A M ERIC AN MUSEUM NOVITATES Number 3868, 44 pp. December 1, 2016 A Revised Subgeneric Classification of Short-tailed Opossums (Didelphidae: Monodelphis) SILVIA E. PAVAN1 AND ROBERT S. VOSS1 ABSTRACT Members of the didelphid marsupial genus Monodelphis have previously been classified into species groups, but such informal subdivisions are inconsistent among authors and have contributed little but confusion to the taxonomic history of the genus. Recent molecular phy- logenetic studies, however, have consistently recovered several strongly supported multispecies clades that merit formal recognition. Here we define and illustrate morphological characters that are useful for diagnosing these monophyletic groups, which we name and rank as subgen- era to conserve binomial usage: Monodelphis Burnett, 1830 (for M. arlindoi, M. brevicaudata, M. domestica, M. glirina, M. palliolata, M. sanctaerosae, and M. touan), Microdelphys Burmeis- ter, 1856 (for M. americana, M. gardneri, M. iheringi, and M. scalops), Monodelphiops Matschie, 1916 (for M. dimidiata and M. unistriata); Mygalodelphys, new subgenus (for M. adusta, M. handleyi, M. kunsi, M. osgoodi, M. peruviana, M. pinocchio, M. reigi, and M. ronaldi); and Pyrodelphys, new subgenus (for M. emiliae). We provide morphological diagnoses and describe pairwise comparisons to facilitate subgeneric identification, and we summarize subgeneric pat- terns of geographical distribution and sympatry to supplement recently published biogeo- graphic analyses of the genus. 1 Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History. Copyright © American Museum of Natural History 2016 ISSN 0003-0082 2 AMERICAN MUSEUM NOVITATES NO. 3868 INTRODUCTION Monodelphis Burnett, 1830, is the most speciose genus of didelphid marsupials, with 22 currently recognized species (Pavan et al., 2014; Pavan, 2015). Insofar as known, species of Monodelphis are terrestrial or semifossorial, predominantly insectivorous opossums that exhibit conspicuous variation in pelage coloration, behavior, and reproductive strategies (Streilein, 1982a, 1982b; Emmons and Feer, 1997; Pine et al., 1985; Pine and Handley, 2008). Unlike most other didelphid genera, which are restricted to either humid forest or savanna-like habitats, Monodelphis inhabits a wide range of environments, including low- land rain forest, dry forest, montane forest, and savannas (Pine and Handley, 2008; Voss and Jansa, 2009). To date there has been no comprehensive revision of the genus, and most relevant taxo- nomic publications have treated single species or species complexes (Pine, 1975, 1976, 1977, 1980; Pine and Handley, 1984; Pine et al., 1985; Ventura et al., 1998; Lemos et al., 2000; Voss et al., 2001; Lew and Pérez-Hernández, 2004; Solari, 2004; Lew et al., 2005; Solari, 2007; Vilela et al., 2010; Pavan et al., 2012; Solari et al., 2012; Voss et al., 2012; Pavan, 2015). The most inclusive morphology-based revisionary study (Gomes, 1991) was exclusively based on Brazil- ian specimens and remains unpublished. Historically, a number of species groups of Monodelphis have been recognized informally, primarily based on pelage markings (Matschie, 1916; Gilmore, 1941; Pine, 1976). However, such morphology-based subdivisions have contributed little but taxonomic confusion (Pine et al., 2013), and none is convincingly supported by character data. By contrast, recent molecular phylogenetic studies based on dense taxonomic sampling and multiple unlinked genes (Pavan et al., 2014; Vilela et al., 2015; Pavan et al., 2016) have consistently recovered several robustly supported multispecies clades (table 1), and some morphological studies (e.g., Voss et al., 2012; Pavan, 2015) suggest that at least some of the groups recovered by molecular phylogenetic research are morphologically diagnosable. Unfortunately, informal nomenclature for these clades is not sufficient for the purposes of biological communication. For example, the monophyletic group that Pavan et al. (2014) called “Clade E” corresponds to the “Adusta Group” of Pavan et al. (2016) and to the combined adusta and kunsi “complexes” of Vilela et al. (2015). Formally diagnosing and naming such groups has the advantage that usage is constrained by typification and priority according to widely accepted rules (ICZN, 1999), and ranking these clades as subgenera promotes stability by preserving long-established binomial combinations. In this report, we define and illustrate morphological characters that are useful for recog- nizing and diagnosing the monophyletic groups previously established by molecular research. These results provide the materials for a formal subgeneric classification, which we intend to serve as the basis for future revisionary research at the species level. Additionally, we summa- rize subgeneric patterns of distribution and sympatry consistent with our previously published biogeographic analyses (Pavan et al., 2016). 2016 PAVAN AND VOSS: SUBGENERA OF SHORT-TAILED OPOSSUMS (MONODELPHIS) 3 TABLE 1. Species-group Classification of Monodelphis (after Pavan et al., 2016). Adusta Groupa, b Americana Groupd, e Brevicaudata Groupf Monotypic “groups” Unsequenced species M. adusta M. americana M. arlindoi M. dimidiatag, h M. ronaldib M. handleyi M. gardneri M. brevicaudata M. emiliaei M. unistriatah M. kunsi M. iheringi M. domestica M. scalopse, j M. osgoodi M. glirina M. peruviana M. palliolata M. pinocchioc M. sanctaerosae M. reigi M. touan M. “species 2” M. “species 3” M. “species 4” a Equivalent to “Clade E” of Pavan et al. (2014) and the combined “adusta” and “kunsi” complexes of Vilela et al. (2015). b Referred to subgenus Mygalodelphys in this report. c Referred to as M. “species 1” by Pavan et al. (2014) and Vilela et al. (2015), subsequently named as M. pinocchio by Pavan (2015). d Equivalent to “Clade D” of Pavan et al. (2014) and the “americana complex” of Vilela et al. (2015). e Referred to subgenus Microdelphys in this report. f Equivalent to “Clade F” of Pavan et al. (2014) and the “brevicaudata complex” of Vilela et al. (2015). Referred to subgenus Monodelphis in this report. g “Clade B” of Pavan et al. (2014). h Referred to subgenus Monodelphiops in this report. i “Clade A” of Pavan et al. (2014). Referred to subgenus Pyrodelphys in this report. j “Clade C” of Pavan et al. (2014). Materials and Methods Source of material: Specimens listed in this report are deposited in the following col- lections: AMNH (American Museum of Natural History, New York); ANSP (Academy of Natu- ral Sciences of Drexel University, Philadelphia); BMNH (Natural History Museum, London, UK); CM (Carnegie Museum of Natural History, Pittsburgh); EBRG (Museo de la Estación Biológica de Rancho Grande, Maracay, Venezuela); FMNH (Field Museum, Chicago); IEPA (Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá, Macapá, Brazil); INPA (Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil); ISEM (Institut des Sciences de l’Evolution, Montpellier, France); KU (Biodiversity Research Center, University of Kansas, Law- rence); LZUFPI (Laboratório de Zoologia Prof. Antônio J. Dumbra, Universidade Federal do Piauí, Teresina, Brazil); MACN-Ma (Colección de Mamíferos del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia,” Buenos Aires, Argentina); MCN-M (Coleção de Mamíferos, Museu de Ciências Naturais da Pontifícia Universidade Católica de Minas Gerais, Belo Hori- zonte, Brazil); MCZ (Museum of Comparative Zoology, Harvard University, Cambridge); MHNCI (Museu de História Natural Capão da Imbuia, Curitiba, Brazil); MN (Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil); MNHN (Muséum National d’Histoire Naturelle, Paris, France); MPEG (Museu Paraense Emílio Goeldi, Belém, Brazil); MSB (Museum of Southwestern Biology, University of New Mexico, Albuquerque); MSU 4 AMERICAN MUSEUM NOVITATES NO. 3868 (Michigan State University, Michigan); MUSM (Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos, Lima, Peru); MVZ (Museum of Vertebrate Zoology, University of California, Berkeley); MZUSP (Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil); NMW (Naturhistorisches Museum Wien, Vienna, Austria); OMNH (Sam Noble Okla- homa Museum of Natural History, Oklahoma); ROM (Royal Ontario Museum, Toronto, Can- ada); TTU (Museum of Texas Tech University, Lubbock); UFMG (Universidade Federal de Minas Gerais, Belo Horizonte, Brazil); UFPA (Universidade Federal do Pará, Belém, Brazil); UFSC (Universidade Federal de Santa Catarina, Florianópolis, Brazil); USNM (National Museum of Natural History, Smithsonian Institution, Washington D.C.); ZMB (Zoologisches Museum Berlin, Berlin, Germany). Uncataloged material is identified by the abbreviation of the museum where it is currently housed followed by field numbers with the following prefixes: AN = A. Nunes; APC = A.P. Carmignoto (Universidade Federal de São Carlos, Brazil); BDP = B.D. Patterson (FMNH); CGB = C.G. Bantel (INPA); JFV = J.F. Vilela (FMNH); LHE = L.H. Emmons (USNM); MTR = M.T. Rodrigues (Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Brazil). The prefixes ARP, CB, EDH, MN6, PEU, PNSC, RL, SAPO, and UNIBAN correspond to field series of the MZUSP; CZ, IAVRD, JUR, LPP, MBA, MS, STA, TF, TGP correspond to field series at the MPEG; the prefix A corresponds to a field series at the MN; “masto” corresponds to a field series at the MACN-Ma; the prefixes CC, LFS, and RM correspond to field series of the UFMG. The unprefixed numeral “144” corresponds to a field series at the UFSC. Taxon sampling: We examined 1931 specimens of Monodelphis for this study, including representative material of all of the 22 species currently recognized as valid. Among the speci- mens we examined are 280 specimens that were sequenced in previous DNA-based phyloge- netic studies. We provide a list of the material examined in appendix 1. Age criteria: Specimens were classified into dental age classes following Pavan et al. (2012), who refined the system originally proposed by Van Nievelt and Smith (2005). Speci- mens were considered juvenile if M4 was not present, subadult if M4 was present but still incompletely erupted,2 and adult if M4 was completely erupted. Adult specimens with only incipient wear on M3 and M4 (cristae unworn or with very narrow and discontinuous strips of exposed dentine) were considered young adults. Those with light wear on M3 and M4 (den- tine narrowly exposed on M3 cristae and very narrowly exposed on M4 cristae) were consid- ered full adults, and those with conspicuous wear on M3/M4 (dentine broadly exposed on M3 cristae and narrowly to broadly exposed on M4 cristae) were considered old adults. Qualitative characters: We examined skulls, skins, and fluid-preserved material for taxonomic variation in qualitative morphological characters. Surveyed characters include those previously described in the literature (e.g., Thomas, 1888a; Pine, 1975; Pine and Handley, 1984; Voss et al., 2001; Voss and Jansa, 2003; Lew and Pérez-Hernández, 2004; Solari, 2004, 2007; Pine and Handley, 2008; Voss and Jansa, 2009; Pavan et al., 2012; Voss et al., 2012; Pine et al., 2 Eruption of M4 and P3 are usually simultaneous in Monodelphis, so subadults by this definition (with incom- pletely erupted M4) usually also have incompletely erupted P3. 2016 PAVAN AND VOSS: SUBGENERA OF SHORT-TAILED OPOSSUMS (MONODELPHIS) 5 FIG. 1. Dorsal views of skins with alternative color patterns (see text for pelage descriptors): A, Monodelphis adusta (KU 157978); B, M. arlindoi (CM 68359); C, M. emiliae (AMNH 268221); D, M. americana (AMNH 133241); E, M. unistriata (MACN-Ma 250). Scale bars = 50 mm. 6 AMERICAN MUSEUM NOVITATES NO. 3868 2013; Duda and Costa, 2015; Pavan, 2015) as well as other characters newly described herein. Descriptive terminology that we use to describe external and craniodental morphology in this report follows Cope (1880), Gregory (1910), Archer (1976), Wible (2003), and Voss and Jansa (2003, 2009). We recorded the sex and age of each specimen to evaluate qualitative characters for sexual dimorphism and ontogenetic variation, respectively, although no formal tests for the effects of age and sex on character variation among conspecific individuals is reported here. COMPARATIVE MORPHOLOGY Species of Monodelphis differ from one another in numerous morphological characters, of which those of the integument, skull, and dentition are maximally useful for taxonomic diag- noses. In particular, we emphasize characters with alternative states that distinguish the mono- phyletic groups of species recognized as subgenera in this report. Therefore, we omit descriptions of characters that are primarily useful for distinguishing closely related species within subgen- era, which will be treated in subsequent publications. In the following descriptive accounts of taxonomic character variation, we follow the spe- cies-group classification of Pavan et al. (2016), which is summarized in table 1. External Characters Dorsal color pattern: The dorsal body pelage of Monodelphis can be either uniformly colored (unpatterned) or distinctively marked. Unpatterned dorsal pelage, lacking any abrupt color transition (fig. 1A), is observed in M. domestica, M. sanctaerosae, some specimens of M. brevicaudata (those from NW Guyana and NE Venezuela), some old adult male specimens of M. americana, and all species of the Adusta Group. By contrast, a grizzled-grayish or -brownish middorsum contrasting with clear (ungrizzled) yellowish, orange, or reddish flanks (fig. 1B) is exhibited by M. dimidiata and by most species of the Brevicaudata Group, whereas a grayish midbody contrasting with reddish head and rump (fig. 1C) is seen in M. emiliae and in adult male specimens of M. scalops. A fourth dorsal pelage phenotype, consisting of three dark lon- gitudinal stripes (fig. 1D), characterizes juveniles and females of M. scalops and most age-sex classes of species in the Americana Group (old adult males of M. americana are the exception; see above). Clear yellowish or orange flanks with a grizzled-brownish or -grayish middorsum that contrasts with a single dark median longitudinal stripe (fig. 1E) is apparently unique to M. unistriata. Ventral pelage markings: Most species of Monodelphis have uniformly colored under- parts that usually consist of hairs that are grayish basally and variously colored distally (e.g., with brownish, reddish, or whitish tips; fig. 2B, C). Some species, however, have self-whitish midventral markings (comprising hairs that are whitish from root to tip) that contrast with the darker (usually brownish or grayish) coloration of the surrounding ventral pelage (fig. 2A). Such markings were observed uniquely on species of the Adusta Group. Mammae: Mammae exhibit greater taxonomic variation in Monodelphis than in any other didelphid genus, encompassing the entire range of morphologies previously reported for the 2016 PAVAN AND VOSS: SUBGENERA OF SHORT-TAILED OPOSSUMS (MONODELPHIS) 7 FIG. 2. Ventral views of skins with alternative pelage markings (see text): A, Monodelphis handleyi (MUSM 23810); B, M. glirina (MVZ 197456); C, M. touan (USNM 549280). Scale bar = 50 mm. 8 AMERICAN MUSEUM NOVITATES NO. 3868 family as a whole. Observed mammary formulae (defined by Voss and Jansa, 2009: 23) range from 2–0–2 = 4 (in M. peruviana) to 13–1–13 = 27 (in M. dimidiata). Lower mammary counts (of nine or fewer mammae) include only abdominal-inguinal teats, but higher counts (≥ 13 mammae in this study) include both abdominal-inguinal and pectoral teats. Mammary mor- phology could not be determined for several species that are currently known only from adult males, or for which we did not examine any females with visible teats. Pedal thenar pad: The plantar (ventral) surface of the hind foot of most plantigrade mammals includes two tarsal and four interdigital pads (Brown and Yalden, 1973). Of these, the thenar (medial tarsal) and the first interdigital pad are clearly separated from one other in most species of Monodelphis (e.g., M. americana; fig. 3B), but in M. emiliae the thenar and first interdigital pad are either fused or in contact (fig. 3A). Pedal hypothenar pad: The hypothenar (lateral tarsal) pad of the hind foot is usually absent or vestigial in several species of Monodelphis, including M. americana, M. scalops (fig. 3C), M. dimidiata, and species of the Brevicaudata Group. By contrast, a small but distinct hypothenar pad is consistently present in members of the Adusta Group, M. iheringi (fig. 3D) and in M. emiliae. Extension of body pelage onto tail: In most species of Monodelphis the body pelage (comprising soft underfur and long guard hairs) extends farther onto the tail dorsally than ventrally (e.g., in M. brevicaudata; Voss et al., 2001: fig. 29A), or it extends to about the same extent dorsally and ventrally (e.g., in M. palliolata; Voss et al., 2001: fig. 29B). By contrast, although the tail base seems almost completely unfurred in species of the Adusta Group, close inspection reveals that body pelage uniquely extends farther onto the tail ventrally than dor- sally (e.g., in M. handleyi). Caudal scale pattern: In most species of Monodelphis the scales that encircle the tail are arranged in predominantly annular series, but some species have caudal scales arranged in spiral series. The annular pattern was observed in M. emiliae, M. scalops, and in species of the Americana and Brevicaudata groups (e.g., M. glirina; fig. 4A), whereas examined specimens of M. dimidiata (fig. 4B) and M. unistriata have caudal scales that are arranged in unambiguously spiral series. Tail scales are small and often inapparent in species of the Adusta Group, in which some species seem to have scales arranged in both annular and spiral series (e.g., M. adusta), whereas others have scales that are mostly in spiral series (e.g., M. pinocchio) or annular series (e.g., M. kunsi). Craniodental Characters Infraorbital foramen: The infraorbital foramen varies taxonomically in its position with respect to the maxillary dentition. In some species this foramen is dorsal to P3 (e.g., in Monodelphis domestica; fig. 5A), while in others it is dorsal to M1 (e.g., in M. adusta; fig. 5B) or to the P3/M1 commissure. Quite variable in a few species (e.g., in M. dimidiata), this char- acter is conservative in many others, and in combination with additional characters it is useful for diagnosing groups of species. For example, the infraorbital foramen is usually dorsal to M1 2016 PAVAN AND VOSS: SUBGENERA OF SHORT-TAILED OPOSSUMS (MONODELPHIS) 9 FIG. 3. Plantar views of left hind feet, illustrating taxonomic differences in plantar pad morphology. The thenar (th) and first interdigital pad (ip1) are fused in M. emiliae (A, MZUSP 35062), and separate in M. americana (B, MZUSP 29469). The hypothenar pad (hy) is absent in M. scalops (C, MZUSP 29203), and present in M. iheringi (D, MZUSP 3421). Not to the same scale. 10 AMERICAN MUSEUM NOVITATES NO. 3868 in the Adusta and Americana groups, but it is often dorsal to P3 among members of the Brevicaudata Group. Frontal process of jugal: In most spe- cies of opossums, the frontal process of the jugal is a prominent landmark that defines the posteroventral limit of the orbital fossa. By contrast, this structure exhibits noteworthy taxonomic variation in Monodelphis. The fron- tal process is usually absent or indistinct in species of the Adusta Group, in which the jugal never projects dorsally above the zygo- matic process of the squamosal (e.g., in M. peruviana; fig. 6A), whereas the frontal pro- cess forms a smoothly rounded dorsal projec- tion in M. emiliae (fig. 6B), M. dimidiata, and members of the Brevicaudata Group. By con- trast, in M. scalops and members of the Amer- icana Group (e.g., M. americana; fig. 6C) the frontal process is well defined and distinctly FIG. 4. Close-up views of tail illustrating caudal angular. scales arranged in annular series (A, Monodelphis glirina, MZUSP MTR 10164) and spiral series (B, M. Parietal/mastoid contact: The pari- dimidiata, MZUSP 34257). Not to the same scale. etal is usually in contact with the mastoid (the occipital exposure of the petrosal bone) in Monodelphis, because the interparietal does not extend laterally to contact the squamosal (e.g., in most specimens of Monodelphis glirina; fig. 7A). In most species of the Adusta Group, however, the interparietal consistently extends laterally to reach the squamosal and, as a result, the parietal is not in contact with the mastoid (e.g., in M. handleyi; fig. 7B). In M. pinocchio the interparietal is absent in all specimens examined, but the parietal does not contact the mastoid because the supraoccipi- tal is in contact with the squamosal. Incisive foramina: The length of the incisive foramina exhibits modest taxonomic varia- tion in Monodelphis. We distinguish “long” and “short” incisive foramina based on their pos- terior endpoints in relation to the upper canines. In M. dimidiata and M. unistriata, for example, the incisive foramina are notably short, extending from the level of I3 or I4 to a point between the left and right paracanine fossae or just to—but not appreciably between—the canines. In most other species the incisive foramina are long, extending posteriorly well between the canines. Maxillopalatine fenestrae: For diagnostic purposes, we distinguish “long” and “short” maxillopalatine fenestrae based on their anterior and posterior endpoints in relation to adja- cent maxillary teeth. Whereas most species have long maxillopalatine fenestrae that extend