplotype groups representing samples collected north and south of the lower Amazon.

Figures

FIG. 2. Dorsal views of skins. Left to right: Marmosops pakaraimae (ROM 115129, holotype), M. parvidens (ROM 114144), M. pinheiroi (ROM 111558). Approximately life size.