Marmosa (Micoureus) rapposa Thomas 1899

Marmosa (Micoureus) rapposa Thomas, 1899

Marmosa rapposa Thomas, 1899b: 42 (original description).

Marmosa budini Thomas, 1920a: 195 (original description).

Marmosa constantiae constantiae: Tate, 1933: 75 (part, based on misidentified material), not constantiae Thomas, 1904a.

Marmosa constantiae budini: Tate, 1933: 76 (new name combination).

Micoureus constantiae: Gardner, 1993 (part; budini treated as synonym), not constantiae Thomas, 1904.

Micoureus regina: Gardner, 1993: 20 (part; rapposa treated as synonym), not regina Thomas, 1898.

Micoureus constantiae constantiae: Anderson, 1997: 156 (part; based on misidentified material), not constantiae Thomas, 1904a.

Micoureus constantiae budini: Anderson, 1997: 156 (new name combination).

Micoureus regina rapposo: Gardner and Creighton, 2008: 81 (new name combination with inappropriate gender change). 4

Marmosa (Micoureus) constantiae: Voss and Jansa, 2009: 101 (part; budini treated as synonym), not constantiae Thomas, 1904a.

Marmosa (Micoureus) regina: Voss and Jansa, 2009: 101 (part; rapposa treated as synonym), not regina Thomas, 1898.

Marmosa (Micoureus) constantiae: de la Sancha et al., 2012 (misidentified material), not constantiae Thomas, 1904a.

Marmosa (Micoureus) budini: Silva et al., 2019: 254 (new name combination).

TYPE MATERIAL AND TYPE LOCALITY: The holotype (by original designation, BMNH 98.11.6.13) consists of the skin and skull of a

4 “Raposa” is the vernacular term for opossum in Peruvian Spanish, so the epithet is to be understood as a noun standing in apposition to the generic name. Although incorrectly spelled according to Spanish orthography, rapposa is the correct original spelling in the sense of the Code (ICZN, 1999: article 32).

large adult female collected by Otto Garlepp in December 1897 on the “Vilcanota River just north of Cuzco ” (Thomas, 1899b: 43) at 1500 m elevation in the Peruvian department of Cusco. As noted by Jenkins and Knutson (1983), the catalog number of this specimen was incorrectly reported by Thomas (as 98.11.1.13). Four juvenile paratypes (BMNH 98.11.6.14–98.11.6.17, also collected by Garlepp at the same locality in December 1897) are assumed to be offspring of the holotype (Thomas, 1899b; Tate, 1933).

According to Ceballos-Bendezú (1981), the type material of Marmosa rapposa was collected at Huadquiña in the district of Santa Teresa, province of La Convención (district and province are sequentially larger administrative units of Peruvian departments). Stephen and Traylor’s (1983) coordinates for Huadquiña (appendix 3: locality 52) place it ca. 85 km NW of Cuzco. According to Stephens and Traylor (1983) “Vilcanota” is a local synonym for the upper Urubamba.

DISTRIBUTION AND SYMPATRY: Based on specimens that we examined and others examined by Silva et al. (2019), Marmosa rapposa occurs along the eastern slopes of the Andes (below about 2500 m) and in adjacent foothills from about 13° S in southeastern Peru (Junín and Cuzco) to about 26° S in northwestern Argentina (Tucumán). Additionally, this species is widely distributed in the lowlands of eastern Bolivia, and we have also seen specimens from Brazil and Paraguay (fig. 12).

Marmosa rapposa occurs sympatrically with M. constantiae in eastern Bolivia (see below) and perhaps also in southeastern Peru, eastern Bolivia, and southwestern Brazil. Additionally, the geographic range of M. rapposa approaches that of M. paraguayana in eastern Paraguay (de la Sancha et al., 2012: fig. 2). 5

DESCRIPTION: The dorsal pelage of Marmosa rapposa is uniformly drab, ranging from a dull yellowish-gray—somewhat similar to Ridgway’s (1912) Grayish Olive—to a somewhat warmer

5 But note that Marmosa rapposa is identified as M. constantiae by de la Sancha et al. (2012).

brownish gray (near Ridgway’s Light Brownish Olive), often slightly paler in lowland specimens than in specimens from montane habitats, but otherwise remarkably constant in coloration throughout the wide geographic distribution of the species. Fur length at mid back ranges from 8 to 16 mm, but most specimens have middorsal fur that is 10–12 mm long; in general, lowland specimens are shorter furred than highland material. By contrast with the tonal uniformity observed in the dorsal pelage, the ventral fur varies considerably in color, from pale yellow (resembling Ridgway’s Cartridge Buff) to pinkish-orange (near Ochraceous Salmon), with yellowish hues predominating in lowland specimens and richer pigments primarily in highland material. A broad, continuous median streak of self- colored fur extends from the chin to the groin in most specimens (fig. 7), but at least some of the lateral fur is often gray based, and a few specimens (only 5% of those scored for this trait; table 5) have mostly gray-based ventral fur; the fur of the chin, throat, and groin, however, is always self-colored. The tail, usually about 130%–140% of head-and-body length, is covered with short fur for about 25 mm or less (usually <20 mm) at its base, and the naked part of the tail is almost always boldly marked or spotted with white distally (particolored). In a few specimens, as much as half of the unfurred distal part of the tail is white, but only the tip is white in many others, and a few specimens (mostly from the Andean foothills of eastern Bolivia) have all-dark tails. The manus and pes are covered dorsally with

TABLE 5

short, pale (usually yellowish) hairs in most specimens, but the metapodials are indistinctly darker in some individuals.

Mature adult skulls (fig. 13A, D) usually have short, wide rostrums; broadly flaring zygomatic arches; and distinct postorbital processes. 6 The maxillopalatine fenestrae are usually widely open (seldom reduced to narrow slits), and often extend posteriorly from the level of P3 to the level of M3. Palatine fenestrae are almost always present and well developed. The auditory bullae are usually smoothly globular; none that we examined are acutely pointed ventrally (“conical” sensu Tate, 1933). The upper molar series (LM) is usually short (8.0– 8.5 mm), the first three upper molars (M1–M3) have long postprotocris-

6 These traits are less well developed in young adults, and a few adults (e.g., USNM 582111, from an isolated high-altitude site) have narrower skulls than usual.

tae, and posterior cingulids are usually present on m1–m3.

VARIATION: Qualitative variation in selected morphological traits is summarized in table 5. With the exceptions noted above (fur pigmentation in lowland versus highland material), no geographic variation in qualitative phenotypic traits was observed, and specimens exhibiting rare traits for one character are not unusual in other respects. For example, the single specimen we examined that lacks posterior cingulids (CM 4947) has well-developed palatine fenestrae, maxillopalatine foramina that extend from P3 to M3, and a particolored tail. Therefore, such variation has the aspect of intraspecific polymorphism rather than taxonomic heterogeneity.

Morphometric variation in our adult material (table 6) is typical of that observed in homogeneous mammalian samples (e.g., with coeffi-

Measurements (mm) and Weights (g) of Marmosa rapposa

a The mean plus or minus one standard deviation, the observed range (in parentheses), and the sample size for each measurement of the following series: AMNH 210398, 210399, 275464, 275466, 275468; CBF 14, 2332, 3569, 3570; MSB 6700, 70281, 70282, 140343, 140347, 140352; MVZ 172583; UMMZ 126676, 155910; USNM 390023, 390573.

b The subadult male holotype of budini. External measurements in scare quotes were not taken by the American method.

c The mean plus or minus one standard deviation, the observed range (in parentheses), and the sample size for each measurement of the following series: AMNH 63860–63863, 72569, 210400, 264923, 264924, 275463, 275465, 275467; BMNH 76.631; CBF 2334, 7551, 7556; FMNH 65678, 66411; MSB 59883, 63277, 87093, 140348, 140349, 140351, 140415; UMMZ 126678, 126679.

d The female holotype of rapposa. External measurements in scare quotes were not taken by the American method.

e Measured by R.S.V. on the dried hind foot.

cients of variation consistently <10 for craniodental dimensions; Yablokov, 1974). Although the holotype of budini (BMNH 20.1.7.134, from Argentina) is a subadult, it is only slightly smaller than our smallest measured adult specimens (from Bolivia, Brazil, Peru, and Paraguay) in two nasal dimensions. By contrast, the old adult female holotype of rapposa (BMNH 98.11.6.13) is substantially larger than any other specimen (of either sex) in several craniodental dimensions, but other specimens from Cuzco (e.g., FMNH 65678, 66411) have unremarkable measurements, and a large (518 bp) fragment of cytochrome b that we were able to amplify and sequence from dried tissue scraped from the holotype skull supports the application of rapposa to specimens that share the external and craniodental traits described above. Therefore, we conclude that the type is simply an unusually large specimen. Other odd attributes of the holotype include a discontinuous facial mask (dark mystacial and circumocular markings are separated by a narrow line of yellowish fur; Thomas, 1899b) and short postprotocristae. However,

TABLE 7

Selected Morphological Comparisons among Species of the Rapposa Group of Marmosa (Micoureus)

a Crown length M1–M4 (see Materials and Methods). Table entries are the mean plus or minus one standard deviation computed from measurements of both sexes.

topotypical paratype skins have continuous facial masks, and the molars of the only preserved topotypical paratype skull (BMNH 98.11.6.14) have long postprotocristae. The problem of atypical holotypes is well known (Daston, 2004) and requires no additional comment here.

COMPARISONS: Marmosa rapposa differs from other members of the Rapposa Group in several characters (table 7). Whereas the ventral pelage of M. rapposa usually includes a broad midventral zone of self-colored fur (sometimes entirely without lateral zones of gray-based hairs), the ventral pelage of M. parda is almost entirely gray based (occasionally with a narrow median streak of self-yellow hairs), and the self-colored ventral fur of M. rutteri is usually narrowed by lateral zones of gray-based hairs and is sometimes discontinuous. Most (>80%) examined specimens of M. rapposa have tails that are marked with white (“depigmented” sensu Silva et al., 2019) distally, but all examined specimens of M. parda and M. rutteri have completely dark tails. According to Silva et al. (2019), specimens of M. rapposa (which they called M. budini) usually have more than three hairs emerging from the posterior edge of each caudal scale, whereas specimens of M. rutteri (which they called M. regina) usually have only three hairs per scale, but we did not score this character for our study.

Craniodental traits provide other diagnostic criteria. In general, skulls of Marmosa rapposa are less robust than those of M. parda and M. rutteri, and they tend to have smaller (but usually distinct) postorbital processes. A less subjective basis for sorting specimens is the palatine fenestrae, which are bilaterally present in>90% of the specimens we examined of M. rapposa and in all examined specimens of M. parda, but which are usually absent (or, when present, are much smaller) in M. rutteri. Lastly, the upper molar toothrow is substantially shorter, on average, in M. rapposa than in M. parda and M. regina.

REMARKS: We include several putative species identified by our mPTP analysis under this binomen (fig. 14). The haplogroup we call rapposa A consists of a single sequence from the Peruvian holotype, whereas rapposa B includes 17 sequences from widely scattered localities in Bolivia, Brazil, and Paraguay. A third haplogroup, rapposa C, includes two sequences from a single locality in the Cordillera Vilcabamba, an outlying spur of the Peruvian Andes. Sequence divergence between rapposa A and rapposa B is only about 3%, but rapposa C differs from the other haplogroups by about 7%–8% (table 4). Although the latter values are notably high for intraspecific sequence comparisons, we are unable to phenotypically distinguish specimens from the Cordillera Vilcabamba from other material of M. rapposa, so it seems best to treat all three haplogroups as conspecific in the absence of other evidence of lineage independence.

Specimens of Marmosa rapposa have long been misidentified as M. constantiae (e.g., by Tate, 1933; Anderson, 1997; Flores et al., 2007; Gardner and Creighton, 2008; Voss et al., 2009; de la Sancha et al., 2012). Indeed, the holotype (BMNH 3.7.7.157) and other specimens of M. constantiae from eastern Bolivia (e.g., AMNH 209158–209162, 210397) and western Mato Grosso (AMNH 384, OMNH 37209) superficially resemble lowland material of M. rapposa by having a continuous median zone of self-yellow ventral fur and tails that are boldly marked with white. Externally, these species are difficult to tell apart where they occur together, although M. constantiae has a longer furry tail base (usually> 25 mm). However, M. constantiae differs from M. rapposa in several craniodental traits, notably by lacking palatine fenestrae, by having short postprotocristae on M1–M3 (fig. 10), and by lacking any trace of posterior cingulids (fig. 11); additionally, M. constantiae has larger molars (LM = 8.7–9.2 mm) and bullae that tend to become distinctly conical in older adults.

For the last 25 years Marmosa rapposa has been treated as a synonym (Gardner, 1993) or subspecies (Gardner and Creighton, 2008) of M. regina, but there is no compelling evidence to support the hypothesis that these are closely related taxa. The type of M. regina (BMNH 98.5.15.4) consists of the skin and skull of an old adult male collected by G.D. Child in “W[est]. Cundinamarca (Bogotá region)” (Thomas, 1898: 275). As noted by Patton et al. (2000: 76), the type locality of regina is probably somewhere in the Río Magdalena valley of Colombia, which is separated from the rest of the enormous geographic range previously attributed to this species (Gardner and Creighton, 2008: map 35) by formidable elevations of the eastern Andean cordillera. Among other traits by which it differs from M. rapposa, the holotype of M. regina lacks palatine fenestrae and has distinctly redder dorsal fur (formerly near Prout’s Brown according to Tate [1933: 83], who saw the type when it was less than 40 years old), a well-developed gular gland, an all-dark tail, and short postprotocristae. Like Tate (1933), Voss et al. (2019) restricted the application of M. regina to the holotype, which does not closely resemble any other specimen of Micoureus that we have examined.

In a well-executed and meticulously documented study of mtDNA sequence data and cra- niodental morphology, Silva et al. (2019) identified the present species as Marmosa budini, a name that we treat as a junior synonym. The holotype of M. budini (BMNH 20.1.7.134) consists of the skin and skull of a subadult 7 male collected by Emilio Budin on 23 July 1919 at 500 m on the Altura de Yuto near the Río San Francisco in the province of Jujuy, Argentina. Except for its slightly smaller nasal measurements (discussed above; see Variation), this specimen is morphologically indistinguishable from sequenced Bolivian material that clusters with the partial sequence we obtained from the type of M. rapposa.

One specimen of Marmosa rapposa —AMNH 72569, from Ñequejahuira at 8000 ft (2450 m) above sea level on the eastern slopes of the Cordillera Real of La Paz department, Bolivia—was part of Tate’s (1931) type series of M. mapiriensis, but it is not conspecific with the holotype (AMNH 72555), which was collected in the adjacent foothills at Ticunhuaya (1500 m). Among other noteworthy differences from M. rapposa, AMNH 72555 lacks palatine fenestrae and posterior cingulids; additionally, it has short postprotocristae, short and narrow maxillopalatine fenestrae, and strongly conical auditory bullae. As noted earlier, we provisionally regard mapiriensis as a junior synonym of M. constantiae.

HABITATS: Explicit descriptions of habitats in which specimens of Marmosa rapposa have been collected are uncommon. Ecological maps suggest that most Andean specimens were collected in montane (“cloud”) forest and that most lowland specimens were taken in dry forests, and these ecological associations are generally supported by brief notations on specimen tags and in field notes. According to Silva et al. (2019: 17), this species occurs in multiple ecoregions (sensu Olson et al., 2001) including “Cerrado, Chaco (savannic and humid), Pantanal, Parana / Paraiba interior forests, Bolivian Yungas, Andean Yun-

7 Thomas (1920a: 196) described this specimen as “adult but not old,” Tate (1933: 76) described it as a “young adult,” and Jenkins and Knutson (1983: 15) described it as an “adult,” but P3 is not quite fully erupted, so we consider it to be subadult.

gas, south-western Amazonian moist forests, Chiquitania dry forests, and Bolivian montane dry forests,” but their list conveys little about the appearance of vegetation in which the species is actually found because many of these ecoregions (e.g., the Cerrado; Eiten, 1972) are mosaics of quite different habitat types. Detailed descriptions of the vegetation at distant localities where M. rapposa have been collected are in Ratter et al. (1973) and Holst (1997), but carefully conducted trapping programs at sites like these would be necessary to establish which local habitats are “sinks” and which are “sources” (Pulliam, 1988) for this species.

Despite their very broad geographic overlap, the only place where Marmosa rapposa and M. constantiae are known to occur sympatrically is the Serranía (or Cordillera) Mosetenes in Cochabamba department, Bolivia (appendix 3: locality 7). In September 2003, Fernando Guerra, Teresa Tarifa, and Eric Yensen collected two specimens of M. rapposa (CBF 7551, 7556) and two specimens of M. constantiae (CBF 7515, 7540) in the Serranía Mosetenes at elevations ranging from 1200 to 1600 m. According to Tarifa et al. (2008), local habitats included bamboo thickets, regenerating montane forest, mature montane forest, and ridge forest; apparently, M. constantiae (“ Micoureus demerarae ”) was captured only in montane forest, whereas M. rapposa (“ Mic. regina ”) was captured in both montane forest and ridge forest. The ridge-forest habitat (figs. 15, 16) of M. rapposa was said to consist of stunted trees heavily laden with epiphytes, and to lack

the “Amazonian elements” observed in mature montane forest.

SPECIMENS EXAMINED (N = 94): Argentina— Jujuy, Altura de Yuto (BMNH 20.1.7.134 [holotype of budini]). Brazil— Mato Grosso, 264 km N Xavantina (BMNH 76.631); Mato Grosso do Sul, 10 km NE Urucum (USNM 390023). Bolivia — Beni, 5 km N Estancia El Porvenir (CBF 14); Chuquisaca, 2 km E Chuyayacu (MSB 63276), El Limón (LHE 1307), Rinconada del Bufete (LHE 1299), Río Limón (MSB 63277); Cochabamba, Serranía Mosetenes (CBF 7551, 7556), 4.4 km N Tablas Monte (AMNH 264924, CBF 3570, MSB 70281), 9.5 km NE Tablas Monte (AMNH 264923, CBF 3569, MSB 70282); La Paz, 4 km NW Alcoche (UMMZ 126679, 127170), Cajuata (CBF 6606, 6607), 20 km NNE Caranavi (UMMZ 126676–126678, 127171), La Reserva (AMNH 275463–275465, 275467; MSB 140341–140345, 140347–140352, 140415), 1 km S La Reserva (CBF 2332, 2334); Los Molinos de Titiamaya (CBF 4996), Ñequejahuira (AMNH 72569), 1 mi W Puerto Linares (TTU 34785); Santa Cruz, 53 km E Boyuibe (AMNH 275466), Buenavista (CM 5049; FMNH 25266, 51902–51905), Cerro Hosane (CM 4941, 4947, 4951), 2 km N Chapare River mouth (AMNH 210398, 210399), 54 km S Chapare River mouth (AMNH 210400), 1 km NE Estancia Cuevas (MSB 67019), Río Surutú (CM 5040), 27 km SE Santa Cruz (MSB 59883), Warnes (USNM 390573); Tarija, 3 km WNW Carapari (AMNH 275468), 5 km NNW Entre Ríos (MSB 87093). Paraguay — Alto Paraguay, Puerto Casado (FMNH 54404); Amambay, Parque Nacional Cerro Cora (MSB 67000, UMMZ 134550); San Pedro, Ganadera La Carolina (UMMZ 174909, 174992). Peru — Cusco, Hacienda Cadena (FMNH 65678, 66411, 68330, 75102), Vilcanota River just north of Cuzco (BMNH 98.11.6.13 [holotype of rapposa], 98.11.6.14–98.11.6.17); Junín, “Camp Two” in Cordillera Vilcabamba (MUSM 13004, 13005; USNM 582111, 582112), 15 km by road SW San Ramón (UMMZ 155909–155911, 158013– 158015), Utcuyacu (AMNH 63860–63863); Puno, 11 km NNE Ollachea (MVZ 172582), 14 km W Yanahuaya (MVZ 172583).