Thylamys pusillus (Desmarest, 1804)

Giarla, T. C., Voss, R. S. & Jansa, S. A., 2010, Species Limits And Phylogenetic Relationships In The Didelphid Marsupial Genus Thylamys Based On Mitochondrial Dna Sequences And Morphology, Bulletin of the American Museum of Natural History 2010 (346), pp. 1-67 : 39-44

Thylamys pusillus (Desmarest, 1804)

SYNONYMS: bruchi Thomas, 1921; citellus Thomas, 1912; nanus Oken, 1816 (unavailable); nanus Olfers, 1818; pulchellus Cabrera, 1934; verax Thomas, 1921 .

DISTRIBUTION: This lowland species (all examined specimens are from, 1000 m above sea level) occurs in southeastern Bolivia, western Paraguay, and northern Argentina. Based on material that we examined, the distribution of Thylamys pusillus is almost coextensive with the tropical and subtropical dry forests and savannas collectively known as the Chaco, but a few collection localities (in the Argentine provinces of Mendoza, Misiones, and San Luis) are just outside the limits of the Chaco as that biome is conventionally recognized by authors (e.g., Short, 1975). Records of this species from Patagonian habitats ( Birney et al., 1996) are based on misidentifications, as are Anderson’s (1997) records from high elevations in the Bolivian department of Chuquisaca (see Remarks, below) and, apparently, a single published record from Uruguay ( González et al., 2000; see Teta et al., 2009). Brown’s (2004: fig. 88) map of the range of T. pusillus includes numerous extralimital records, all of which are apparently based on misidentifications or erroneous synonymies.3

The known geographic range of Thylamys pusillus overlaps that of T. pallidior in northern Argentina, where the two species have been collected sympatrically in the Reserva Biósfera de Ñacuñán (ca. 34 ° S, 68 ° W) in Mendoza province. The range of T. pusillus also overlaps that of T. venustus in southeastern Bolivia, where these species have been collected sympatrically near Carandaytí (gazetteer locality 44) in Chuquisaca department, and near Villa Montes (21 ° 15 9 S, 63 ° 30 9 W) in Tarija department.

3 Brown’s (2004) erroneous records for Thylamys pusillus include (1) Anderson’s (1997) misidentified specimens of T. venustus (see Remarks, below) from high elevations in Chuquisaca department, Bolivia; (2) Thomas’s (1912) and Tate’s (1933) use of ‘‘ Marmosa marmota’’ (erroneously listed as a synonym of T. pusillus ) for specimens of T. macrurus collected in eastern Paraguay; (3) Brazilian specimens of T. karimii (erroneously synonymized with T. pusillus by Gardner, 1993); (4) Birney et al.’s (1996) misidentified Patagonian specimens of T. pallidior (see Remarks, below); (5) Cope’s (1889) report of ‘‘ Philander pusillus ’’ (based on ANSP 4632 [ Thylamys karimii ]) from Chapada dos Guimarães in the Brazilian state of Mato Grosso; and (6) Mares et al.’s (1981) report of ‘‘ Marmosa karimii ’’ (based on MZUSP 16961 [ Cryptonanus agricolai ]; see Remarks, below) from Pernambuco. The basis for Bertoni’s (1914, 1939) cited reports of ‘‘ Marmosa pusilla ’’ from Puerto Bertoni in Alto Paraná, Paraguay is unknown, but Bertoni may have used pusilla in the sense of Thomas (1888, 1900), who applied this epithet to specimens that are now placed in Cryptonanus and Gracilinanus (see Voss et al., 2009).

MORPHOLOGICAL DIAGNOSIS: Body pelage tricolored (abrupt line of transition from darker middorsal to paler lateral coloration present); ventral pelage entirely self-white (yellowish in some museum specimens); plantar pads of manus separate, surrounding concave central palmar surface, and with well-developed dermatoglyphs; manual claws short, not extending much if at all beyond fleshy apical pads of digits; tail longer than combined length of head and body (LT/HBL X 100 5 116%; N 5 30), without pale tip; ventral prehensile surface of tail tip well developed. Nasal bones long (extending posteriorly as far as lacrimals) or very long (extending beyond lacrimals); lacrimal foramina usually concealed inside orbit or partially exposed on orbital rim; infraorbital foramen usually above P3; nasolabial fossa shallow; supraorbital margins often beaded, the beads sometimes laterally expanded as postorbital processes in old male specimens; maxillary fenestrae usually present; crown of second upper incisor (I2) consistently smaller than or subequal to crown of I3; stylar cusp C usually present on M1 and M2; metaconule usually well developed on M3.

COMPARISONS: Thylamys pusillus can be distinguished from other members of the nominotypical subgenus by a unique combination of qualitative external and craniodental characters (table 16). Additionally, pusillus is smaller than most other species in the subgenus Thylamys (LM 5 4.8–5.8 mm; N 5 58), and the skull is unusually wide relative to its length, a distinctive proportion that is conspicuous in side-by-side cranial comparisons (Voss et al., 2009: fig. 5).

Thylamys pusillus has previously been confused with two other small congeners with self-white ventral pelage, T. karimii and T. pallidior . Diagnostic morphological differences between T. pusillus and T. karimii , first clearly stated by Carmignotto and Monfort (2006), are effectively summarized in our diagnosis of the subgenus Xerodelphys (above) and need not be repeated here. By contrast, morphological comparisons between T. pusillus and T. pallidior , although discussed in substantive detail by Voss et al. (2009), merit additional comment based on the larger samples of both species examined for this study.

Thylamys pusillus and T. pallidior are most reliably distinguished externally by claw length: whereas the manual claws of pusillus are short, not extending much (if at all) beyond the fleshy apical pads of the digits, those of pallidior are substantially longer, projecting well beyond the fleshy fingertips. Additionally, pusillus is, on average, shorter furred than pallidior . Among 53 measured adult specimens of pusillus , the middorsal fur ranges in length from 6–11 mm, but most specimens (79%) have middorsal fur that is only 7–9 mm long. By contrast, among 44 measured adult specimens of pallidior , the middorsal fur ranges in length from 10–15 mm, but most specimens (82%) have fur that is 11–13 mm long. Although a couple of millimeters’ difference in average fur length does not sound like much, the contrast is visibly and tactilely apparent with representative specimens of both species in hand. A third external difference that might be useful for field identification concerns ventral pelage color, which is completely self-white in almost all examined specimens of pusillus , whereas narrow lateral zones of gray-based hairs are often present in pallidior .

Tables 7–13 document modal differences between Thylamys pusillus and T. pallidior in several craniodental characters, notably including infraorbital foramen position (usually over P 3 in pusillus , usually over M 1 in pallidior ), maxillary fenestrae (usually present in pusillus , usually absent in pallidior ), stylar cusp C (usually present in pusillus , usually absent in pallidior ), and metaconules (usually well developed in pusillus , usually indistinct or absent in pallidior ). These species are additionally distinguished by cranial proportions described and illustrated by Voss et al. (2009: 421, fig. 5).

Although no single qualitative craniodental character unambiguously distinguishes Thylamys pusillus from T. pallidior (contra Voss et al. [2009], who examined smaller series of both species), specimens that are atypical in one character are seldom atypical in others. For example, USNM 390033, a Paraguayan specimen that we identify as pusillus despite its lack of maxillary fenestrae, exhibits most of the other distinctive characteristics of the species, including completely self-white ventral pelage, short claws, weakly beaded supraorbital margins, infraorbital foramen above P3, well developed stylar cusp C on M1 and M2, and a well-developed metaconule on M3. Thus, specimens can be reliably identified to species using a combination of traits.

REMARKS: Our analyses of cytochrome- b sequence data recovered several robustly supported haplogroups that we regard as conspecific despite the presence of noteworthy geographic size variation ( Teta et al., 2009; Voss et al., 2009). Because the collection localities of sequenced specimens of Thylamys pusillus are spatially clustered with large intervening areas from which no sequence data are available ( fig. 7), geographic sampling bias is a possible explanation for the seemingly distinct groups in our cytochrome- b analyses. Nevertheless, sequence divergence among these haplogroups is impressive: 6.8% between haplogroup A and haplogroup B, 7.6% between haplogroup A and haplogroup C, and 5.8% between haplogroup B and haplogroup C. If these really are conspecific mitochondrial lineages, they are old ones. In the event that diagnostic morphological criteria are eventually found to reliably distinguish these haplogroups, we discuss the application of available names in the paragraphs that follow.

Haplogroup A, represented in our analyses by samples from southeastern Bolivia and western Paraguay, corresponds to Thylamys pusillus in the strict sense of Voss et al. (2009), who designated a neotype from the Paraguayan department of Boquerón; nanus is an objective junior synonym (based on the same type material); and verax , a subjective junior synonym, is also based on a western Paraguayan type (table 14). Voss et al. (2009) conjectured that typical pusillus might be restricted to the tropical and subtropical dry forests north of the Río Pilcomayo, from which measured specimens seem to be larger (with upper molar tooth rows. 5 mm) than specimens collected south of the Pilcomayo—in Argentina —which are mostly smaller (with tooth rows, 5 mm). However, a previously unexamined USNM series from Fortín Guachalla (22 ° 27 9 S, 62 ° 20 9 W) on the north bank of the Pilcomayo is geographically intermediate to the material examined by Voss et al. (2009), and it is also morphologically intermediate (with LM 5 4.9–5.3 mm), suggesting that geographic variation is clinal rather than abrupt, and that the Pilcomayo does not separate morphologically distinctive forms.

Haplogroup B, represented by geographically adjacent samples from the Argentine provinces of Catamarca and Santiago del Estero, corresponds to the small-bodied phenotype that Voss et al. (2009) associated with bruchi, a name that has been variously treated as a junior synonym of Thylamys pusillus (e.g., by Voss and Jansa, 2009) or T. pallidior (e.g., by Gardner, 2005). Although the type locality of bruchi is in the Argentine province of San Luis, from which no additional pusillus -like material is known to have been collected, the subadult holotype (BMNH 21.4.21.8) has all the distinguishing characteristics of pusillus , including short claws, an infraorbital foramen that is dorsal to P3, distinct maxillary fenestrae, a welldeveloped stylar cusp C on M1 and M2, and a well-developed metaconule on M3. The name pulchellus (based on a specimen from Santiago del Estero; table 14) also applies to this haplogroup according to Teta et al. (2009), but we have not examined the type.

Voss et al. (2009) thought that bruchi might be distinct from pusillus based on the smaller size of specimens collected south of the Pilcomayo by comparison with specimens collected in Paraguay and Bolivia, and because they observed correlated geographic variation in the frequency of stylar cusp C on M3. As discussed above, however, newly examined material suggests that geographic size variation in this complex is clinal and does not provide a satisfactory basis for identifying unsequenced specimens. Representative voucher specimens of haplogroup B are, in fact, smaller than vouchers of haplogroup A (table 17), but observed metrical differences are small, and stylar cusp C occurs polymorphically on M 3 in voucher material of both haplogroups. Because close scrutiny has not revealed additional phenotypic differences between specimens that might be referred to bruchi on the one hand and to pusillus on the other, it seems appropriate to adopt the taxonomically conservative view that these are conspecific forms.

Haplogroup C represents the nominal taxon citellus, an identification that is convincingly established by sequence data that we obtain- ed from a century-old paratype ( BMNH 1898.8.19.12; table 1).4 This haplogroup occurs in the so-called Mesopotamian region of Argentina (between the Paraná and Uruguay rivers), where our samples were collected in the provinces of Corrientes , Entre Ríos , and Misiones. Measured voucher material and other (unsequenced) Mesopotamian specimens are larger than bruchi (e.g., with LM 5 5.4–5.8 mm), but they overlap broadly with typical pusillus (from the Chaco Boreal ) in all measured craniodental dimensions and lack any distinguishing qualitative trait. Whereas several specimens from Corrientes (e.g., BMNH 98.8 .19.9, 98.8.19.11, 98.8.19.12) have white-tipped tails, for example, this marking was not observed in material that we examined from Misiones .

Specimens from high elevations (. 2000 m) in the Andes of Chuquisaca department, Bolivia, that Anderson (1997: 164) identified as Thylamys pusillus all appear to be examples of T. venustus . Relevant specimens that we examined include sequenced material from ‘‘ 9 km by road N Padilla,’’ ‘‘ 11 km N and 16 km W Padilla,’’ ‘‘ 12 km N and 11 km E Tarabuco,’’ ‘‘ 2 km N Tarabuco,’’ and ‘‘ 4 km N Tarabuco’’ (see Specimens Examined in our account for T. venustus , below). Although some material from these localities remains unexamined, the lack of any verified high-elevation records of T. pusillus and the lack of accurately diagnostic couplets in Anderson’s (1997: 29) key to Thylamys lead us to believe that none of his Andean material represents this species.

Specimens of Thylamys pallidior have sometimes been misidentified as T. pusillus , most recently by Birney et al. (1996), who reported finding two distinct phenotypes in

4 Creighton and Gardner (2008: 114) alleged that ‘‘ marmota Thomas, 1896 ’’ is a senior synonym of citellus, but Thomas’s (1896) use of marmota Oken, 1816—an unavailable name based on Azara’s fourth opossum (the Paraguayan species currently known as Thylamys macrurus ; Voss et al., 2009)—for Argentinian material was a misidentification that he subsequently corrected ( Thomas, 1912). Because Thomas (1896) was not proposing a new name, his citation of a previous description ( Thomas, 1894) to clarify the application of Oken’s epithet cannot be construed as a nomenclaturally valid indication in the sense of the Code ( ICZN, 1999: Article 12).

TABLE 17 Measurements (mm) of Sequenced Adult Specimens of Thylamys pusillus a

material they collected in ‘‘Monte’’ and ‘‘Patagonian’’ habitats of Chubut province, Argentina. However, we examined Birney at al.’s material (in the MMNH) and found no morphological differences between their Monte and Patagonian series. The morphometric variation among adult MMNH specimens from Chubut is well within the normal range of intraspecific variation in Thylamys , and both series conform qualitatively to our diagnosis of T. pallidior . 5 No speci-

5 Birney et al. (1996) claimed that their Monte and Patagonian series differed in pelage traits (fur color and texture) and in the position of the infraorbital foramen above the maxillary tooth row. However, three of their four Monte specimens are juveniles with obviously immature pelage; their single Monte adult (MMNH 15722) closely resembles Patagonian specimens in pelage characteristics. Apparently, the authors mistook dP3 for M1 when they recorded the position of the infraorbital foramen above the tooth row in their Monte juveniles. The position of the infraorbital foramen in MMNH 15722 is indistinguishable from the morphology seen in their Patagonian series (above stylar cusp B of M1)

men in either series resembles T. pusillus . Unfortunately, tissue samples from Birney at al.’s Chubut material (which may still exist in a freezer at Texas Tech University; C.J. Phillips, personal commun.) could not be obtained for our sequencing study.

SPECIMENS EXAMINED (N 5 84): Argentina — Catamarca, Bella Vista ( OMNH 32562 , 32563 ), Chumbicha ( OMNH 23483 ), 5.2 km NW Chumbicha ( OMNH 32561 ) ; Corrientes, Estancia Corona, near Goya ( BMNH 94.6.30.1), Goya ( BMNH 98.8 .19.9 [holotype of citellus], 98.8.19.10–98.8.19.12) ; Entre Ríos, La Paz ( BMNH 23.12.12.16) ; Mendoza, Ñacuñán Reserve ( UWBM 72205 ) ; Misiones, Dos de Mayo ( ZSM 1966 /70–1966/ 74) ; San Luis, Alto Pencoso ( BMNH 21.4 .21.8 [holotype of bruchi]) ; Santiago del Estero, 6 km S and 2 km E Pampas de los Guanacos ( OMNH 23479 ) ; Tucumán, Tapia ( USNM 236332 ). Bolivia — Chuquisaca, 3.8 km by road E Carandaytí ( AMNH

TABLE 18 Morphological Comparisons among Species in the Elegans Group of Thylamys

261268; MSB 55846 ); Santa Cruz, 53 km E of Boyuibe ( AMNH 275441 ; MSB 87105), Tita ( AMNH 260025 ) ; Tarija, Estancia Bolívar ( AMNH 275440 , 275442 , 275445 , 275446 ; MSB 67016–67018, 87103, 87104), 8 km S [and] 10 km E Villa Montes ( AMNH 246442– 246444 , 246446–246449 , 246452 ). Paraguay — Alto Paraguay, Destacamento Militar Gabino Mendoza ( TTU-TK 65601 , 65632 , 65635 ), Fortín Pikyrenda ( TTU-TK 65592 , 65612 ), Palmar de las Islas ( TTU-TK 65458 , 65463 ) ; Boquerón, Estancia ‘‘ El 43’’ ( TTU-TK 60217 , 60227 ), Estancia Toledo ( FMNH 164097 ), Experimental Farm ( FMNH 164095 , 164096 ), Fortín Guachalla ( FMNH 54369 ; USNM 390027–390033 ), Orloff ( FMNH 63862 ), Parque Cué ( TTU-TK 63360 , 63367 ), Parque Nacional Teniente Agripino Enciso ( TTU-TK 65031 , 65104 , 65215 , 66463 , 66468 , 66469 , 66476 ; USNM 555660 ), Schmidt Ranch ( FMNH 164086 ), 410 km NW Villa Hayes ( MVZ 144312 , 144313 ), 460 km NW Villa Hayes ( MVZ 144311 [neotype of pusillus and nanus]) ; Chaco, 50 km WNW Fortín Madrejon ( UMMZ 124676 ) ; Nueva Asunción, 1 km SW km 620 [of] Trans-Chaco Road ( UMMZ 176357 ) ; 19 km by road WSW km 588 [of] Trans-Chaco Road ( UMMZ 176358 , TWN 240, 275, 390). Presidente Hayes, Misión Central ( BMNH 20.12 .18.34 [holotype of verax ]), 295 km NW Villa Hayes ( MVZ 144310 ) .