A M ERIC AN MUSEUM NOVITATES Number 3872, 20 pp. February 10, 2017 A New Species of Monodelphis (Didelphimorphia: Didelphidae) from the Brazilian Amazon SILVIA E. PAVAN,1,2 ANA C. MENDES-OLIVEIRA,3 AND ROBERT S. VOSS1 ABSTRACT We describe a new species of the didelphid marsupial genus Monodelphis from Brazil, where it appears to be widely distributed in the states of Pará, Mato Grosso, Rondônia, and Acre. Monodelphis saci, new species, belongs to the subgenus Mygalodelphys, and analyses of DNA sequence data suggest that it is most closely related to M. handleyi, M. osgoodi, and M. peruviana. Diagnostic morphological traits include pelage coloration, qualitative aspects of cra- niodental morphology, and a distinctive range of morphometric variation. The new species has sometimes been misidentified in the literature as M. kunsi, a distinct but apparently allopatric taxon. Monodelphis saci occurs sympatrically with M. emiliae, M. glirina, and M. touan in the rainforested lowlands south of the Amazon River. INTRODUCTION American marsupials of the genus Monodelphis Burnett, 1830, are widespread in South America, ranging from high elevations in the Andes across Amazonia to the Atlantic Forest in southeastern Brazil and the temperate grasslands of northern Argentina (Pine and Handley, 1 Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History. 2 Current address: Coordenação de Zoologia, Museu Paraense Emílio Goeldi. 3 Laboratório de Ecologia e Zoologia de Vertebrados, Instituto de Ciências Biológicas, Universidade Federal do Pará. Copyright © American Museum of Natural History 2017 ISSN 0003-0082 2 AMERICAN MUSEUM NOVITATES NO. 3872 TABLE 1. Mean uncorrected cytochrome-b distances (scaled as percent sequence divergence) among spe- cies of Monodelphis, subgenus Mygalodelphys. The diagonal elements (in parentheses) correspond to mean pairwise distances among conspecific sequences. See Pavan et al. (2014) for analytical methods, GenBank accession numbers, and other information about sequenced material. adusta handleyi kunsi osgoodi peruviana pinocchio reigi “species 2” adusta (N = 7) (0.6) handleyi (N = 6) 12.8 (0.5) kunsi (N = 22) 13.2 15.1 (3.6) osgoodi (N = 6) 11.0 9.3 14.2 (1.9) peruviana (N = 17) 11.0 9.5 13.9 8.4 (3.8) pinocchio (N = 3) 14.5 15.0 11.1 14.3 13.9 (1.0) reigi (N = 2) 9.2 9.8 14.2 9.2 9.4 13.3 (0.4) “species 2” (N = 3) 9.7 9.2 13.6 8.1 8.9 14.0 9.4 (2.7) 2008; Pavan et al., 2016). Twenty-two named species in five subgenera are currently recognized as valid (Pavan and Voss, 2016), but several new species remain to be described (Pavan et al., 2014, 2016; Vilela et al., 2015). This report concerns the Brazilian form that Pavan et al. (2014, 2016) called Monodelphis “species 2.” Their analyses of DNA sequence data indicated that this informally recognized taxon—represented by several specimens from Pará and Rondônia—belongs to a monophyletic group with M. adusta (Thomas, 1897) and six other congeneric species comprising the “Adusta Group” (fig. 1). Consistently large genetic distances among members of this complex (>8%, uncorrected, at the cytochrome-b locus; table 1) suggested that each is an evolutionarily inde- pendent lineage, but this inference was not explicitly tested with either multilocus data or phenotypic traits in Pavan et al.’s (2014, 2016) reports. Subsequently, Pavan and Voss (2016) referred “species 2” to the subgenus Mygalodelphys based on these molecular results. Close examination of sequenced specimens corresponding to Monodelphis “species 2” indi- cates that this form can be distinguished from all other congeneric taxa by a distinctive suite of external and craniodental features. These traits provide a sufficient basis for referring unsequenced material (including recently collected specimens from Acre and Mato Grosso) to a new species, which we formally describe and name below. MATERIAL AND METHODS Specimens listed in this report are deposited in the following collections (in the United States except as noted otherwise): AMNH (American Museum of Natural History, New York), ANSP (Academy of Natural Sciences, Philadelphia), BMNH (Natural History Museum, London, UK), CM (Carnegie Museum of Natural History, Pittsburgh), FMNH (Field Museum, Chicago), KU (Biodiversity Research Center and Natural History Museum, Uni- versity of Kansas, Lawrence), LMUSP (Coleção do Laboratório de Mamíferos da Escola Superior de Agricultura “Luiz de Queiroz,” Universidade de São Paulo, São Paulo, Brazil), MACN-Ma (Colección de Mamíferos del Museo Argentino de Ciencias Naturales “Ber- 2017 PAVAN ET AL.: NEW SPECIES OF MONODELPHIS 3 Brazil, São Paulo: MZUSP 30740 Brazil, Minas Gerais: MTR 10770 pinocchio Brazil, Espírito Santo: MTR 11578 Bolivia: Tarija: AMNH 263968 Brazil, Tocantins: MZUSP 35059 kunsi Brazil, Mato Grosso: MPEG 43017 Guyana, Potaro-Siparuni: ROM 114699 reigi Peru, Loreto: KU 157978 Peru, Loreto: TTU 101164 adusta Ecuador, Pastaza: TTU 84899 Brazil, Rondônia: UNIR M451 Brazil, Pará: MPEG 40575 Brazil, Pará: MPEG 42956 species 2 Brazil, Pará: MPEG 38947 Peru, Loreto: AMNH 276709 Peru, Loreto: AMNH 276698 handleyi Peru, Loreto: AMNH 276704 Bolivia, Cochabamba: AMNH 264922 osgoodi MPML Peru, Loreto: AMNH 272695 BPP Peru, Junin: USNM 582110 Bolivia, La Paz: AMNH 264562 peruviana 0.05 Peru, Cusco: MVZ 171412 substitution/site Peru, Cusco: FMNH 172032 FIG. 1. Phylogenetic relationships of species of the subgenus Mygalodelphys based on a maximum-likelihood analysis of DNA sequence data from one mitochondrial and four nuclear genes (4983 aligned sites; after Pavan et al., 2014). Support statistics from maximum-parsimony (MP) and maximum-likelihood (ML) bootstrap analyses are indicated at each resolved node along with Bayesian posterior probabilities (BPP). White wedges indicate MP and ML bootstrap frequencies ≤50%, gray indicates bootstrap frequencies between 50% and 75%, and black indicates bootstrap frequencies ≥75%. For Bayesian statistics, white indicates BPP <0.95, whereas black indicates BPP ≥0.95. nardino Rivadavia,” Buenos Aires, Argentina), MCN-M (Coleção de Mamíferos, Museu de Ciências Naturais da Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, Bra- zil), 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), MSU (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), OMNH (Sam Noble Oklahoma Museum of Natural History, Oklahoma), ROM (Royal Ontario Museum, Toronto, Canada), TTU (Museum of Texas Tech University, Lubbock), UFMG (Universidade Federal de Minas Gerais, Belo Horizonte, Brazil), UFMT (Coleção Zológica do Instituto de Biociências da Universidade Federal de Mato Grosso, Mato Grosso, Brazil), UFPA (Universidade Federal do Pará, Belém, Brazil), UFSC (Universidade Federal de Santa Catarina, Florianópolis, Bra- zil), UNIR (Fundação Universidade Federal de Rondônia, Porto Velho, Brazil), and USNM (National Museum of Natural History, Smithsonian Institution, Washington DC). Our descriptive terminology for external and craniodental morphology follows Wible (2003) and Voss and Jansa (2009); capitalized color nomenclature follows Ridgway (1912). External measurements (typically recorded to the nearest millimeter, mm) and weight (in grams, g) for each examined specimen were transcribed from specimen labels or field notes. External measurements included total length (nose to tail tip, TL), length of tail (basal flexure to tip, LT), length of hind foot (heel to tip of longest claw, HF), and length of ear (from notch, Ear). Head-and-body length (HBL) was computed by subtracting LT from TL. 4 AMERICAN MUSEUM NOVITATES NO. 3872 -68º -64º -60º -56º -52º 48º 0º Amazonas s n ós nti á aj a u p c Jur Purus Madeira 8 T7a Xingu To -4º 3 6 1 9–11 5 4 2 Amazonas -8º Pará 13 12 Acre 14 Rondônia Mato Grosso -12º FIG. 2. Collecting localities of Monodelphis saci. Localities for which we did not examine specimens are rep- resented by squares. Numbers are keyed to localities mentioned in the text. Craniodental measurements were determined to the nearest 0.01 mm using digital calipers as specimens were viewed under a stereomicroscope (at 6–25×), but craniodental measurement values and sample means are rounded to the nearest 0.1 mm in our tables and text. The following dimensions were recorded: condylo-basal length (CBL), measured from the occipital condyles to the anteriormost point of the premaxillae; nasal length (NL), the greatest anteroposterior dimen- sion of either bone; nasal breadth (NB), measured between the triple-point sutures of the nasal, frontal, and maxillary bones on each side; palatal length (PL), measured from the anteriormost point of the premaxillae to the postpalatine torus, including the postpalatine spine (if present); palatal breadth (PB), measured across the labial margins of the upper fourth molar (M4) crowns at or near the stylar A position; maxillary toothrow length (MTR), measured from the anterior margin of the upper canine (C1) to the posterior margin of M4; length of molars (LM), measured from the anteriormost labial margin of M1 to the posteriormost point on M4; length of M1–M3 (M1–3), measured from the anteriormost labial margin of the upper first molar (M1) to the posteriormost point on upper third molar (M3); width of M3 (WM3), measured from the labial margin of the crown at or near the stylar A position to the lingual apex of the protocone; length of maxillopalatine fenestra (LMPF), the greatest anteroposterior dimension of one maxillopala- tine fenestra; least interorbital breadth (LIB), measured at the narrowest point across the frontals between the orbits, even when the postorbital constriction (between the temporal fossae) is nar- rower; postorbital constriction (POC), measured at the narrowest point across the frontals 2017 PAVAN ET AL.: NEW SPECIES OF MONODELPHIS 5 between the temporal fossae; breadth of braincase (BBC), measured immediately above the zygo- matic process of the squamosal on each side; zygomatic breadth (ZB), measured at the widest point across both zygomatic arches. RESULTS Monodelphis (Mygalodelphys) saci, new species Figures 4–8 Holotype: The holotype consists of the skin, skull, postcranial skeleton, and preserved tissues of an adult male (UFPA 1422, original number JD 05) from Bom Jardim, Tapajós, Itai- tuba, Pará, Brazil (5.61° S, 57.12° W; fig. 2: locality 9), collected on 11 January 2013 by A.C. Mendes-Oliveira. Paratypes: We refer 17 other examined specimens from the Brazilian state of Pará to Monodelphis saci, including: the skull, postcranial skeleton, and preserved tissues of a young adult animal of unknown sex (MPEG 38947 [original number IAVRD 1135]) from Barragem da Pêra, Serra dos Carajás, Marabá (6.00° S, 50.21° W; fig. 2: locality 1) collected on 22 Febru- ary 2005 by personnel from the Vale do Rio Doce Environmental Institute; the skins, skulls, and postcranial skeletons of three adult males (MCN-M 2301, MN 73872, MN 74003 [original numbers BM 72, FMH 127, FMH 420]), one juvenile male (MCN-M 1962 [original number ELP 007]), and one juvenile female (MN 74002 [original number FMH 356]) from Floresta Nacional de Carajás, Parauapebas (6.05° S, 50.25 W; fig. 2: locality 2)4; the skin, skull, and postcranial skeleton of an adult female (MN 75511 [original number FMH 827]) from Floresta Nacional de Tapirapé-Aquiri, Marabá (5.80° S, 50.52° W; fig. 2: locality 3) collected on 24 Feb- ruary 2010 by D. Gettinger; the skin and preserved tissues of an adult male (MPEG 40575 [original number CT 05]) from Rio das Tropas, Floresta Nacional do Crepori, Itaituba (6.52° S, 51.43° W; fig. 2: locality 4) collected on 29 April 2008 by S. Morato and L. Phov; a skin with skull in alcohol and preserved tissues of an adult female (MPEG 42956) from Mina do Palito, Itaituba (6.31° S, 55.78° W; fig. 2: locality 5), collected on 21 March 2012 by A.O. Maciel and J.O. Gomes; the skin of an apparently juvenile male (MPEG 41820 [original number CAC 308]) from Jardim do Ouro, Itaituba (ca. 6.27° S, 55.90° W; fig. 2: locality 6) collected on 4 April 2011 by C. Braga; the skin and skull of an adult male (MZUSP 12207 [original number B-M-1]) from Uruá, Parque Nacional da Amazonia, Transamazon Km 65 (4.62° S, 56.25° W; fig. 2: locality 7) collected on 22 August 1978 by L.C. Branch; the skins, skulls, postcranial skeletons, and preserved tissues of two adult males (UFPA 1394, 1395 [original numbers JB 09, JB 10]) from Boca do Rato, Tapajós, Itaituba (5.23° S, 56.93° W; fig. 2: locality 8) collected on 19 Janu- ary 2013 by A.C. Mendes-Oliveira; the skin, skull, and postcranial skeleton of an adult male (UFPA 1260 [original number JMID 27]) and the skin and preserved tissues of an adult female 4 Of these, MCN-M 2301 was collected on 18 December 2008 by R. Carvalho; MCN-M 1962 was collected on 16 January 2009 by E.L. Paschoalini; and MN 73872, 74002, and 74003 were collected respectively on 14 February 2009, 25 July 2009, and 25 February 2010, by D. Gettinger. 6 AMERICAN MUSEUM NOVITATES NO. 3872 FIG. 3. Forest vegetation along the middle Tapajós, Pará, Brazil, illustrating capture sites of Monodelphis saci. A–B, terra firme forest (Bom Jardim and Penedo); C, igapó forest (Boca do Rato). (UFPA 1738 [original number JD 33]) from Penedo, Tapajós, Itaituba (with two sets of coor- dinates [5.59° S, 57.12° W and 5.57° S, 56.13° W]; fig. 2: localities 10, 11) collected on 15 October 2012 and 17 June 2013 by A.C. Mendes-Oliveira; the skin, skull, and carcass in alcohol of an adult male (UFSC 5210 [original number JC 3409]) from Marabá (specific locality unknown) collected on 25 January 2013 by G. Mette; and the skin of an apparently juvenile female (MPEG 42601 [original number L079]) from São Félix do Xingu, (specific locality unknown) collected on 27 October 2011 by L.H. Diniz and T.R. Diniz. Other specimens: Four additional Brazilian specimens, apparently representing this spe- cies, have been reported in the literature, but we were not able to examine them for the present study. Among these, Semedo et al. (2011) reported one specimen (UFMT 1355) from Fazenda São Nicolau, Mato Grosso (9.85° S, 58.22° W; fig. 2: locality 12), collected in December 2009. Additionally, Pavan et al. (2014) analyzed DNA sequences from one specimen (UNIR M451) from Madeflona, Floresta Nacional do Jamari, Rondônia (9.14° S, 63.00° W; fig. 2: locality 13), collected in February 2012 by R. Mendonça and M.R. Messias. Lastly, Abreu-Júnior et al. (2016) reported two specimens (LMUSP 279, 280) from Estação Ecológica do Rio Acre, Acre (10.75° S, 70.52° W; fig. 2: locality 14) collected in April 2015 and February 2016. Associated sequence data: DNA sequences from one mitochondrial gene (cytochrome b), two autosomal exons (IRBP exon 1, BRCA1 exon 11), one autosomal intron (SLC38 intron 2017 PAVAN ET AL.: NEW SPECIES OF MONODELPHIS 7 7), and one X-linked intron (OGT intron 14) obtained from MPEG 40575 and MPEG 42956 were included in the phylogenetic analyses of Pavan et al. (2014) and are deposited in GenBank with accession numbers KM071402, KM071124, KM071035, KM071316, and KM071221 (cor- responding to sequences obtained from MPEG 40575), and KM071403, KM071123, KM071034, KM071315, and KM071220 (corresponding to sequences obtained from MPEG 42956). DNA sequences from cytochrome b, BRCA1 exon 11, and OGT intron 14 loci of MPEG 38942 were also included in the phylogenetic analyses of Pavan et al. (2014) and are deposited in GenBank with accession numbers KM071404, KM071036, and KM071317. Distribution: Monodelphis saci is currently known from at least 14 localities scattered along the south bank of the Amazon in the Brazilian states of Pará, Mato Grosso, Rondônia, and Acre (fig. 2). Description: Dorsal pelage superficially brownish from behind ears to rump (varying from near Clove Brown to Olive Brown, slightly darker on the rump than over the shoul- ders), without distinct stripes or other sharp pigmental discontinuities, but head conspicu- ously reddish (near Sepia); middorsal fur 4–5 mm long and grayish basally. Ventral pelage gray-based and usually brownish on most of chin, throat, groin, and flanks, but abruptly self-whitish midventrally on chest and abdomen.5 Pinnae macroscopically naked, but densely covered internally and externally with short, brown hairs. Mystacial and supraorbital vibris- sae mostly dark, with longest mystacial hairs extending behind eyes when laid flat against cheek but not reaching pinnae. There are two supraorbital vibrissae on each side (but only one is present on the right side on MPEG 42601 and UFPA 1422). Genal vibrissae lighter colored than the remaining facial vibrissae, usually reaching the pinnae but rarely extending behind their posterior border. Gular gland (indicated by an area of yellowish fur on the throat) present in all mature males and, apparently, in one out of three mature females exam- ined. Hands and feet covered dorsally with short, mostly light-brown hairs. Ungual tufts very short (restricted to the bases of the manual claws and reaching only the middle of the pedal claws). Thenar and first interdigital pad of pes separate (not fused). Hypothenar pad of pes present (e.g., on MCN-M 2301) or absent (e.g., on MPEG 42956). Scrotal skin light brownish to cream, covered with pale (near Tilleul-Buff) hairs. Mammary formula apparently 3–0–3 = 6 (MPEG 42956), all abdominal-inguinal. Tail about half as long as combined length of head and body (mean LT/HBL = 0.51 in 8 males, 0.46 in three females; tables 2, 3), dark brown dorsally but mottled ventrally with pale blotches in mature specimens. Body pelage extends onto tail farther ventrally than dorsally. Caudal scales (discernible mostly on the distal portion of the tail) arranged in predominantly spiral series. Skull unremarkable in general aspect (not conspicuously flattened; rostrum neither greatly elongated nor unusually short). Infraorbital foramen dorsal to anterior root of M1; anterior margin of lacrimal dorsal to M2 or to M1/M2 commissure; two lacrimal foramina usually present on anterior orbital margin. Interorbital region hourglass shaped, with rounded supra- orbital margins, and lacking distinct processes, but supraorbital surface of frontals with 5 The ventral pelage of MPEG 40575, MZUSP 12207, and UFSC 5210 is dirty cream in general aspect, such that this marking is absent or indistinct. 8 AMERICAN MUSEUM NOVITATES NO. 3872 FIG. 4. Adult female of Monodelphis saci (MPEG 42956), from Mina do Palito, Itaituba, Pará, Brazil. Photos: A.O. Maciel. V-shaped temporal scars in large males (e.g., UFPA 1395, UFSC 5210, MZUSP 12207); sagittal crest absent even in largest adult males examined; nuchal (occipital) crest present, restricted to dorsolateral margin of the skull (interrupted middorsally); no parietal-mastoid contact on pos- terior braincase (interparietal extends laterally to contact squamosal, except on left side of MZUSP 12207); zygomatic arches laterally expanded, with anterior connection to skull marked by shallow but distinct inflection in all examined mature specimens; frontal process of jugal absent or indistinct. Incisive foramina extending from level of third upper incisors to between upper canines (never behind C1s); maxillopalatine fenestrae extending from M1 to posterior margin of M2 or middle of M3; anterior margin of maxillopalatine fenestrae usually posterior to infraorbital foramen in mature specimens (but ventral to the foramen on UFPA 1394); palatine fenestrae present (e.g., in MPEG 38947; MN 73872, 75511) or absent (e.g., MZUSP 12207; UFPA 1260, 2017 PAVAN ET AL.: NEW SPECIES OF MONODELPHIS 9 1395); posterolateral palatal foramina small (not extending anteriorly between M4s) and com- plete (with an entire posterior bony margin); basisphenoid concealed by alisphenoid in lateral view (not exposed through sphenorbital fissure in posteromedial orbit); infratemporal crest of alisphenoid usually distinct; tympanic wing of alisphenoid small, uninflated, and widely sepa- rated from rostral tympanic process of petrosal; rostral tympanic process narrow, triangular, and widely separated from caudal tympanic process (fenestra cochleae exposed); anterior pro- cess of malleus exposed between ectotympanic annulus and tympanic wing of alisphenoid; extracranial course of mandibular nerve not enclosed by bone (secondary foramen ovale absent); stapes columelliform and imperforate; subsquamosal foramen large (substantially wider than the squamosal strut which separates this opening from the postglenoid foramen); parocciptal process elongated, dorsoventrally directed. Crowns of I2–I5 increasing in width from front to back (such that the crown of I5 is dis- tinctly wider than the crown of I2); upper canines usually simple, without distinct accessory cusps (but tiny accessory cusps are sometimes present in juveniles and young adults; e.g., in MN 74002, 74003, 75511); postcanine diastemata very small or absent in upper dentition; P2 and P3 usually subequal in width, or P3 slightly wider than P2 (e.g., on UFPA 1260 and 1422). Lower dentition also without distinct postcanine diastemata; p2 and p3 subequal in height; anterior cingulid of lower molars narrow (on m2 and m3 these shelves are unambiguously lingual to the hypoconids of m1 and m2, respectively); lower milk premolar (dp3) narrow, with an incomplete (bicuspid) trigonid and a minimally differentiated anterior cingulid (MN 74002); entoconids of m1–m3 small or indistinct. Comparisons: Monodelphis saci shares the diagnostic external and craniodental traits of the subgenus Mygalodelphys and therefore differs from species in other subgenera by having body fur that extends onto the tail farther ventrally than dorsally, lacking a distinct frontal process of the jugal, lacking parietal-mastoid contact on the lateral braincase, having a small sphenorbital fissure through which the basisphenoid is not exposed laterally, having narrow anterior cingulids on m2 and m3, and having indistinct entoconids on m1–m3 (Pavan and Voss, 2016). Additionally, M. saci can be distinguished externally from sympatric congeners by its much smaller size and by its lack of conspicuously patterned dorsal pelage: whereas M. saci is uniformly brownish with reddish highlights only on the head, M. glirina (Wagner, 1842) and M. touan (Shaw, 1800) have reddish flanks, and M. emiliae (Thomas, 1912) has a grayish mid- body contrasting with its reddish head and rump. Monodelphis saci can be distinguished from other species of the subgenus Mygalodelphys by a distinctive range of morphometric variation (tables 2, 3)6 as well as qualitative external and craniodental traits. Among the latter, no other species of Mygalodelphys has a distinctly reddish head, nor does any other congener have pale mottling on the underside of the base of the tail. Other relevant comparisons with species of Mygalodelphys are summarized below. Monodelphis saci can be readily distinguished from M. handleyi Solari, 2007, and M. ron- aldi Solari, 2004, by its much smaller size (most external and all craniodental dimensions of 6 For comparative measurements of M. handleyi, M. ronaldi, M. reigi, M. osgoodi, M. pinocchio, and M. kunsi see Pavan (2015: table 1). 10 AMERICAN MUSEUM NOVITATES NO. 3872 FIG. 5. Dorsal (A), lateral (B), and ventral (C) views of the holotype skin of Monodelphis saci (UFPA 1422). Scale bar = 50 mm.