A New Genus and Species of Rodent from the Brazilian Atlantic Forest (Rodentia: Cricetidae: Sigmodontinae: Oryzomyini), with Comments on Oryzomyine Biogeography

Home , Akodon spegazzinii, Brucepattersonius, Drymoreomys, Holochilus brasiliensis, Microryzomys, Oligoryzomys nigripes

Zoological Journal of the Linnean Society, 2011, 161, 357–390. With 9 ﬁgures

A new genus and species of rodent from the Brazilian Atlantic Forest (Rodentia: Cricetidae: Sigmodontinae: Oryzomyini), with comments on oryzomyine biogeography

ALEXANDRE R. PERCEQUILLO1*, MARCELO WEKSLER2 and LEONORA P. COSTA3

1Departamento de Ciências Biológicas, Escola Superior de Agricultura ‘Luiz de Queiroz’, Universidade de São Paulo, Avenue Pádua Dias, 11, Caixa Postal 9, Piracicaba, São Paulo, 13418-900, Brazil 2Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024-5192, USA 3Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, Avenue Marechal Campos, 1468, Campus de Maruípe, Vitória, Espírito Santo, 29040-090, Brazil

Received 1 September 2009; revised 29 October 2009; accepted for publication 2 November 2009

We describe in this paper a new genus and species of cricetid rodent from the Atlantic Forest of Brazil, one of the most endangered eco-regions of the world. The new form displays some but not all synapomorphies of the tribe Oryzomyini, but a suite of unique characteristics is also observed. This new forest rat possesses anatomical characteristics of arboreal taxa, such as very developed plantar pads, but was collected almost exclusively in pitfall traps. Phylogenetic analyses of morphological (integument, soft tissue, cranial, and dental characters) and molecular [nuclear – Interphotoreceptor retinoid binding protein (Irbp) – and mitochondrial – cytochrome b – genes] datasets using maximum likelihood and cladistic parsimony approaches corroborate the inclusion of the new taxon within oryzomyines. The analyses also place the new form as sister species to Eremoryzomys polius,an Andean rat endemic to the Maranon valley. This biogeographical pattern is unusual amongst small terrestrial vertebrates, as a review of the literature points to few other similar examples of Andean–Atlantic Forest pairings, in hylid frogs, Pionus parrots, and other sigmodontine rodents.

ADDITIONAL KEYWORDS: Brazil – cytochrome b – Irbp – morphology – phylogeny – South America – systematic – total evidence.

INTRODUCTION now reduced to less than 7–10% of its pre-Columbian distribution in Brazil (Brito, 2004; Metzger, 2009). The Atlantic Forest is one of the most diverse and The biological diversity of the Atlantic Forest, in threatened tropical forests in the world (Ribeiro et al., terms of both richness and endemism, is amongst the 2009). Originally ranging from Rio Grande do Norte highest in the world (Fonseca, 1985; Ribeiro et al., to Rio Grande do Sul in Brazil, and in eastern Para- 2009). The biome is thus considered a threatened guay and northern Argentina, the ‘Mata Atlântica’ is biodiversity hotspot (Myers et al., 2000; Laurance, 2009), and conservation efforts are under way to protect all remaining forested areas in the region *Corresponding author. E-mail: [email protected] (Metzger, 2009).

The Atlantic Forest is composed of different types of consequence of increased inventory efforts, new collect- vegetation formations (e.g. ‘restinga’, lowland, and ing techniques (e.g. pitfall traps), and the emergence of montane forests), distributed from sea level to about a new generation of South American mammalogists 2000 m altitude (Hueck, 1972). The ‘Mata Atlântica’ (see Patton et al., 1997: 463). occurs along the coastal lowlands, the mountains or We report here a new sigmodontine rodent pre- ‘Serras’ of eastern Brazil (Clapperton, 1993), and viously unknown to the scientific community. Two throughout the major river basins of eastern South independent programmes of inventories of small America (e.g. Paraguay, Paraná, São Francisco). The mammals in the south-eastern Brazilian Atlantic forests of this region are currently isolated from Ama- Forest recently obtained several specimens of this zonian lowland forests by open landscapes of the new forest rat. Based on these specimens, as well as Caatinga and Cerrado biomes, but there is plausible on specimens sorted from museum and collections, we evidence that throughout the Pleistocene it was inter- performed an integrative analysis of variation mittently connected by corridors of riparian forests (Wheeler, 2004). Our comparative analyses of skins, during moist interglacial intervals (Vivo, 1997; Costa, skulls, skeletons, and fluid-preserved specimens indi- 2003). cate that the new form is a very distinctive member of The Atlantic Forest harbours an impressive diver- the tribe Oryzomyini (sensu Voss & Carleton, 1993; sity of mammals, with nearly 250–260 species Steppan, 1995; Weksler, 2006). Herein we report phy- currently recognized in approximately 110 genera logenetic analyses of morphological and molecular (Galindo-Leal & Gusmão-Câmara, 2003; Wilson & (nuclear and mitochondrial) datasets in order to Reeder, 2005). A major component (about one fifth) of establish the phylogenetic position of this new form. the mammalian diversity of Atlantic Forest is the We follow the taxonomic procedure advocated by subfamily Sigmodontinae (Muroidea : Cricetidae), Weksler, Percequillo & Voss (2006) in their new clas- with about 19 genera and 50 species (Musser & Car- sificatory arrangement of oryzomyines, recognizing leton, 2005; D’Elía et al., 2007). Our knowledge of this highly distinctive forms as new genera. We also sigmodontine diversity, however, is still poor, in con- provide morphological comparisons to closely related trast to other well-known mammalian groups, such as taxa and to sympatric taxa throughout its geographi- primates (e.g. Brachyteles, Callicebus, Cebus; Mitter- cal distribution, and discuss the biogeographical and meier et al., 1999; Silva-Junior, 2001; Roosmalen, conservation implications of our finding, providing Roosmalen & Mittermeier, 2002; Rylands, Kierulff & another piece of the complex puzzle of evolutionary Mittermeier, 2005). history of South American sigmodontines. Our incomplete scientific knowledge of Atlantic Forest diversity is exemplified by several new sigmodontines recently described or ‘rediscovered’. In the MATERIAL AND METHODS last decade, 12 sigmodontines new to science have been formally described: Abrawayaomys chebezi Pardiñas, SPECIMENS Teta & D’Elía, 2009; Akodon paranaensis Christoff The material we examined consisted of skins and et al., 2000; Akodon philipmyersi Pardiñas et al., 2005; skulls deposited in the following zoological collections: Akodon reigi González, Langguth & Oliveira, American Museum of Natural History (AMNH), New 1999; Brucepattersonius paradisus, Brucepattersonius York, USA; Fundação Universidade Regional de Blu- guarani, Brucepattersonius misionensis Mares & menau (FURB), Blumenau, Brazil; Museu Nacional Braun, 2000; Cerradomys langguthi and Cerradomys da Universidade Federal do Rio de Janeiro (MN), Rio vivoi Percequillo, Hingst-Zaher & Bonvicino, 2008; de Janeiro, Brazil; Museu de Zoologia da Univer- Hylaeamys seuanezi (Weksler, Geise & Cerqueira, sidade de São Paulo (MZUSP), São Paulo, Brazil; 1999); Juliomys rimofrons Oliveira & Bonvicino, 2002; Museum of Comparative Zoology (MCZ), Cambridge, and Juliomys ossitenuis Costa et al., 2007. In addition, USA; Museum of Vertebrate Zoology (MVZ), Berkeley, some species previously known only from the late 19th USA; National Museum of Natural History (USNM), and the early 20th centuries have recently been Washington, D.C., USA; The Field Museum (FMNH), reported again, such as Abrawayaomys ruschii (see Chicago, USA; The Natural History Museum (for- Pereira et al., 2008), Bibimys labiosus (see Paglia merly British Museum of Natural History, BMNH), et al., 1995; D’Elía, Pardiñas & Myers, 2005; Gonçalves London, England; Universidade de Brasília (UnB), et al., 2005), Blarinomys breviceps (see Silva et al., Brasília, D.F., Brazil; Universidade Federal da 2003), Phaenomys ferrugineus (see Bonvicino et al., Paraíba (UFPB), João Pessoa, Brazil; Universidade 2001), Rhagomys rufescens (see Percequillo, Gonçalves Federal de Santa Catarina (UFSC), Florianópolis, & Oliveira, 2004; Steiner-Souza et al., 2008), and Brazil. Upper case letters preceding museum Juliomys pictipes (see Pardiñas et al., 2008; de la numbers refer to sex of voucher specimens: M, male; Sancha et al., 2009). These discoveries are a direct F, female; I, sex unknown. Other abbreviations used

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 357–390 ORYZOMYINI PHYLOGENY AND BIOGEOGRAPHY 359 for examined specimens are: s, skin; sk, skull; skel, parametric (Mann-Whitney) analyses on the skull partial skeleton; car, carcass in 70% ethanol; fl, fluid measurements. Tests of goodness of fit (Yates cor- preserved specimens (ethanol 70%). A gazetteer of rected chi-square, appropriate for small samples) collecting localities is provided in Appendix 1 and were also performed in qualitative comparisons, in a list of examined specimens is presented in order to test differences between trait frequencies of Appendix 2. samples throughout the geographical range. Principal component analysis was also performed, using the covariance matrix of 14 log-transformed cranial mea- EXTERNAL AND CRANIAL MEASUREMENTS surements (we excluded the variable LN, for which We obtained the following external measurements in there are several missing values). Statistical proce- millimetres (mm) from original specimen tags: head dures are detailed in Neff & Marcus (1980) and Sokal and body length (HB), tail length (TL), ear length (E), & Rohlf (1995). hind foot length with claw (HF), and body mass (W). Cranial measurements were obtained with digital callipers to the nearest 0.01 mm. We employed the MORPHOLOGICAL CHARACTER SCORING following measurements (see Voss, 1988; Brandt & The new taxon was scored for morphological charac- Pessôa, 1994; and Musser et al., 1998 for illustra- ters described by Weksler (2006) and employed in tions): condylo-incisive length (CIL), measured from previous phylogenetic analyses of oryzomyines (Voss the greater curvature of one upper incisor to the & Weksler, 2009; Turvey et al., in press). The list of articular surface of the occipital condyle on the same morphological characters, with notes of changes in side; length of diastema (LD), from the crown of the scoring as described elsewhere (Weksler et al., 2006; first upper molar to the lesser curvature of the upper McCain, Timm & Weksler, 2007; Voss & Weksler, incisor on the same side; length of molars (LM), crown 2009), is presented in Appendix 3. The character length from molar 1 (M1) to molar 3 (M3); breadth of matrix used for the analyses is presented as Support- M1 (BM1), greatest crown breadth of the first maxil- ing Information (Table S1). The morphological char- lary molar across the paracone-protocone; length of acter matrix can also be viewed at, and downloaded incisive foramen (LIF), greatest anterior-posterior from, the Morphobank repository (http://www. dimension of one incisive foramen; breadth of incisive morphobank.org), or upon request to the authors. We foramina (BIF), greatest dimension measured across followed the terminology and definitions employed by the internal surface of both incisive foramina; breadth Musser et al. (1998) for age classes. To describe the of rostrum (BR), greatest dimension measured across qualitative character variation we used the terminol- the external border of the nasolacrimal capsules; ogy proposed by Hooper & Musser (1964), Carleton length of nasals (LN), greatest anterior-posterior (1973, 1980), Reig (1977), Voss & Linzey (1981), Voss dimension of one nasal bone; length of palatal bridge (1988), Carleton & Musser (1989), Voss (1993), Voss & (LPB), measured from the posterior border of the Carleton (1993), Steppan (1995), and Weksler (2006). incisive foramen to the anterior border of the mesopterygoid fossa; breadth of bony palate (BBP), measured across the hard palate on the lingual surface of MOLECULAR TECHNIQUES first upper molars crowns; least interorbital breadth Genomic DNA was isolated from tissue samples pre- (LIB), least distance across the frontal bones; zygo- served in ethanol using the DNeasy (Qiagen) or Pure- matic breadth (ZB), greatest dimension across the gene (Gentra) extraction kits. A fragment containing squamosal root of zygomatic arches; breadth of zygo- the full-length cytochrome b (cyt-b) gene (1143 bp) matic plate (BZP), across central area of zygomatic was amplified with the primers Mus14095 (5′-GAC plate; orbital fossa length (OFL), greatest length of ATG AAA AAT CAT CGT TGT AAT TC-3′) and the orbital fossa between the squamosal and maxil- Mus15398 (5′-GAA TAT CAG CTT TGG GTG TTG lary roots of the zygomatic arch; bular breadth (BB), RTG-3′; both from Anderson & Yates, 2000), using greatest breadth from the petrosal-basioccipital standard PCR procedures. Amplifications were per- suture to the dorsal process of the ectotympanic. formed as 20 mL reactions using Ampli-Taq Gold poly- merase Mastermix (Perkin–Elmer) and recommended concentrations of primers and templates. Reactions STATISTICAL ANALYSES were performed for 30–35 PCR cycles of denaturation In order to evaluate intrapopulational (sex) and geo- at 94 °C for 20 s, annealing at 61 °C for 15 s and graphical variation, we compared adult specimens extension at 72 °C for 60 s. After purification, PCR (age classes following Musser et al., 1998) from products were sequenced with the same primers used selected and pooled samples of the new taxon. in the PCR amplification and additional internal Univariate comparisons were performed through non- primers: L14648 (5′-TGA ATY TGA GGR GGC TTC

TCA GTA-3′; Anderson & Yates, 2000), cyt-b.LS analysis. Base frequencies were empirically estimated (5′-GTT GAA TGA ATC TGG GGC GG-3′; Irwin, from the data. Nodal bootstrap values (Felsenstein, Kocher & Wilson, 1991), MVZ16 (5′-TAGGAARTA 1985) for the likelihood analysis were calculated using TCAYTCTGGTTTRAT-3′; Smith & Patton, 1993), and 1000 pseudoreplicates under the GTRCAT model in oryzo1 (5′-GAATGYCAGCTTTGGGTGYTGGTA-3′; RAxML (Stamatakis, 2006b). new). Nucleotide sequences were determined using automated sequencers ABI 3100 or ABI 3130xl. Stop codons were eliminated for the analyses (ﬁnal RESULTS sequence length = 1140 bp). Ampliﬁcation of the Inter- SYSTEMATIC ZOOLOGY photoreceptor retinoid binding protein (Irbp) ORDER RODENTIA BOWDICH, 1821 fragment followed Weksler (2003). All resulting new FAMILY CRICETIDAE FISCHER, 1817 sequences (35 cyt-b and one Irbp) have been deposited SUBFAMILY SIGMODONTINAE WAGNER, 1843 in GenBank (accession numbers GU126515– TRIBE ORYZOMYINI VORONTSOV, 1959 GU126550) and incorporated into a data matrix con- DRYMOREOMYS GEN. NOV. (FIGS 1–6) taining previously published sequences (Bonvicino & Type species: Drymoreomys albimaculatus gen. et sp. Moreira, 2001; Weksler, 2003). nov.

PHYLOGENETIC ANALYSIS Contents: Only the type species is included. Morphological characters and DNA sequences were subjected to phylogenetic analyses using cladistic par- Etymology: From the Greek word drymus (forest), the simony (Farris, 1983; Swofford et al., 1996) and Latin oreo (mountain), and the Greek mys (mouse or maximum likelihood approaches (Felsenstein, 1981, rat), in reference to the habitat of this genus, the 2003; Swofford et al., 1996). The datasets were used lower montane humid forests of south-eastern Serra in combined and separate analyses. Parsimony analy- do Mar, in Brazil. sis was employed for the total combined super-matrix and for each individual dataset. Maximum likelihood Geographical distribution: All known specimens analyses were used for each gene individually and for referred to Drymoreomys are from the eastern slopes the combined molecular super-matrix. Characters of the Serra do Mar, in the coastal Brazilian Atlantic were equally weighted in all analyses. Irbp and cyt-b Rainforest from São Paulo to Santa Catarina states, sequence characters were always treated as unor- at altitudes ranging from 650 to 1200 m (Fig. 1). dered, but some multistate morphological characters were ordered as described in Weksler (2006). We Morphological diagnosis: Drymoreomys albimacula- employed the ‘polymorphic’ coding of Wiens (1995) for tus is characterized by the following unique combina- characters with intraspecific variation. tion of morphological traits: very long, dense and lax The heuristic search algorithm implemented by dorsal pelage; ventral patches of white on gular, tho- PAUP* 4.0b10 (Swofford, 2001) was used in all parsi- racic and inguinal fur; long unicoloured tail; dorsal mony analyses. Each heuristic search employed 1000 surface of pes with proximal brown patches; nasals replicates of random taxon addition with tree and premaxillary bones projected anteriorly forming a bisection- reconnection (TBR) branch swapping; only short tube; long and wide incisive foramina; short clades with at least one unambiguous synapomorphy palate with multiple posterolateral palatal pits were retained. Jackknife values (Farris et al., 1996) for recessed in shallow fossae; robust alisphenoid strut; the parsimony analysis were calculated using 1000 protostyle in M1 present; paracone connected by pseudoreplicates with heuristic searches employed enamel bridge to middle or to anterior portion of within each replicate (36.8% character removal per M1protocone; lower molars with anterolophid; ure- replicate; ten random addition replicates, TBR branch thral process of the glans penis with large lateral swapping, no more than 100 trees saved per replicate). lobule; and very large preputial glands. The maximum-likelihood trees were calculated using RAxML (Stamatakis, 2006a). The general time- Morphological description: Medium sized rodent, with reversible (GTR) model of nucleotide substitution moderate head and body size and body mass (Rodríguez et al., 1990), corrected for site-specific rate (Tables 1, 2); tail length longer than combined head heterogeneity using gamma distribution with four and body (about 118–132% of head and body length); classes (Yang, 1994) was used in all analyses. Gene- pinnae small (about 13–16% of head and body length); specific unlinked models were employed in the analysis pes short (about 19–24% of head and body length). of combined Irbp–cyt-b datasets; only taxa with com- Dorsal pelage very long, extremely dense and lax, plete sequences for both genes were included in this consisting of long and dense underfur (wool hairs;

Figure 1. Known collection localities of Drymoreomys albimaculatus gen. et sp. nov. in south-eastern Brazil; the open circle indicates the type locality of this species. Inset: South America. See Gazetteer (Appendix 1), where numbers are associated with collection localities. thin, wavy, and short) and longer and lax overfur tively lighter than dorsal pelage. Flanks dull reddish- (cover and guard hairs; thick and long). Dorsal body brown; banded cover hairs and dark guard hairs rare. colour dull orange to fulvous buff weakly grizzled with Pinnae rounded and small, reaching the posterior reddish-brown; wool hairs (range: 12–14 mm) with margin of eye when laid forward; pinnae covered basal part greyish and distal part (1/10 of total internally with short golden hairs and externally length) orange or brown; cover hairs long (range: densely covered with reddish-brown hairs. Mystacial 14–17 mm), with distal quarter dark brown with a vibrissae usually extending posteriorly for few milli- subterminal orange band; guard hairs sparse and metres beyond the caudal margins of the pinnae when long (range: 17–21 mm), with distal half entirely laid back; superciliary vibrissae short, not extending reddish to dark brown. Ventral pelage composed by posteriorly beyond pinnae. Dorsal surface of manus wool, cover, and guard hairs; individual hairs greyish- covered by brown hairs, digits covered with white/ based and tipped with white, except in gular, thoracic silvery hairs; manus with short white ungual tufts on (in all examined specimens), and inguinal (only 15.4% dII–dV (d = digit). Pes short and moderately wide of examined specimens; six out of 39 specimens) with conspicuous tufts of long ungual white to silvery regions, which exhibit entirely white hairs; general hairs at bases of claws on dII–dV and short ungual ventral colour greyish, with distinctive white patches hairs on dI; plantar pads very large and ﬂeshy, (Fig. 2) in gular, thoracic, and inguinal regions (the interdigital pads set close together; plantar surface inguinal patch of white fur is variably present or amongst pads covered with plantar squamae, ﬂesh absent); ventral pelage abruptly paler and distinc- coloured; hypothenar pad large and distinct; claw of

Skull (Fig. 3) with long, tapering rostrum; nasals and premaxillae produced anteriorly, forming short bony rostral tube; rostrum flanked by shallow zygomatic notches; interorbital region long and narrow, anteriorly convergent, with squared to lightly beaded supraorbital margins; braincase oblong, without or with weakly developed temporal crests; interparietal wedge-shaped, not in contact with squamosal; lambdoidal and nuchal crests weakly developed in adults. Nasals and premaxillaries projected anteriorly beyond incisors, forming a short tube (similar to Handleyomys); nasals extending posteriorly beyond lacrimal bones (in 16 out of 19 specimens examined); lacrimals equally sutured to maxillaries and frontals. Zygomatic plate (in lateral view) not projected forward, without dorsal free margin and anterior margin straight or slightly concave, and zygomatic spine absent; posterior margin of zygomatic plate anterior to M1 alveolus; jugal present and large, maxillary and squamosal not overlapping in zygoma. Frontosquamosal suture colinear with frontoparietal suture. Parietals with broad lateral expansions on braincase. Incisive foramina long (averaging about 71% of length of diastema) and wider posteriorly, sometimes extending to the alveolus or anterocones of M1 [reaching the anterocones in five out of 19 (26%) adult examined specimens]; lateral margins abruptly constricted anteriorly near the premaxillary–maxillary suture [in nine out of 19 (47%) adult specimens] or sharply and abruptly constricted posteriorly, near the posterior border (in nearly 10% of adult specimens; Fig. 4). Palate short and wide (sensu Hershkovitz, 1962; Fig. 5); posterolateral palatal pits small to moderately large, single to multiple and recessed in shallow fossae; palatal excrescencies absent; mesopterygoid fossa wider to or equal to parapterygoid fossae; parapterygoid fossae perforated by several nutritive foramina; piriform fenestra (= middle lacerate foramen) narrow. Mesop- terygoid fossa extending anteriorly to or between left and right M3, reaching the hypocone (Fig. 5); bony Figure 2. Ventral view of the dried skin of the holotype of roof of mesopterygoid fossa completely ossified or per- Drymoreomys albimaculatus gen. et sp. nov. MZUSP forated by small sphenopalatine vacuities restricted 34716 from Parque Estadual Intervales, São Paulo, show- to presphenoid (only marginally in basisphenoid). ing the gular and pectoral patch of entirely white hairs. Alisphenoid strut present [in all adult specimens (N = 19) examined for this trait; only one out of 35 dI extending to or just beyond middle of phalange 1 of specimens do not exhibit the strut (2.8%), a young dII; claw of dV extending beyond the first interpha- specimen from E. B. Boracéia, São Paulo], a robust langeal joint of dIV (reaching the middle of phalange bony bar separating buccinators–masticatory 2 of dIV); dorsal (volar) surface of pes densely covered foramen and accessory oval foramen. Stapedial with brown hairs and white/silvery hairs: brown hairs foramen, squamoso-alisphenoid groove and spheno- grouped in dark proximal patches of variable length frontal foramen absent; posterior opening of alisphe- and width, white hairs distributed along the distal noid canal large and conspicuous, but without portion of pes and digits. Tail unicoloured; tail scales posterior groove or depression; secondary anastomo- very reduced; tail densely covered with short and stiff sis of internal carotid artery crosses dorsal surface of brown hairs on dorsal and ventral surface. parapterygoid plate (= carotid circulatory pattern 3 of

Figure 3. Cranium (dorsal, ventral, and lateral views) and mandible (lateral view) of the holotype of Drymoreomys albimaculatus gen. et sp. nov. MZUSP 34716, from Parque Estadual Intervales, São Paulo (condylo-incisive length 30.67 mm).

Voss, 1988). Postglenoid foramen large and rounded; periotic exposed posteromedially between ectotym- subsquamosal fenestra large and patent. Ectotym- panic and basioccipital but usually not extending panic bullae globose; Eustachian tube short; stape- anteriorly to carotid canal; mastoid perforated by dial process long and narrow, overlapped to lateral conspicuous posterodorsal fenestra. Mandible long margin of squamosal; tegmen tympani variably over- and shallow (Fig. 3); coronoid process large, falciform lapping squamosal; posterior suspensory process of or triangular, nearly equal in height to condyloid squamosal absent; bony projection dorsolateral to process; superior notch shallow; angular process stapedial process present, overlapped to squamosal; short, not surpassing the condyloid process posteri-

Figure 4. Detail of the ventral view of the cranium of Drymoreomys albimaculatus gen. et sp. nov., showing the incisive foramina with lateral margins abruptly constricted anteriorly near the premaxillary-maxillary suture [left specimen, MZUSP BO 42, from Estação Biológica de Boracéia, São Paulo; length of incisive foramen (LIF): 5.71 mm] and with abruptly constricted lateral margins, near the posterior border (right specimen, MZUSP BO 41, also from E. B. Boracéia; LIF: 5.74 mm).

Figure 5. Detail of the ventral view of the cranium of Drymoreomys albimaculatus gen. et sp. nov., showing the palate, the anterior margin of mesopterygoid fossa, and the sphenopalatine vacuities of the same specimens depicted in previous ﬁgure [MZUSP BO 42, length of palatal bridge (LPB): 5.03 mm; MZUSP BO 41, LPB: 5.34 mm]. orly; inferior notch shallow; capsular process of lower Upper incisors opisthodont, with smoothly rounded incisor alveolus not noticeable; superior and inferior enamel band; enamel band orange to yellowish in masseteric ridges weak, converging anteriorly as an colour. Maxillary tooth-rows subparallel or weakly open chevron or conjoined as a single, weak crest. convergent anteriorly (Figs 3, 5). Labial and lingual

Figure 6. Molar series in occlusal view of Drymoreomys albimaculatus gen. et sp. nov.: Left pair: upper (left) and lower (right) molars of the holotype, MZUSP 34716 [length of molars (LM): 5.25 mm, breadth of M1 (BM1): 1.49 mm]; Right pair: upper (left) molar series of the paratype, MZUSP BO 43 (LM: 4.90 mm, BM1: 1.35 mm), from Estação Biológica de Boracéia, São Paulo, and lower (right) molar series of the paratype, MZUSP AB 422 (LM: 4.97 mm, BM1: 1.39 mm), from Reserva do Morro Grande, São Paulo.

flexi of upper molars shallowly penetrating at molar or three (labial, medial, and lingual) fossettes; mesol- midline (Fig. 6). Labial and lingual cusps arranged in oph well developed, long, connected to distinct opposite pairs. Labial and lingual cusps high (molar mesostyle. Third upper molar (M3) with mesoloph, nearly hypsodont) and compressed anteroposteriorly; posteroloph, and persistent hypoflexus; paracone labial cusps notably distinct on molar topography. and protocone distinguishable on molar surface, Occlusal surfaces of labial cusps of upper molars hypocone reduced and metacone greatly reduced orientated posteriorly; occlusal surface of lingual and completely fused with posteroloph. Labial cusps labially orientated. First upper molar (M1) accessory root of M1 possibly absent (not visible in anterocone divided into labial and lingual conules lateral view). (anteromedian flexus present); anteroloph well devel- Mandibullary toothrows with labial cusps slightly oped and fused with anterostyle on labial cingulum, anterior to lingual cusps; occlusal surface of lingual separated from anterocone by persistent anteroflexus; cusps orientated anteriorly and occlusal surface of protostyle present (in most specimens) as an isolated labial cusps lingually orientated. In lingual view, the accessory cuspule or fused to anterior mure; paracone cusps are orientated anteriorly, whereas in labial connected by enamel bridge to middle or to anterior view the cusps are orientated dorsally. First lower portion of protocone; mesoloph well developed, long, molar (m1) anteroconid divided by an anteromedian connected to distinct mesostyle on labial margin of flexid; anterolabial cingulum developed on m1 and molar. Second upper molar (M2) protoflexus variably m2, and variably present on m3; anterolophid present present; mesoflexus long and obliquely or transver- on all lower molars; mesolophid present on m1, m2, sally orientated, divided into two (labial and lingual) and usually on m3; ectolophid variably present on m1

Table 1. Descriptive statistics of external and craniodental measurements (in mm) and weight (in g) of adult specimens of Drymoreomys albimaculatus gen. et sp. nov. from four geographical samples of São Paulo, eastern Brazil

01TeLnenSceyo London, of Society Linnean The 2011 © Ribeirão Reserva Morro Parque Estadual Intervales Grande Grande E. B. Boracéia

MZUSP 34716 F, MAM MVZ Sample

adult Holotype 15 F 182089 F mean RG 47 M AB 397, AB 423 I BO 24, BO 41 I AL ET

HB 149 135 125 136.3 ± 2.1 103 (109–143) 2 – . TL 176 170 165 170.3 ± 5.5 113 (150–162) 2 – HF 28 30 30 29.3 ± 1.2 23 (18.5–19) 2 – E 20 20 20 20 18 (27.5–29) 2 – W 57 58 50 55.0 ± 4.4 21 (52–102) 2 – CIL 30.67 30.79 30.53 30.7 ± 0.1 24.94 (28.22–29.92) 2 (28.26–29.93) 2 LD 8.56 8.37 8.13 8.4 ± 0.2 6.87 (7.99–8.24) 2 (7.88–7.98) 2 LM 5.25 5.43 5.01 5.2 ± 0.2 5.03 (5.00–5.15) 2 (5.02–5.07) 2

olgclJunlo h ina Society Linnean the of Journal Zoological BM1 1.49 1.48 1.44 1.47 ± 0.03 1.37 (1.38–1.39) 2 (1.42–1.44) 2 LIF 6.33 6.37 5.82 6.2 ± 0.3 5.16 (5.59–5.99) 2 (5.74–5.78) 2 BIF 2.82 2.85 2.65 2.77 ± 0.11 2.3 (2.55–3.03) 2 (2.79–2.96) 2 BR 5.99 5.95 5.31 5.8 ± 0.4 4.77 (4.82–5.73) 2 (5.33–5.57) 2 LN 12.37 12.26 12.52 12.4 ± 0.1 10.44 (11.57–12.06) 2 – LPB 5.33 5.38 5.59 5.4 ± 0.1 4.7 (5.37–5.77) 2 (5.07–5.34) 2 BBP 3.07 2.83 2.94 2.95 ± 0.12 2.41 (2.67–2.75) 2 (2.95–2.96) 2 LIB 5.69 5.64 5.33 5.6 ± 0.2 5.4 (5.01–5.57) 2 (5.32–5.52) 2 ZB 17.84 16.66 17.08 17.2 ± 0.6 14.39 (15.45–17.6) 2 – BZP 2.65 2.43 2.65 2.6 ± 0.1 1.9 (2.46–2.55) 2 (2.15–2.47) 2 OFL 11.37 11.24 11.32 11.3 ± 0.07 9.96 (10.69–11.25) 2 (10.6–11.66) 2 BB 4.87 5.06 5.17 5.0 ± 0.2 4.66 (4.97–4.99) 2 (4.68–4.78) 2

Mean ± standard deviation (minimum–maximum), N. F, female; I, sex unknown; M, male; HB, head and body length; TL, tail length; HF, hind foot length with claw; E, ear length; W, body mass; CIL, condylo-incisive 2011, , length; LD, length of diastema; LM, length of molars; BM1, breadth of M1; LIF, length of incisive foramen; BIF, breadth of incisive foramina; BR, breadth of rostrum; LN, length of nasals; LPB, length of palatal bridge; BBP, breadth of bony palate; LIB, least interorbital breadth; ZB, zygomatic breadth; BZP, breadth

161 of zygomatic plate; OFL, orbital fossa length; BB, bular breadth. 357–390 , ORYZOMYINI PHYLOGENY AND BIOGEOGRAPHY 367

Table 2. Descriptive statistics of external and cranioden- immediately posterior to articular facet; trochlear tal measurements (in mm) and weight (in g) of Drymore- process long and shelf-like. omys albimaculatus gen.etsp. nov. from two Stomach unilocular and hemiglandular, with geographical samples of Santa Catarina, southern Brazil gastric glandular epithelium limited to antrum. Glans penis without lateral bacular mounds; distal cartilagi- Parque nous apparatus tridigitate, with the central digit Estadual more robust than lateral ones; dorsal papilla with one Serra do Parque Natural Municipal apical spine; urethral process with large lateral Tabuleiro Nascentes do Garcia lobule. Preputial glands very large.

UFSC 860 I, Comparisons: Drymoreomys has 12 putative mor- sub-adult Adults* phological autapomorphies as recovered in our HB 116 131.45 ± 5.01 (122–139) 11 phylogenetic analysis (below). In particular, some TL 158 160.30 ± 11.05 (140–175) 10 morphological traits displayed by Drymoreomys are HF 28 28.55 ± 1.67 (25.8–30.5) 11 rarely seen in oryzomyines, such as very large inter- E 19.5 19.36 ± 1.94 (16–22) 11 digital plantar pads (only observed in Oecomys and W 55.55 ± 6.68 (44–64) 11 Megalomys amongst other oryzomyines); short rostral CIL 27.09 30.23 ± 1.14 (28.25–32.37) 11 tube; posterior hard-palate border penetrating ante- LD 7.35 8.23± 0.37 (7.51–8.88) 11 riorly between molars (seen only in Nephelomys LM 5.34 5.16 ± 0.11 (4.93–5.32) 11 levipes;inEremoryzomys polius the mesopterygoid BM1 1.5 1.45 ± 0.04 (1.4–1.53) 11 fossa reaches the posterior margin of M3, but does not LIF 5.53 5.87 ± 0.37 (5.48–6.59) 11 penetrate between the molar rows); maxillary tooth- BIF 2.38 2.80 ± 0.18 (2.59–3.22) 11 rows weakly convergent anteriorly (only Lundomys BR 4.9 5.47 ± 0.31 (4.95–5.98) 11 and Holochilus possess nonparallel tooth-rows); and LN 11.46 12.20 ± 1.40 (11.25–13.51) 5 dorsal papilla in glans penis with an apical spine (also LPB 5.02 5.52 ± 0.28 (5.03–5.88) 11 observed in Sigmodontomys alfari; Hooper & Musser, BBP 2.61 2.71 ± 0.22 (2.35–3.04) 11 1964). Finally, some traits of this new taxon are LIB 5.35 5.44 ± 0.21 (5.09–5.68) 11 unique amongst oryzomyines, such as: the dorsal ZB 16.14 17.02 ± 0.69 (16.19–17.99) 11 surface of pes with dark patches of brown hairs; BZP 2.38 2.48 ± 0.18 (2.11–2.73) 11 all-white ventral patches; reduced lateral bacular OFL 10.61 11.23 ± 0.31 (10.77–11.63) 11 mounds; urethral process of the glans penis with BB 5.29 4.94 ± 0.15 (4.61–5.2) 11 large lateral lobule; and very large preputial glands. Drymoreomys is recovered as the sister group of the *Included specimens are: FURB 6267, 9621, 9664, 9756, Andean genus Eremoryzomys within oryzomyine 9831, 9833, 9838, 9862, 9902, 9903, 12044. Mean ± standard deviation (minimum–maximum), N. clade D in the phylogenetic analysis (see below). Each F, female; I, unknown sex; M, male; HB, head and body genus, however, is characterized by strikingly differ- length; TL, tail length; HF, hind foot length with claw; E, ent anatomical traits. In addition to the traits ear length; W, body mass; CIL, condylo-incisive length; described above, the dorsal pelage of Drymoreomys is LD, length of diastema; LM, length of molars; BM1, reddish-brown whereas it is greyish in Eremory- breadth of M1; LIF, length of incisive foramen; BIF, zomys; the tail is unicoloured in Drymoreomys but breadth of incisive foramina; BR, breadth of rostrum; LN, bicoloured in Eremoryzomys. The skull of Drymore- length of nasals; LPB, length of palatal bridge; BBP, omys exhibits the interorbital region with weakly breadth of bony palate; LIB, least interorbital breadth; ZB, beaded supraorbital margins (Eremoryzomys exhibits zygomatic breadth; BZP, breadth of zygomatic plate; OFL, well-developed supraorbital crests); posterolateral orbital fossa length; BB, bular breadth. palatal pits recessed in shallow depressions (the pits are conspicuous and always positioned in deeply recessed fossa in E. polius); mesopterygoid fossa com- only; hypoﬂexid deep on all lower molars; posterof- pletely ossiﬁed or perforated by small sphenopalato- lexid on m3 large and persistent. All lower molars ine vacuities (the vacuities are large in with two roots at anterior and posterior positions. Eremoryzomys). Drymoreomys is also clearly distinct Twelve ribs present. Fifth lumbar (17th thoraci- in external and cranial features from other genera columbar) vertebra with or without well-developed within clade D; Table 4 summarizes the morphologi- anapophysis. Thoracicolumbar vertebrae number 19; cal variation amongst some genera that are included sacrals four; caudals 36–38; haemal arch between in this clade. second and third caudal vertebrae with posterior Two other sigmodontine genera resemble Dry- spinous process. Trochlear process of calcaneum moreomys in external characters, Rhipidomys and

Oecomys, and we provide morphological comparisons DRYMOREOMYS ALBIMACULATUS GEN. with sympatric forms of these taxa to avoid misi- ET SP. NOV.(FIGS 1–6) dentifications. Drymoreomys and Oecomys possess Holotype: MZUSP 34716, an adult female collected by very long and dense dorsal reddish brown pelage; Meika A. Mustrangi (original field number MAM 8; long mystacial vibrissae; short ears; tail longer than previous collection number MVZ 182088), 21.vii.1992. head and body; short hind foot; very large and The holotype consists of an undamaged skin, skull, fleshy interdigital pads often in contact. However, and postcranial partial skeleton. A liver tissue sample there are several anatomical traits that discriminate is preserved in ethanol in the Museum of Vertebrate Drymoreomys and Oecomys, such as the plantar Zoology tissue collection, under original field number surface of pes covered with squamae (the sole is MAM 8. Irbp and cyt-b sequence data are available in smooth in Oecomys); dorsal surface of pes with dark GenBank under the accession numbers GU126515 patches of brown hairs (pes completely white in and GU126516, respectively. Oecomys); ventral pelage with gular, thoracic, and, External and selected skull dimensions (in mm) of occasionally, inguinal patches of self-whitish hairs holotype are as follows: HB = 149, LT = 176, HF = 28, (venter without patches in Oecomys); short rostral Ear = 20, Wt = 57, CIL = 30.67, LD = 8.56, LM = 5.25, tube (absent in species of Oecomys); interorbital BM1 = 1.49, LIF = 6.33, BIF = 2.82, BR = 5.99, region with weakly beaded supraorbital margins LN = 12.37, LPB = 5.33, BBP = 3.07, LIB = 17.84, (Oecomys exhibits well-developed supraorbital ZB = 5.69, BZP = 2.65, OFL = 11.37, BB = 4.87. crests); shorter palate, with small to large multiple posterolateral palatal pits recessed in shallow fossae Paratypes: We assign all specimens herein studied (Oecomys presents longer palate, with multiple large (see Specimens examined below) as paratypes of D. posterolateral palatal pits recessed in deep fossae); albimaculatus. stapedial foramen, squamoso-alisphenoid groove and sphenofrontal foramen absent, posterior opening of Type locality: Brazil, Estado de São Paulo, Município alisphenoid canal large and conspicuous, but de Ribeirão Grande, Parque Estadual Intervales, base without posterior groove or depression, and second- do Carmo, 700 m; 24°20′S, 48°25′W (collecting field ary anastomosis of internal carotid artery crosses coordinates given by the collector). Originally known dorsal surface of parapterygoid plate (pattern 3 of as Fazenda Intervales, the Parque Estadual Inter- Voss, 1988; most species of genus Oecomys exhibit vales is situated between the valleys of Rio Paranapa- pattern 1, except Oecomys mamorae and Oecomys nema (a tributary of Rio Paraná) and Rio Ribeira de concolor that also exhibit pattern 3; Oecomys cathe- Iguape (an important Atlantic Forest river drainage rinae, a sympatric form to the new genus and that flows directly to Atlantic Ocean), on the slopes of species described here shows pattern 1); presence of Serra de Paranapiacaba. anteromedial flexus in M1; anterolophid present on m2 and m3; urethral process with large lateral lobule; and apex of dorsal papilla with single Distribution: As for the genus, i.e. known currently spine. from a few localities in the eastern Slopes of the Serra The genus Rhipidomys, an arboreal thomasomy- do Mar Range in São Paulo and Santa Catarina, ine, also superficially resembles Drymoreomys in Brazil (Fig. 1). There is a gap in the distribution of some morphological traits, especially in respect to collecting localities of D. albimaculatus on Paraná the dark patches of brown hairs in the dorsal state and we interpret this as a sampling artefact surface of pes; shallow zygomatic notch; interorbital rather than actual evidence of disjunct populational region without dorsolateral beads or crests; short distribution. palate; and carotid circulatory pattern (type 3 of Voss, 1988). However, Drymoreomys displays Etymology: From the Latin albus (white) and the several character discordances such as the Latin maculatus (spot, stain), in reference to the mystacial vibrissae, which in Rhipidomys patches of entirely white fur on the gular, thoracic, are longer, thicker, and denser than those and inguinal regions. observed in Drymoreomys. Additionally, all specimens of Drymoreomys possess gular to pectoral Morphological description and diagnosis: Same as for patches of white hair, which are absent in Rhipi- the genus. domys. Finally, one oryzomyine cranial synapomorphy is enough to discriminate these two genera, Comments: The first three known specimens of Dry- namely, the absence of the posterior suspensory moreomys albimaculatus were originally obtained by process of squamosal connected to the tegmen Dr Meika Mustrangi during the austral winter of tympani. 1992 at Parque Estadual Intervales, São Paulo, and

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 357–390 ORYZOMYINI PHYLOGENY AND BIOGEOGRAPHY 369 were housed at the Museu de Zoologia da Univer- (Fig. 1), and thus were grouped in order to increase sidade de São Paulo and the Museum of Vertebrate sample sizes for statistical comparisons. We believe Zoology. Another specimen was trapped by Drs Julio that the gap in the species distribution is just a Voltolini and Jorge Cherem at the Parque Estadual sampling artefact and that forthcoming sampling da Serra do Tabuleiro, in Santa Catarina in the same efforts in Paraná state will provide a better notion of year as Mustrangi’s specimens and deposited at the the distribution and geographical variation of this Universidade Federal de Santa Catarina. More species. recently, independent inventories throughout the Although available samples are small, no morpho- Atlantic Forest in the states of São Paulo (Pardini & logical variation, either qualitative or quantitative Umetsu, 2006; Bueno, 2008; and also unpublished (Tables 1–3), could be confidently assigned to sexual data and vouchers available at Museu de Zoologia da dimorphism in D. albimaculatus, a pattern also Universidade de São Paulo) and Santa Catarina observed in other studies of sexual variation in ory- (unpublished data and vouchers available at the zomyines and sigmodontines (Goldman, 1918; Musser Fundação Universidade Regional de Blumenau, & Williams, 1985; Voss, 1988; Carleton & Musser, Santa Catarina), sampled several other specimens 1989; Voss & Marcus, 1992). Correspondently, Mann– that could be confidently assigned to D. albimacula- Whitney tests performed on the sample from tus. All specimens remained unstudied in museum Nascentes do Garcia (our largest sample, N = 11 adult drawers and the ecological data obtained from those specimens, with three males and eight females) specimens were not published, pending a formal revealed that there are no significant differences description for both the genus and species. between the sexes. The most noticeable age differences are observed Specimens examined: BRAZIL:SÃO PAULO: Cotia, in the texture and colour of dorsal fur, which in Reserva do Morro Grande: F: MZUSP BS 1441 (s, sk), young individuals is shorter, less dense, and pre- AB 397, 398, 422, 423, 698 (sk, fl). Bananal, Estação dominantly greyish brown. In addition, the gular Ecológica de Bananal: F: MZUSP 33782 (s, sk, car) and thoracic patches in the ventral region are Ribeirão Grande, Mina Limeira: M: MZUSP RG 47; F: smaller and narrower in young specimens of all MZUSP RG 48 (sk, fl). Ribeirão Grande, Fazenda samples. In the skull, differences in the configura- Intervales, Carmo: F: MVZ 182089, MZUSP 34716 tion of the posterior border of the hard palate can (holotype of D. albimaculatus), MZUSP MAM 15 (s, be attributed to age differences: in very young speci- sk, skel). Salesópolis, Estação Biológica de Boracéia: mens (i.e. specimens with M3 partially erupted or M: MZUSP BO 41, 42, 44, plus three specimens just erupted), the anterior margin of the mesoptery- without field number; F: MZUSP BO 24, 43, plus two goid fossa penetrates between molar tooth-rows, specimens without field number (sk, fl). SANTA CATA- reaching the protocone of M3 (Boracéia, MZUSP BO RINA: Parque Estadual da Serra do Tabuleiro: UFSC 44; Ribeirão Grande, MZUSP RG 48); in young 860 (s, sk). Blumenau, Parque Natural Municipal specimens the anterior margin reaches the hypocone Nascentes do Garcia: M: FURB 9621, 9664, 9756, or the hypoflexus of M3 (Morro Grande, MZUSP AB 9787, 9833, 9838, 9862, 9871, 9902, 12044 (s, sk); F: 698, BS 1441; Nascentes do Garcia, FURB 9962); FURB 9792, 9794, 9831, 9869, 9903 (s, sk); U: FURB and in subadult and adult specimens the fossa pen- 9666, 9743, 9962 (s, sk). Blumenau, Parque Natural etrates to the level of M3 hypocone or to the level of Municipal Nascentes do Garcia, Terceira Vargem do M3 alveolus (Boracéia, MZUSP BO 24, 41; Morro Ribeirão Garcia, Vale do Espingarda: F: FURB 6267 Grande, MZUSP AB 397, 423); there is no specimen (s, sk). with a long palate amongst the studied exemplars. Ontogenetic differentiation is also observed in quantitative traits (Tables 1 and 2), with adults exhibit- PHENOTYPIC VARIATION: ONTOGENY, SEX, ing larger absolute and mean values than subadults AND GEOGRAPHY in most cranial variables. Individuals of D. albimaculatus exhibit small Some integumental and cranial traits vary amongst amounts of variation, both within and amongst popu- the geographical samples. All adult specimens lations, in integumental, cranial, dental, and morpho- present a very dense, long, soft, and lax dorsal fur; in metric traits. Intrapopulation variation is described samples from São Paulo and Serra do Tabuleiro, the below in terms of age and sex. Quantitative geo- wool hairs range from 12 to 14 mm, the cover hairs graphical variation was analysed comparing two from 14 to 17 mm, and the guard hairs from 20 to groups composed of São Paulo (Intervales, Boracéia, 21 mm, whereas the specimen from Nascentes do Ribeirão Grande, and Morro Grande) and Santa Cata- Garcia exhibits shorter hairs, with wool hairs varying rina (Tabuleiro and Nascentes do Garcia) populations. from 13 to 14 mm, cover hairs from 14 to 15 mm, and Localities in each set are closely located to each other guard hairs that range from 17 to 18 mm. The col-

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 357–390 370 Table 3. Morphological comparisons amongst genera Drymoreomys and Eremoryzomys, and other selected genus group taxa of Oryzomyini clade D (Weksler, 2006) from eastern South America .R PERCEQUILLO R. A. Characteristic Drymoreomys Eremoryzomys* Cerradomys* Nectomys* Sooretamys*

Dorsal pelage Reddish-brown Greyish to yellowish/ Reddish or Brownish Greyish to brownish yellowish-brown yellowish-brown Ventral pelage Greyish Whitish Greyish to buff Buff Greyish to buff

01TeLnenSceyo London, of Society Linnean The 2011 © White ventral patches Present Absent Absent Absent Absent Dorsal surface of pes Present Absent Absent Absent Absent (some specimens with dark patches exhibit darker hairs, not forming a distinct patch)

Hind feet Without webs, with Without webs, with Without webs, with Webbed, with long claws, Without webs, with AL ET medium claws, with medium claws, with medium claws, with with very short ungual medium claws, with long ungual tufts long ungual tufts shorter ungual tufts tufts medium ungual tufts Plantar pads Very large and fleshy Large and fleshy Large and fleshy Small Large and fleshy . Tail colour Not bicoloured Bicoloured Variably bicoloured Not bicoloured Not bicoloured Mystacial vibrissae Long Medium Medium Short Medium Rostrum Long, with short rostral Short, without short Short, without short Short, without short Short, without short tube rostral tube rostral tube rostral tube rostral tube Zygomatic notch Shallow and narrow Deep and wide Deep and wide Deeper and wider Deep and wide Interorbital region Anteriorly convergent, Anteriorly convergent, Anteriorly convergent, Anteriorly convergent, Hourglass shaped, with with squared to lightly with beaded with highly developed with highly beaded squared supraorbital

olgclJunlo h ina Society Linnean the of Journal Zoological beaded supraorbital supraorbital margins supraorbital margins, supraorbital margins margins margins forming crests Incisive foramen Long and wide posteriorly, Very long and wide Long and wide medially, Short and wide Long and wide medially, reaching or not M1 medially, reaching M1 reaching or not M1 posteriorly, never reaching or not M1 paracone reaching M1 Posterolateral palatal pits Small to moderately large, Large and complex, Large and complex, Large and complex, Large and complex, single to multiple and recessed in deep fossa recessed in deep fossa recessed in deep fossa recessed in deep fossa recessed in very shallow fossa Mesopterygoid fossa Extending anteriorly, Extending anteriorly, Not reaching the M3 Not reaching the M3 Not reaching the M3 penetrating between M3 reaching the posterior margin of M3 Bony roof of Completely ossiﬁed or Perforated by large Completely ossiﬁed or Perforated by large Perforated by large mesopterygoid fossa perforated by small sphenopalatine vacuities perforated by small to sphenopalatine vacuities sphenopalatine vacuities sphenopalatine vacuities large sphenopalatine restricted to vacuities

2011, , presphenoid Alisphenoid strut Present Usually present Absent Absent Absent Maxillary tooth-rows Weakly convergent Parallel Parallel Parallel Parallel 161 anteriorly

357–390 , First upper molar (M1) Anteromedian flexus Anteromedian flexus Anteromedian flexus Anteromedian flexus Anteromedian flexus present absent absent absent absent

*See list of examined specimens in Appendix 2. ORYZOMYINI PHYLOGENY AND BIOGEOGRAPHY 371 oration ranges from orange to fulvous buff weakly possess very small ectostylids), whereas almost all grizzled with reddish-brown colour (in most speci- specimens from Santa Catarina have well-developed mens) to ochraceous brown weakly grizzled with ectolophids (ten out of 11 specimens; Yates X2 = 3.89; brown in a few specimens from Serra do Tabuleiro P = 0.049), Regarding the anterior length of the and Nascentes do Garcia (UFSC 860, FURB 9862, mesopterygoid fossa, nine out of 11 specimens from 9871, 9903). All studied specimens present patches of Santa Catarina have the mesopterygoid fossa reach- white fur on gular and thoracic position on the ing the hypocone of M3, whereas only two out of eight ventral region; presence of inguinal patches, however, specimens from São Paulo have this condition (Yates is variable: inguinal patches were observed in 20% of X2 = 4.02; P = 0.045). specimens (four out of 20 individuals) from the São Comparisons between pooled samples of São Paulo Paulo sample and in nearly 11% of specimens (two out and Santa Catarina revealed that adults are similar of 19 individuals) from Santa Catarina; based on the in cranial measurements throughout their distribu- results of the Yates corrected chi-square test (Yates tion (all means are statistically similar), and the X2 = 0.67; P = 0.41), we accept the null hypothesis descriptive statistics for the six populations studied that the frequencies between the two samples are (Tables 1, 2) also demonstrate this homogeneity in similar. size. The first and the second principal components, Considering the skull, there are few informative extracted from the nonsingular covariance matrix, traits varying in frequency amongst geographical are responsible for 61.7% of the total variance, and samples. The incisive foramina are slightly or the variance along the first component is influenced abruptly constricted anteriorly in a few adult speci- by variables such as breadth of incisive foramina, mens from São Paulo (38%; three out of eight indi- breadth of bony palate, breadth of rostrum, and zygo- viduals) and more commonly observed in specimens matic breadth; breadth of incisive foramina, breadth from Santa Catarina (54%; six out of 11 specimens); of zygomatic plate and breadth of bony palate are the difference in frequency, however, is not statisti- more associated to the second component (Table 4). cally significant (Yates X2 = 0.07; P = 0.79). One speci- The loadings of the first principal component eigen- men from São Paulo (MZUSP BO 41) and one from vectors are all negative, indicating a size factor. Plots Santa Catarina (FURB 9838) exhibit an abrupt con- of principal component scores (not shown) revealed no striction near the posterior margin of the incisive congruent pattern of variation related to sex, age, or foramina. The posterior margins of incisive foramina geography. Considering the limited number of avail- project between first molars in 50% of adults from São able samples and specimens and the lack of sharp Paulo (Fig. 4; four out of eight individuals), reaching qualitative and quantitative discontinuities through- either the alveolus of M1 or the anterocone of M1. out the range of D. albimaculatus, we adopt a con- This frequency is considerably larger when compared servative position and assume that the observed to that observed in the Santa Catarina exemplars geographical variation does not merit taxonomic (9%; one out of 11 specimens), but the difference again recognition. is not statistically different (Yates X2 = 2.17; P = 0.14). The presence of narrow and small sphenopalatine vacuities usually restricted to the presphenoid also PHYLOGENETIC ANALYSES presents discrete variation throughout the geographi- The concatenated matrix of morphological (charac- cal range, with 63% of specimens from São Paulo ters presented in Appendix 3) and molecular data showing this condition (five out of eight individuals; provided 766 informative characters (morphology: 88 in one specimen only we observed vacuities extending characters; cyt-b: 473; Irbp: 205). Parsimony analy- through the basisphenoid) and 73% of specimens from sis of this super-matrix resulted in two trees [5513 Santa Catarina (eight out of 11 specimens, with one steps, consistency index (CI) = 0.23, retention index specimen presenting long vacuities reaching the (RI) = 0.41] that differ only with respect to relation- basisphenoid). The statistical analysis suggests that ships within the genus Oecomys. The strict consen- the frequencies of specimens presenting vacuities sus tree (Fig. 7) has the same basal structure as the from São Paulo and Santa Catarina, although differ- trees recovered in previous analyses of morphology ent, are not statistically significant (Yates X2 = 0.00; and Irbp (Weksler, 2003, 2006), with oryzomyines P = 0.98). Only two traits showed significant results divided into four clades (labelled A to D in Fig. 7). in the Yates tests, albeit barely: the presence of ectol- Although relationships within all major clades differ ophid in lower first molar and the anterior length of from those recovered by previous analyses, most of the mesopterygoid fossa. Only three specimens from the novel patterns of intergeneric relationships have São Paulo (N = 8) possess the ectolophid (all speci- low nodal support. Exceptions are the moderate mens from Intervales; the few adult specimens from (jackknife = 61%) support for the inclusion of Mind- Morro Grande, Ribeirão Grande, and Boracéia omys hammondi within clade B, and the very high

Table 4. Results of principal component analysis of adult placed within the oryzomyines, Neacomys is recovered specimens of Drymoreomys albimaculatus gen. et sp. as the most basal member of the tribe, and none of nov. from São Paulo and Santa Catarina from 14 cranio- the major oryzomyine clades (A–D) are recovered. dental variables Nodal support values, however, are very low overall: only three intergeneric relationships had jack- Eigenvectors knife values above 50% (Aegialomys + Nesoryzomys, Microryzomys + Oreoryzomys,andSigmodontomys + First Second Melanomys). Drymoreomys is recovered as sister group to Eremoryzomys with low support (jack- CIL -0.251 0.050 knife < 50%). LD -0.245 0.101 The maximum likelihood tree of combined genes LM -0.098 0.024 (Fig. 8) has the largest number of nodes with high BM1 -0.121 0.136 support values. The basal structure of oryzomyines is LIF -0.248 -0.068 BIF -0.317 0.538 the same as that recovered in the Irbp-only analysis BR -0.473 0.280 of Weksler (2003), with clades B, C, and D, but not A LPB -0.103 -0.152 (Scolomys is the basal-most oryzomyine, but with low BBP -0.460 -0.565 support). Relationships within each clade, however, LIB -0.239 0.196 are mostly different from Weksler (2003) and show ZB -0.308 0.010 moderate to high nodal support. In particular, all BZP -0.220 -0.458 nodes within clade D have bootstrap values > 50%. OFL -0.182 -0.052 Drymoreomys is again securely placed as sister taxon BB -0.080 -0.028 to Eremoryzomys (bootstrap = 98%) in the most basal Eigenvalue 0.014 0.006 lineage of clade D (68%). Other noteworthy novelties % of variance 42.590 19.200 from this analysis are the high nodal support values for Transandinomys and Euryoryzomys (boot- Components loadings influencing the dispersion of scores strap = 99%), Neacomys and the clade containing are in bold. Oreoryzomys and Microryzomys (90%), moderate CIL, condylo-incisive length; LD, length of diastema; LM, support for Cerradomys plus Sooretamys (75%), and length of molars; BM1, breadth of M1; LIF, length of for this clade plus Holochilus and Pseudoryzomys. incisive foramen; BIF, breadth of incisive foramina; BR, Finally, this is the first analysis in which Aegialomys breadth of rostrum; LN, length of nasals; LPB, length of and Nesoryzomys are recovered as a monophyletic palatal bridge; BBP, breadth of bony palate; LIB, least group with moderate nodal support (75%). The sepa- interorbital breadth; ZB, zygomatic breadth; BZP, breadth rate maximum likelihood analyses of Irbp and cyt-b of zygomatic plate; OFL, orbital fossa length; BB, bular (trees not shown) were very similar to the parsimony breadth. trees, and also recovered Drymoreomys as sister group to Eremoryzomys. nodal support (jackknife = 95%) for Eremoryomys + Drymoreomys within clade D. Parsimony analyses of each data partition (trees NATURAL HISTORY AND CONSERVATION STATUS not shown) produced different hypotheses for higher- Reserva Florestal do Morro Grande level oryzomyine relationships and for the placement This state preserve is located in the Cotia municipal- of Drymoreomys, but with varying levels of support. ity, 34 km west of São Paulo, in the Atlantic Highland The analysis of Irbp sequences (four trees; 693 steps; in altitudes ranging from 860 to 1075 m a.s.l. This CI = 0.53, RI = 0.70) is the only separate analysis that Atlantic Forest reserve has an area of approximately recovered a tree with mostly well-supported interge- 10 870 ha and contains a mosaic of secondary forests neric nodes. This tree is almost identical to previous in different succession stages, with some areas pre- results (Weksler, 2003, 2006), with the inclusion of senting 70–80 years of regeneration and other Drymoreomys as sister group to Eremoryzomys (jack- patches of older and mature forest. The main forest knife = 98%) within clade D (jackknife = 50%). Analy- type that covers Morro Grande is the dense montane sis of morphological characters (243 trees; 524 steps, humid forest (‘Floresta Ombrófila Densa Montana’ of CI = 0.25, RI = 0.62) produced a consensus tree with a Veloso, Rangel-Filho & Lima, 1991), but there are major basal polytomy that includes a clade containing also transitional areas with semi-deciduous forests Sooretamys, Wiedomys, and Drymoreomys (jack- and mixed Araucaria humid forests. The local climate knife < 50%). Analysis of cyt-b sequences produced is characterized by moderate annual precipitation one tree (7193 steps, CI = 0.20, RI = 0.34) that is (1200–1300 mm), weakly seasonal, with a short dry radically different from other results. Wiedomys is season from April to August (mean precipitation in

Figure 7. Phylogenetic analysis of oryzomyine relationships: Consensus cladogram of two most parsimonious trees (5513 steps, consistency index = 0.23, retention index = 0.41) of combined molecular (Irbp + cytochrome-b) and morphological characters. Jackknife (> 50%) nodal support indices are shown below branches. Clades A, B, C, and D are the same as those recovered by Weksler (2006). Outgroups include Peromyscus maniculatus (Neotominae); Nyctomys sumichrasti (Tylomyinae); and Delomys sublineatus, Thomasomys baeops, and Wiedomys pyrrhorhinos (Sigmodontinae). Oryzomyine generic taxonomy follows Weksler et al. (2006).

Figure 8. Maximum likelihood tree of combined molecular [Irbp + cytochrome b (cyt-b)] datasets (likelihood =-22 318.75). Bootstrap (> 50%) nodal support indices are shown below branches. Estimated parameters for the model are as follows: Irbp – substitution rate matrix: 1.13 (AC), 4.94 (AG), 0.6 (AT), 0.42 (CG), 6.15 (CT), and 1 (GT); a (shape parameter of gamma distribution) = 0.377; cyt-b – substitution rate matrix: 12.82 (AC), 28.51 (AG), 12.88 (AT), 1.13 (CG), 86.29 (CT), and 1 (GT); a=0.275. Clades B, C, and D are the same as those recovered by Weksler (2006). See Figure 7 for outgroup taxa used in the analysis. Oryzomyine generic taxonomy follows Weksler et al. (2006). © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 357–390 ORYZOMYINI PHYLOGENY AND BIOGEOGRAPHY 375 driest month, August, 30–60 mm) and a longer wet reserve was cleared in the early 20th century for season from September to March (mean precipitation cinchona (quinine) plantation. Secondary forest in in wettest month, January, 150–200 mm). The mean this area has a continuous and low canopy (mean monthly temperature ranges from 12.9 °C in July to height 5–10 m) and only two strata (canopy and 21.1 °C in February (for further additional informa- understory); palms, bromeliads, and ferns are abun- tion see Metzger et al., 2006). dant, as well epiphytic mosses, ferns, orchids, brome- According to Pardini & Umetsu (2006), D. albimacu- liads, vines, and other plants (see Heyer et al., 1990 latus is rare in the mosaic of continuous and frag- for additional information). mented areas of Reserva Florestal do Morro Grande, All D. albimaculatus specimens from Boracéia were with only one specimen sampled in 592 individuals caught in pitfall traps during a herpetofauna inven- captured. Bueno (2008) captured D. albimaculatus on tory conducted in the area in 2004 by Miguel T. U. 21 occasions (five individuals) through 3930 captures Rodrigues and N. Liou. Six pitfall trap lines with 24 (0.5%), in a long-term capture–recapture study. All buckets arranged in six stars were set in previous specimens were captured in continuous landscapes trails in the forest; all lines sampled relatively flat composed of undisturbed and disturbed forests, in terrain, covered with mature forest (trees with diam- seven distinct capture sites. One specimen, BS 1441, eter at breast height of 1 m), and abundant lianas, was a nulliparous nonlactating female, trapped during epiphytes, bamboo, and Heliconia thickets. As the rainy season (January 2003) in an area of mature mammals were not the prime objective of this survey, forest. Five additional specimens (AB 397, 398, 422, there is no detailed or precise information available 423, 698) were subsequently obtained at Morro Grande (external measurements, sex, and reproductive data) by R. Pardini’s team in pitfall traps, during a long-term resultant from field observations for the ten speci- sampling effort: four specimens were collected between mens; thus, data presented are derived from 2 and 8 December 2005 and one on 8 December 2006 fluid preserved specimens. The sample consists of six (AB 698). Only one of the three males obtained males, being two young individuals with abdominal presented scrotal testes; both females showed testes, two young adult specimens, and two adults un-perforated vaginas, but one was pregnant. with scrotal testes; the four females exhibit unperfo- Other sigmodontine rodents captured by Pardini & rated vaginas. Umetsu (2006) at Morro Grande were Akodon montensis, Blarinomys breviceps, Brucepattersonius sorici- Carmo, Parque Estadual Intervales nus, Delomys sublineatus, Euryoryzomys russatus, This is a protected area of Atlantic Forest with nearly Juliomys pictipes, Nectomys squamipes, Oligoryzomys 42 000 ha in the southern portion of São Paulo state nigripes, Oxymycterus dasytrichus, Rhagomys rufe- (approximately 270 km west-southwest of the city of scens, Rhipidomys mastacalis, Sooretamys angouya, São Paulo), in the watersheds (Serra de Paranapia- and Thaptomys nigrita. caba) of Rio Paranapanema, a tributary of Rio Paraná, and of Rio Ribeira de Iguape, that flows directly to Estação Biológica de Boracéia Atlantic Ocean. Parque Estadual Intervales is contigu- Boracéia is the biological field station of the Museu de ous to other protected areas, namely Parque Estadual Zoologia da Universidade de São Paulo, and is located Turístico do Alto Ribeira, Parque Estadual Carlos nearly 80 km east of the city of São Paulo. The station Botelho, and Estação Ecológica Xituê, resulting in one is located in a 16 450 ha reserve that encompasses the of the largest Atlantic Forest remnants in Brazil. The water treatment plants that supply part of the city of park landscapes vary from lowlands, ranging from 60 São Paulo and other nearby cities. to 350 m (Saibadela Base Camp), to complex systems Boracéia is situated at 900 m a.s.l. on the crest of of hills and mountains that vary from 800 to 1095 m an escarpment of coastal Serra do Mar, in the water- (Carmo and Barra Grande Base Camps). shed of rivers that flow directly to the Atlantic Ocean The climate in Parque Estadual Intervales is tem- (Rio Guaratuba) and to Rio Tietê (Rio Claro), which perate humid, with mean annual temperature in cold flows to Rio Paraná. High precipitation (average months around 12 °C and in warmer months ranging annual rainfall around 3058 mm) and orographic around 22 °C; in some elevated areas the lowest abso- moisture (as dense fog) contributes to the humidity of lute temperature during winter can reach -4 °C, with the exuberant forest. From November to January the temporary frost. The annual precipitation ranges weather is warm and wet, whereas the period from from 2000 to 3000 mm, but in some lowland areas May to August is characterized by cooler and drier may reach 4200 mm yearly. The climate is seasonal, climate, with temperatures below 0 °C in some winter but there is no marked dry period; the winter season, months. drier and cold, extends from April to September, with The main vegetation type at Boracéia is dense a monthly mean temperature of 17.4 °C, monthly montane humid forest (Heyer et al., 1990). Part of the mean rainfall of 139 mm, and monthly mean air

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 357–390 376 A. R. PERCEQUILLO ET AL. humidity of 79%. The summer, wet and hot, lasts by specimens of the genus Tibouchina, a group of from October to March and is characterized by a pioneer trees very common in the Atlantic Forest. monthly mean precipitation of 306 mm, monthly Along with the new species here described, other mean temperature of 20.9 °C, and monthly mean air small didelphid and sigmodontine mammals captured moisture of 83% (data from Viera & Izar, 1999; Man- at this site include: Didelphis aurita, Monodelphis tovani, 2001; and Osses, Nazareth & Machado, 2008). americana, Monodelphis scalops, Marmosops paulen- The vegetation at Intervales changes from the sis, Marmosops incanus, Philander frenatus, Akodon dense lower montane humid forest to dense montane cursor, Abrawayaomys ruschii, Blarinomys breviceps, humid forest. The trap site where D. albimaculatus Brucepattersonius soricinus, Delomys sublineatus, was collected is located in an area known as Carmo, Juliomys pictipes, Juliomys ossitenuis, Oligoryzomys situated in the north-western portion of the park, in nigripes, Phaenomys ferrugineus, Rhipidomys masta- the valley of Rio do Carmo where altitudes range from calis, Sooretamys angouya, and Thaptomys nigrita. 600 to 900 m, in areas of dense montane forest. This area is covered by mature or old secondary forests. Three specimens were collected by M. A. Mustrangi Parque Estadual da Serra do Tabuleiro during the austral summer, in June 1992: all are Located at Santo Amaro da Imperatriz, a municipal- mature adult females, one being pregnant with three ity nearly 40 km westwards of Florianópolis in Santa embryos. Catarina state, this preserve is situated between sea level and 1000 m, occupying an area of 87 405 hect- ares (all information provided here is from Voltolini, Ribeirão Grande 1997; J. Cherem, pers. comm.). The mean annual This sampling area is located near the perimeter of precipitation is nearly 1600 mm, and February exhib- Parque Estadual Intervales and therefore shares its the highest monthly mean rainfall (210 mm), with the latter most geographical and climatic char- whereas June is the driest month, with only 68 mm of acteristics. Two specimens were trapped by N. mean rain. The average temperature ranges from 22 Leiner in a long-term mammal monitoring project, to 24 °C in January (austral summer) and from 14 in an area of cement mining. The two specimens, and 16 °C in June (austral winter). female and male young adults, were trapped in The main type of vegetation at Serra do Tabuleiro pitfall traps in October and December of 2005, is dense montane humid forest. More luxuriant veg- respectively. The pitfall trap line was set in a dis- etation is located at the deep and more humid valleys, turbed secondary forest. and consists of well-structured forests with high canopy and diverse community of epiphytes. Exposed Estação Ecológica de Bananal slopes are steep and covered with drier forest, com- This preserve is situated in the extreme north- posed of bamboos, ferns, and small trees. Bromeliads eastern portion of São Paulo state, approximately are common throughout the study area. 350 km from the city of São Paulo. It is a 884 ha A single specimen of D. albimaculatus was captured conservation unit located on the Serra do Mar, on the in November 1993 during an inventory at Serra do southern (Atlantic) slope of Serra da Carioca range, at Tabuleiro, in a trap set on the ground. It was a 22°48′S and 44°22′W, in an altitudinal range from pregnant female that gave birth at the UFSC mammal 1200 to 1950 m. The climate is warm and wet, laboratory; one of the offspring was examined during without a dry season, and the mean annual tempera- this study (UFSC 860). The traps were assembled in a ture is 20 °C; during colder months the minimum 220 m transect through a habitat gradient along the temperatures range from -1 to 4 °C, and during eastern slope of the Serra do Tabuleiro from 400 to summer the average temperatures vary from 25 to 460 m, ranging from humid forest with abundant 28 °C (climatic data from park administration). The terrestrial bromeliads to drier forests. This transect is dominant vegetation type is dense montane humid parallel to a perennial watercourse, Rio Plaza. The evergreen forest, in different succession stages sampling consisted of conventional terrestrial trap- through the reserve, from well-disturbed (early stages ping as well as arboreal trapping, from April 1991 to of forest cover) to pristine areas. April 1994, in an effort of 15 400 trap/nights. The only specimen obtained during a survey con- Other small mammals sympatric with D. albimacu- ducted in December, 2003, employing Sherman and latus at Serra do Tabuleiro were the marsupials pitfall traps, was a young female with unperforated Gracilinanus microtarsus, Micoureus paraguayanus, vagina; this individual was captured in a pitfall trap, Philander opossum; the sigmodontines Akodon mon- in a camping site that was abandoned nearly tensis, Brucepattersonius iheringi, Delomys sublinea- 10–15 years ago, covered by a low and unstructured tus, Euryoryzomys russatus, Juliomys pictipes, forest with nearly 8–10 m in height, composed mainly Nectomys squamipes, Oligoryzomys nigripes, Soore-

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 357–390 ORYZOMYINI PHYLOGENY AND BIOGEOGRAPHY 377 tamys angouya, Oxymycterus hispidus, Rhipidomys by IUCN (2001) to assess its conservation status, mastacalis, Thaptomys nigrita; and the echimyid especially those regarding population issues (e.g. cri- Phyllomys dasythrix. teria A, C, D, and E; IUCN, 2001). Considering geographical information (criterion B), D. albimaculatus Mono, Parque Natural Municipal Nascentes presents an extent of occurrence and area of occu- do Garcia pancy superior to 20 000 and 2000 km2, respectively, The Parque Natural Municipal Nascentes do Garcia which represent the area thresholds to threat catego- is perched on the eastern slope of Serra do Espigão, in ries. Therefore, the biological data regarding this Santa Catarina state. The sampling site of D. albi- species do not allow it to be classified as a threatened maculatus, Mono, is located at 650 m and character- taxon (considering subcategories B1 or B2), even in ized by a mosaic of secondary forests approximately the lower threat category (Vulnerable). In addition, 25 years old, with extensive clutches of bamboo and this species is present in several protected areas. old abandoned pastures. However, the species is known from fewer than ten F. Steiner-Souza and S. Althoff trapped small localities and is distributed throughout an area under mammals in the Mono region for 16 consecutive intense deforestation and fragmentation processes months, from February 2005 to June 2006. Their (Ribeiro et al., 2009). Both aspects are listed under sampling efforts included conventional traps (small one important subcriterion (a) of criterion B to recog- and medium wire mesh live traps) set on the ground, nize species under threat. We assume, however, that double door Havarhart traps set employing a catwalk the capture of this species in only seven localities is a method, and pitfall traps (25 litter buckets) irregu- sampling artefact, and that forthcoming field work larly set throughout their study (see Steiner-Souza will provide further geographical information on this et al., 2008). Sixteen specimens of D. albimaculatus species. Taking into account the fragmented nature of were caught during the field work with catwalk traps the Atlantic Forest in southern Brazil, we suggest during the months of August and September 2004 that this species should be considered ‘Near Threat- (two males and one specimen with undetermined sex), ened’, and recommend a careful re-examination of from March to July 2005 (six males, five females, and this status in future assessments of endangered one specimen with undetermined sex) and in June mammalian species, hopefully in the light of new 2006 (one male). ecological and population data.

Summary DISCUSSION Based on the available natural history data compiled above, we can assume that D. albimaculatus is an Recent studies have signiﬁcantly advanced our mor- Atlantic Forest specialist, inhabiting dense and phological, systematic, and biogeographical knowl- humid montane and premontane forests. The altitu- edge of the tribe Oryzomyini, with the demonstration dinal range of the species extends from 400 to about of the monophyly and composition of the tribe (Voss 1000 m along the oriental slopes of Serra do Mar, & Carleton, 1993; Steppan, 1995; Weksler, 2003); from central Santa Catarina to central São Paulo improvement of understanding internal phylogenetic state. This species does not appear to exhibit prefer- relationships (Carleton & Olson, 1999; Smith & ences exclusively for pristine forests, being found also Patton, 1999; Bonvicino & Moreira, 2001; Weksler, in secondary and disturbed forests, even in areas that 2003, 2006); delineation of genus-group taxa content were completely deforested a few decades ago. Avail- of the tribe (Voss & Carleton, 1993; Voss, able evidence in literature (Pardini & Umetsu, 2006; Gómez-Laverde & Pacheco, 2002; Weksler et al., Bueno, 2008; also, R. Pardini, pers. comm.), however, 2006); and the discovery of important fossil remains suggests that D. albimaculatus needs areas of con- (Carleton & Olson, 1999; Pardiñas, 2008). The new tinuous (pristine or disturbed) forest to inhabit. genus and species described herein provides evidence Females are reproductively active in June and from that this knowledge is still incomplete. Probably at November to December, and males possess scrotal least some of other less-explored regions of South testes in December (it is important to notice that America still harbour undescribed endemic taxa. The reproductive data were available for only a few speci- present biological diversity of the tribe, estimated as mens), suggesting that reproduction may take place 120 extant or recently extinct species in 31 genera throughout the year. (Weksler et al., 2006; D’Elía & Pardiñas, 2007; Per- The fragmentary current knowledge on the ecology cequillo et al., 2008), will probably increase with and natural history of D. albimaculatus, along with further taxonomic and systematic work in the next the fact that this represents a new taxon for which several decades. Considering our need for better there is no available past temporal information, pre- knowledge of species diversity and distribution to cludes us from employing some of the criteria deﬁned implement conservation policies (Wheeler, Raven &

Figure 9. Distribution map of known collection localities of sister taxa Drymoreomys albimaculatus gen. et sp. nov. and Eremoryzomys polius in South America. Inset: detail of collection localities of E. polius in upper Río Marañon basin, in northern Peru; see Gazetteer (Appendix 1), where numbers are associated with collection localities.

Wilson, 2004), inventory and taxonomic studies intergeneric relationships differ between the parsi- should be stimulated in the next few years. mony and likelihood analyses only for nodes with low Resolution and nodal support for recovered support in at least one of them (usually parsimony). phylogenetic relationships amongst oryzomyines The sister-taxon relationship between D. albimacu- receive substantial support in the present analyses. latus and Eremoryzomys polius recovered with strong The results of the combined Irbp/cyt-b maximum nodal support in both parsimony and maximum like- likelihood analysis, in particular, provide the ﬁrst set lihood analyses is a wholly unexpected result. Biogeo- of well-supported hypotheses for relationships within graphically, D. albimaculatus and E. polius form an major oryzomyine lineages, especially clade D awkward pair: the ﬁrst is endemic to lower montane (Weksler, 2003, 2006). The basal structure of ory- areas (400–1000 m) in the Atlantic Forest of eastern zomyine phylogeny, with taxa divided into three Brazil, whereas the second is an Andean endemic major clades, is corroborated in the present analyses, (760–2100 m) from the valley of the lower Río Marañon but ‘clade A’ (composed of Scolomys and Zygodonto- in northern Peru (Fig. 9). The two taxa are both mys) was only recovered in the parsimony analyses restricted to well-known Neotropical centres of ende- that included morphological data. By contrast, Sco- mism (Müller, 1973; Cracraft, 1985). Drymoreomys lomys and Zygodontomys were never recovered as albimaculatus is a member of the Serra do Mar centre, sister taxa in any molecular analysis, but were whereas E. polius is distributed in the Marañon centre. always placed as basal members of the tribe. Other Sister-group relationships between members of the

Serra do Mar and Marañón centres are unknown in past connection between eastern (Atlantic Forest) and the literature, and other phylogenetic pairings of western South America (Andean life zones) small restricted Atlantic Forest and Andean endemics as terrestrial vertebrate communities, which subse- sister taxa are not very common amongst Neotropical quently diverged into the present lineages. terrestrial vertebrates. We found only four clear cases The Atlantic Forest has long been considered as a of such Andean and Atlantic Forest clades or taxa with unique entity, either as a biome (Fonseca, 1985; Myers sister relationships: hylid frogs, parrots, and akodont et al., 2000) or as a biogeographical region, being and thomasomyine rodents. None of these examples, recognized as an important centre of endemism however, share the highly particular pattern of Dry- (Müller, 1973; Cracraft, 1985). Several lines of evi- moreomys and Eremoryzomys. dence (Moojen, 1948; Por, 1992; Vivo, 1997) suggested In their comprehensive systematic revisions of that the Atlantic Forest and the lowland Amazon family Hylidae, Faivovich et al. (2004, 2005) observed Forest, the two major forested landscapes of South that in the subgroup Hypsiboas pulchellus an America currently isolated by the dry corridor of open ‘...Andean clade is nested within an Atlantic Forest/ vegetation, had a common past history (Vivo, 1997; Cerrado clade...abiogeographic pattern that we are Costa, 2003). As a consequence, these regions fre- not aware of in other vertebrate groups’ (Faivovich quently appear as closely phylogenetically related on et al., 2004: 946). More precisely, the Andean clade area-relationship analyses (Cracraft, 1988; Cracraft & from Argentina and Bolivia is sister to a clade con- Prum, 1988; Bates, Hackett & Cracraft, 1998), or their taining taxa from the Atlantic Forest, pampas, and species are recovered as sister taxa (Patton et al., 1997; from scrubland from Sierras of Central Argentina Patton, Silva & Malcolm, 2000). However, these (Faivovich et al., 2004, 2005). studies only considered forested areas and their faunas Parrots of the genus Pionus display a similar for comparative analyses, which probably biased the pattern (Ribas et al., 2007): the Pionus maximillianus results obtained. Costa (2003), in a multitaxa mam- species group, distributed in eastern Brazil, Para- malian biogeographical analysis employing molecular guay, and Argentina from sea level to 2000 m, is markers, suggested that the central South American recovered as the sister taxon to the Pionus sordidus dry forests played a important role in the evolutionary group, which is distributed through the Andes, from history of small mammals, with species from this Bolivia to Venezuela ranging from 450 to 3000 m. region being more closely related to the Atlantic Vicariance is hypothesized as the main process Forest, to the Amazon Forest, or sister to both taxa. of diversiﬁcation between montane (Andean) and This author also stated that the biogeographical lowland (eastern South America) clades (Ribas et al., history of the Neotropics would hardly be explained by 2007: 2404). a single unifying hypothesis. Our examples cited above Phylogenetic studies on the genus Akodon (by additionally suggest a historical relationship between Pardiñas et al., 2005; Gonçalves et al., 2007; Smith & the Serra do Mar and Austral Andean centres of Patton, 2007) recovered Atlantic Forest species of the endemism (Hypsiboa), between Serra do Mar and the Akodon cursor group (including A. cursor, Akodon Peruvian Andes (Akodon, Rhagomys), and between montensis, Akodon mystax, Akodon paranaensis, Serra do Mar and the Andean Cordillera (Pionus). and Akodon reigi) as the sister group to the Andean In these cases, however, the general pattern is that Akodon boliviensis group (namely A. boliviensis, both Atlantic Forest and Andean taxa are inhabitants Akodon fumeus, Akodon juninensis, Akodon kofordi, of humid forest formations. By contrast, E. polius Akodon lutescens, Akodon spegazzinii, Akodon subfus- inhabits a Central Andean valley, westward to the cus). Another sigmodontine genus with an Atlantic Cordillera Central of Peru and in a rain-shadow area, Forest-Andean connection is Rhagomys with two characterized by hot and arid climate (Osgood, 1914: species: Rhagomys rufescens (that occurs from Santa 145; Cracraft, 1985). Accordingly to Osgood (1914), all Catarina to Espírito Santo; Percequillo et al., 2004; six specimens of E. polius were obtained at Tambo Steiner-Souza et al., 2008), and the recently described Carrizal (c. 1500 m), that is located east of Balsas Rhagomys longilingua (from the eastern slope of the (c. 300 m) on the right bank of Río Marañon: ‘A tiny Andes from Peru and Bolívia; Luna & Patterson, 2003; spring here is surrounded by a clump of trees...and D’Elía et al., 2006; Villalpando, Vargas & Salazar- the steep slope below has some moderately extensive Bravo, 2006). The former species inhabits lowland and thickets of low bushes which moisture from the spring montane humid forests in the Serra do Mar, from sea permits to ﬂourish. Elsewhere conditions are arid level to nearly 1100 m, whereas the latter is restricted with occasional bunches of grass, cactuses, or small to the lowland humid, montane, and cloud forests of bushes’. Another area, Condechaca (BMNH speci- the Bolivian and Peruvian Andes, from 450 to 2100 m. mens), is situated just a few kilometres southwards of The general congruence of biogeographical patterns Chachapoyas and ‘...issurrounded by relatively arid amongst birds, frogs, and rodents highlights a possible foothills’ (Thomas, 1926: 157).

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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Table S1. Data matrix for morphological and molecular characters. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.

APPENDIX 1 11. Río Utcubamba, 29 km south, 38 km east of Bagua, 762 m [on the original label, 2500 ft.] Collecting localities of genera Drymoreomys and 5.9°S, 78.2°W (collector). Not recorded col., Eremoryzomys in South America. 24.viii.1967. MVZ 135657. 12. Tambo Carrizal, mountains east of Balsas, 1524 m [on the original label, 5000 ft.] c. 06°47′S, 77°52′W GAZETTEER (Stephens & Traylor, 1983); type locality of Ory- Brazil zomys polius. W. H. Osgood and M. P. Anderson, SÃO PAULO cols., 18.v.1912. FMNH 19762-7. 1. Cotia, Reserva Florestal do Morro Grande, 860– 13. Tingo, 30 km south, 41 km east of Bagua, Río 1075 m. 23°41′S, 46°58′W (collector). Renata Utcubamba, 3000 ft. 5.9°S, 78.2°W (collector). Carl Pardini, collector (thereafter col.), 22.i.2003. B. Koford, col., 25.viii.1967. MVZ 135658. MZUSP BS 1441, AB 397, 398, 422, 423, 698. CAJAMARCA 2. Bananal, Estação Ecológica de Bananal, 1200 m. 22°48′22″S, 44°22′08″W (collector). Alexandre R. 14. Cutervo, Chaupe, 1800 m. 05°10′S, 79°10′W Percequillo, col., 13.xii.2003. MZUSP 33782. (Stephens & Traylor, 1983). H. Watkins, col., 3. Ribeirão Grande, Parque Estadual Intervales, 03.ii.1923. AMNH 64054. Carmo, 700 m. 24°20′S, 48°25′W (collector); type 15. San Ignacio, 1400 m. 05°08′S, 78°59′W (Stephens locality of Drymoreomys albimaculatus. Meika A. & Traylor, 1983). H. Watkins, col., v.1923. AMNH Mustrangi, col., 21–22.vii.1992. MZUSP 34716, 64055-6. MVZ 182089. UNKNOWN LOCALITY ′ ′ 4. Ribeirão Grande, Mina Limeira; 24°10 S, 48°21 W –. Specimen MCZ 17047 (see Appendix 2) was col- (USBGN). Natalia Leirner, col., x–xii.2005. lected during the summer of 1916 by G. K. Noble MZUSP RG 47, 48. under the auspices of the Harvard Peruvian Expedi- 5. Salesópolis, Estação Biológica de Boracéia, tion, which sampled the north-western portion of ′ ′ 900 m. 23°38 S, 45°52 W (Heyer et al., 1990). Peru (see Bangs & Noble, 1918), in an area delimited Miguel T. U. Rodrigues, col., 19–24.ii.2004. by the localities of Payta (also spelled Paita, in Piura MZUSP BO 24, 41–44. Department, 05°06′S 81°07′W), Tabaconas (Cajama- SANTA CATARINA rca Department, 05°19′S 79°18′W), and Chiclayo (Lambayeque Department, 06°46′S 79°51′W). There 6. Blumenau, Parque Natural Municipal Nascentes are conﬁrmed records of Eremoryzomys polius in ′ ″ ′ ″ do Garcia, 650 m. 27°02 58 S, 49°08 57 W (collec- Amazonas and Cajamarca departments (see above), tor). Francisco Steiner, col., ii.2005–v.2006. FURB but possible occurrences at Lambayeque and Piura 9621, 9664, 9666, 9743, 9756, 9787, 9833, 9838, are zoogeographically coherent. 9862, 9871, 9902, 9962, 12044. 7. Blumenau, Parque Natural Municipal Nascentes do Garcia, Terceira Vargem do Ribeirão Garcia, APPENDIX 2 Vale do Espingarda. Not located; same coordi- List of specimens examined. nates as previous locality. Juliano Cristofolini, col., 29.ix.2001. FURB 6267. 8. Parque Estadual da Serra do Tabuleiro, 400– CERRADOMYS SPP. 460 m. 27°44′S, 48°49′W (J. Albuquerque, pers. BOLIVIA: BENI: San Joaquin: M: FMNH 96103, comm.). Julio Voltolini and Jorge J. Cherem, cols. 116762, 116773, 116775-8, 116810, 116812, 116819, UFSC 860. 116848-9, 116852, 116855-6, 116858-9, 116880, USNM 364746, 390673; F: FMNH 96109, 116754-6, 116760-1, 116763, 116767, 116788, 116790, 116832, Peru 116854, 116866, 116875, 116902, 116910. BRAZIL: AMAZONAS GOIÁS: Anápolis: M: AMNH 134633, 134640, 134655, 9. 19 km (by road) east of Balsas, 1944.6 m [on the 134660, MN 4338, 4345; F: AMNH 134629, 134636, original label, 6380 ft.] c. 06°44′S, 77°50′W 134650, 134785, MN 4347. PARAÍBA: Natuba: M: (FMNH). B. D. Patterson, col., 2–3.v.1987. FMNH UFPB 24, 38, 41, 63, 175, 258, 2066, 2073, 2078; F: 129242-3, 129245. UFPB 25, 31, 35, 257, 2068. Pirauá, Natuba: M: 10. Condechaca, Río Utcubamba, 2133.6 m [on the UFPB 1, 178, 180, 181, 182, 183, 221, 2059; F: UFPB original label, 7000 ft.] 06°21′27″S, 77°54′39″W 12, 220; I: UFPB 47. Salgado São Félix: M: UFPB: M (NIMA). Godman-Thomas Expedition, R. W. 28, 37, 39, 45, 46, 228, 231, 2057; F: UFPB 29, 37, Hendee, col., 14.xi.1925. BMNH 26.5.3.16. 233; I: UFPB 229. Teixeira, Pico do Jabre: M: UFPB

1955, 1977, 2367; F: UFPB 1976, 2060, 2366. DIS- omys albimaculatus and other taxa, and changes in TRITO FEDERAL: Brasília: I: FMNH 128313. Fazenda oryzomyine scoring from Weksler (2006). Água Limpa: M: UFPB 1925. Parque Nacional de Brasília: M: UnB 338, 346, 348, 922, 957; F: UnB 343, 347, 923, 924. Reserva Biológica de Águas Emenda- INTEGUMENTARY ANATOMY das: M: UnB 488, 493, 527, 529, 535, 554, 574, 576, 1. Four mammae present in inguinal and abdominal 586, 1314; M: UnB 499, 526, 553, 577; I: UnB 597, pairs (0); or six mammae in inguinal, abdominal, 603. Reserva Ecológica Roncador: M: UnB 954; F: and postaxial pairs (1); or eight mammae in UnB 939. inguinal, abdominal, postaxial, and pectoral pairs (2). 2. Claws of manus small, not extending much beyond digital pads, not keeled (0); or claws long, EREMORYZOMYS POLIUS extending conspicuously beyond digit pads and PERU: F: MCZ 17047. AMAZONAS: 19 km (by road) ventrally, keeled for about half their length (1). east of Balsas: M: FMNH 129243, 129245; F: FMNH 3. Ungual tufts at base of manual claws present and 129242. Condechaca, Río Utcubamba: M: BMNH long (0); or reduced or absent (1). 26.5.3.16. Río Utcubamba, 29 km south, 38 km east of 4. Hypothenar pad of pes present (0); or absent or Bagua: MVZ 135657. Tambo Carrizal, mountains east vestigial (1). of Balsas: M: FMNH 19766-7; F: FMNH 19762-5. 5. Plantar pads on hind feet large and fleshy, inter- Tingo, 30 km south, 41 km east of Bagua, Río Utcu- digitals 1–4 set close together, often in contact (0); bamba: MVZ 135658. CAJAMARCA: Chaupe: AMNH or pads smaller but still fleshy, interdigitals 1 and 64054. San Ignácio: AMNH 64055-6. 4 displaced proximally relative to 2 and 3 (1); or interdigital pads distributed as in state 1 but extremely small and with low relief (2). NECTOMYS SPP. 6. Plantar surface of hind feet smooth, without well- BRAZIL: SÃO PAULO: Salesópólis, Estação Biológica developed squamae (0); or plantar surface de Boracéia: M: MZUSP 6896, 8849, 9728-30; F: covered with squamae (1). The plantar surface of MZUSP 21250; I: MZUSP 10419. Sigmodontomys aphrastus is densely covered with distinct squamae distal to thenar pad, i.e. state ‘1’ (McCain et al., 2007). 7. Ungual tufts present on all claws of hind foot as OECOMYS CATHARINAE a uniform thick sheath extending to or beyond BRAZIL: SÃO PAULO: Parque Estadual Intervales: claw tip (0); or tufts absent on digit I (dI), present M: MVZ 182087, 200983, 200984, 200986; F: MVZ on dII–dV as a uniform thick sheath extending to 200982, 200985. or beyond claw tip (1); or tufts absent on dI, present as sparse cover and with few hairs extending beyond the claw tip on dII–dV (2); or RHIPIDOMYS MASTACALIS tufts extremely reduced or absent on all claws (3). Sigmodontomys aphrastus has reduced tufts on BRAZIL: SÃO PAULO: Bananal, Estação Ecológica de dII-dV (McCain et al., 2007; contra Weksler, Bananal: M: MZUSP EBM 054; F: MZUSP 32525-7, 2006). MZUSP EBM 756. 8. Natatory fringes on hind feet absent (0); or present (1). 9. Interdigital webbing on hind feet absent (0); or SOORETAMYS ANGOUYA present but small, not extending to first interpha- BRAZIL: SÃO PAULO: Salesópolis, Estação Biológica langeal joint of any digit (1); or present and long, de Boracéia: M: MZUSP 9470, 9727, 9740, 9741, 9887, extending to or beyond first interphalangeal 9888, 10820, 10852, 20579, 21956, 23933, 23945, joints of digits II, III, and IV (2). 23949; F: MZUSP 10201, 10368, 20578, 21930, 23934, 10. Dorsal surface of hind feet densely covered with MAM 423, U: MZUSP 20575, 22467, 25511. white hairs, feet appear solid white (0); or dorsal surface sparsely covered with short silvery hairs, feet appear greyish white or pale tan (1); or dorsal surface covered with dark hairs, feet APPENDIX 3 appear brown (2); surface of pes densely covered Morphological characters used in phylogenetic analy- with brown hairs and white/silvery hairs (3). sis. We include here new information for Drymore- New state ‘3’ added to describe condition of

Drymoreomys. Sigmodontomys aphrastus is now cally constricted with conspicuously beaded scored as polymorphic ‘[12]’ (see McCain et al., supraorbital margins (2); or interorbital region 2007). convergent anteriorly (cuneate) with weakly 11. Ventral surface of tail covered with dark hairs (0); beaded supraorbital margins (3); or interorbital or covered with hairs with dark basal band and region convergent anteriorly with well-developed white distal band (1); or covered with white hairs supraorbital crests (4). Obs. Hylaeamys mega- (2). Observation Sooretamys angouya is now cephalus is now considered to have state ‘3’, i.e. scored ‘0’ instead of ‘1’ (its tail is unicoloured; interorbital region anteriorly convergent with Weksler et al., 2006). weakly beaded supraorbital margins instead of 12. Tail densely furred, scales not visible even at ‘1’, i.e. hourglass-shaped with squared margins higher magnification (0); or tail sparsely furred, (Weksler et al., 2006). We scored D. albimacula- scales macroscopically obvious (1). tus as state ‘3’ based on the older specimens 13. Dorsal and ventral fur without grooved spines (0); available. or with grooved spines (1). 23. Postorbital ridge absent, posterior orbital wall 14. Ventral fur with plumbeous or dark grey base (0); without conspicuous relief, frontosquamosal or ventral fur entirely white, without dark base suture exposed (0); or postorbital ridge present (1). Obs. Oreoryzomys is now scored ‘0’ instead of ‘1’ and concealing frontosquamosal suture in most (its ventral pelage is grey-based, not entirely old specimens (1). white; Weksler et al., 2006). Some specimens of D. 24. Frontosquamosal suture continuous with the albimaculatus present patches of entirely whitish frontoparietal suture, dorsal facet of frontal never hairs on gular and thoracic region, but we codified in contact with squamosal (0); or frontosquamosal D. albimaculatus as having plumbeous ventral fur suture anterior to frontoparietal suture, leading given its predominance in the ventral region. to an area of contact between dorsal facet of 15. Dorsal and ventral colours sharply delimited, frontal and squamosal (1). dorsum much darker than pale ventral surface, 25. Parietals restricted to the dorsal surface of the resulting in conspicuous countershading (0); or braincase, or slightly expanded below the lateral dorsal and ventral colours subtly delimited, edges of the dorsal at about the squamosal root dorsum slightly darker than ventral surface, of the zygomatic arch (0); or parietals deeply resulting in weak countershading (1); or limits of expanded onto lateral surface of the braincase (1). dorsal and ventral colours indistinct, ventral 26. Interparietal wider than posterior border of fron- surface dark, countershading absent (2). tals, in contact with squamosal (0); interparietal 16. Subauricular patches absent (0); or present (1). strap-shaped, nearly as wide as posterior border of frontals, but not in contact with squamosal (1); or interparietal wedge-shaped, about half as wide SKULL as posterior border of frontals, not in contact with 17. Rostral tube absent (0); or present (1). squamosal (2). 18. Nasals with blunt posterior margin (0); or nasals 27. Basicranial flexion weakly pronounced, foramen with acutely pointed terminus, forming a sharp magnum orientated mostly caudad (0); or angle (1). strongly pronounced, foramen magnum orien- 19. Nasals short, not extending posteriorly beyond tated mostly posteroventrally (1). the triple-point suture between the maxillary, 28. Zygomatic plate narrow and zygomatic notch frontal, and lacrimal (0); or long, extending indistinct; anterior border of plate flat, below or posteriorly well beyond the maxillary–frontal– slightly in front of anterior margin of superior lacrimal suture (1). maxillary root of zygoma (0); or plate broad with 20. Premaxillaries long, extending posteriorly beyond moderate or deep notch; anterodorsal margin the nasals (0); or shorter, extending posteriorly to smoothly rounded, conspicuously anterior to about the same level as the nasals (1); or very superior maxillary root of zygoma (1); or plate short, terminating anterior to the nasals (2). broad and notch conspicuous; anterodorsal 21. Lacrimal equally contacting maxillary and margin produced as a sharp corner or spinous frontal bones (0); or lacrimal contacting mainly process, conspicuously anterior to superior max- maxillary (1). illary root of zygoma (2). 22. Interorbital region symmetrically constricted 29. Posterior margin of zygomatic plate situated (hourglass-shaped or amphoral), with rounded anterior to the alveolus of M1 (0); or approxi- supraorbital margins (0); or interorbital region mately even with the alveolus of M1 (1). Drymore- symmetrically constricted with squared supraor- omys albimaculatus was scored as polymorphic bital margins (1); or interorbital region symmetri- for this character.

30. Jugal present and large, maxillary and squamo- vacuities present but reduced, situated posterior sal processes of the zygoma not overlapping (0); to basisphenoid–presphenoid suture (3). or jugal present and small, maxillary and squa- 37. Stapedial foramen and posterior opening of mosal processes overlapping, but not in contact alisphenoid canal large, squamosal–alisphenoid (1); or jugal absent, or reduced to slivers of bones, groove and sphenofrontal foramen present (0); maxillary and squamosal processes in contact or stapedial foramen and posterior opening of (2). The jugal of Eremoryzomys polius is large alisphenoid canal large, squamosal–alisphenoid without overlap of maxillary and squamosal groove and sphenofrontal foramen absent (1); (state ‘0’). or stapedial foramen and posterior opening of 31. Posterior margins of incisive foramina conspicu- alisphenoid canal small, squamosal–alisphenoid ously projecting between first molars (0); or ter- groove and sphenofrontal foramen absent, sec- minating anteriorly or at the front of first molar ondary branch crosses dorsal surface of pterygoid alveoli (1). plate (2). 32. Palate short, mesopterygoid fossa extends ante- 38. Alisphenoid strut present, buccinator-masticatory riorly between the molar rows (0); or palate of and accessory foramen ovale separate (0); or strut intermediate length, mesopterygoid fossa extends absent, buccinator-masticatory and foramen anteriorly between the maxillary bones but not ovale confluent (1). between M3s (1); or palate long, mesopterygoid 39. Anterior opening of alisphenoid canal present, fossa does not extend anteriorly between the large (0); or absent (1). maxillary bones (2). 40. Subsquamosal fenestra present (0); or fenestra 33. Bony palate flat, or with shallow lateral excava- vestigial or absent (1). tions, never with median longitudinal ridge (0); or 41. Ectotympanic bullae small, exposed flange of with deep lateral troughs separated by median periotic extends to internal carotid canal (0); or longitudinal ridge (1). ectotympanic bullae intermediate, exposed wedge 34. Posterolateral palatal pits absent (0); or one of periotic smaller and not contributing to wall of simple small foramen present at each side of the carotid canal (1); or ectotympanic bullae large, posterior palate (1); or posterolateral palatal pits periotic bone mostly masked in ventral view (2). always present as conspicuous perforations, 42. Posterior suspensory process of squamosal usually more than one foramen, not recessed in present and connected to the tegmen tympani (0); fossae or recessed in shallow depression (2); or or posterior suspensory process absent, tegmen posterolateral palatal pits always present as per- tympani not touching or barely in contact with forations within deeply recessed fossa, generally squamosal (1). with three foramina, one directed posteriorly, 43. Mastoid completely ossified, or with a diminutive one anteriorly, and one dorsally (3). The postero- pit in the dorsal contact with the exoccipital lateral palatal pits of Mindomys hammondi border (0); mastoid with conspicuous fenestra (1). and Sigmodontomys aphrastus are polymorphic 44. Capsular process of lower incisor alveolus absent (states ‘1’ and ‘2’; i.e. ‘C’), as some analyses of (0); or projection present but reduced as a slight additional exemplars revealed multiple postero- rounded elevation (1); or projection present, well lateral palatal pits recessed in moderately developed as a conspicuous swelling with acute deep fossae (Weksler et al., 2006; McCain et al., projection (2). 2007). 45. Superior and inferior masseteric ridges converge 35. Parapterygoid fossae at same level as palate (0); anteriorly as an open chevron (0); or anterior or parapterygoid fossae dorsally excavated but portion of ridges conjoined as single crest not reaching level of mesopterygoid roof (1); or (1). parapterygoid fossae deeply excavated, reaching 46. Anterior edge of masseteric crests below m1 (0); level of mesopterygoid roof (2). Eremoryzomys or edge anterior to m1, extending to diastema (1). polius is now scored as ‘1’ instead of ‘2’, because 47. Entoglossal process of basihyal present as small its parapterygoid fossae are distinctly shallower knob, basihyal arched, and thyrohyal long, than those of Holochilus and Lundomys (Weksler greater than or equal to the length of the basihyal et al., 2006). (0); or entoglossal process absent, basihyal 36. Sphenopalatine vacuities present as large aper- straight, and thyrohyal short, less than length of tures along the presphenoid, reaching basisphe- basihyal (1). noid (0); or vacuities present but reduced, generally as narrow openings, anterior to DENTITION basisphenoid–presphenoid suture (1); or vacuities 48. Labial accessory root of M1 absent (0); or present absent, mesopterygoid roof totally ossified (2); or (1). The labial accessory root of M1 buttressing

the paracone is absent in Sooretamys angouya dentine basin without enamel connection (2). (changed from ‘1’ to ‘0’). Mindomys hammondi and Aegialomys xanthaeo- 49. Labial and lingual accessory roots of m1 absent lus have posterior, not anterior, connection of (m1 with two roots total) (0); or one accessory root protocone to paracone (Weksler et al., 2006). present (three roots total) (1); or two accessory 61. Mesolophs on M1 and M2 well developed, extend- roots present (four roots total) (2). Examination of ing from the median mure to the labial cingulum, additional specimens of Oreoryzomys balneator, fused with mesostyle (0); or mesolophs small, not Euryoryzomys lamia, and Euryoryzomys maccon- extending to labial cingulum and not fused with nelli revealed the absence of labial and lingual the mesostyle (1); or mesolophs on M1 and M2 accessory roots on the first lower molar (Weksler absent (2). et al., 2006). The new state definitions ignore root 62. Median mure connected to protocone on M1 (0); position when only a single accessory root is or median mure not connected to protocone (1). present. 63. Protoflexus of M2 present (0); or absent (1). Speci- 50. Second lower molar with two roots (0); or three mens of Aegialomys xanthaeolus have a well- roots (1). developed protoflexus on M2 (Weksler et al., 51. Incisors opisthodont (0); or orthodont (1). 2006). Changed from ‘1’ to ‘0’; fully adult specimens 64. Paracone on M2 without accessory loph (0); of Mindomys hammondi and Sigmodontomys or accessory loph present posterior to paracone aphrastus are opisthodont (Weksler et al., 2006; (1). McCain et al., 2007). 65. Mesoflexus present as single internal labial fos- 52. Enamel band of upper incisors smoothly rounded, sette on M2 (0); or mesoflexus divided into labial or flattened but without labial bevel (0); or band and medial fossetti (1). Euryoryzomys lamia and flattened medially, with distinct labial bevel (1). Mindomys hammondi have two internal fossettes 53. Molars bunodont and brachydont (0); or molars in all examined (Weksler et al., 2006). Some planar and hypsodont (1). individuals of D. albimaculatus present the 54. Labial flexi not patent, closed off by labial cingula mesoflexus (or mesofossette) divided in three (0); or labial flexi patent, cingula absent (1). fossetti, labial, medial, and lingual (scored 55. Maxillary tooth-rows parallel (0); or anteriorly as ‘1’). convergent (1). 66. Mesoloph on M3 present and well developed (0); 56. Flexi of M1 and M2 do not interpenetrate (0); or or absent or vestigial (1). flexi meet at midline, enamel overlaps (1); or flexi 67. Posteroloph on M3 present (0); or absent (1). interpenetrate (2). 68. Hypoflexus on M3 present, remaining excavated 57. Anterocone of M1 divided into labial and lingual until later wear stages (0); or hypoflexus absent conules by anteromedian flexus (0); or anterocone or diminutive, disappearing with little occlusal partially divided into labial and lingual conules wear (1). by internal fold of procingulum, anteromedian 69. Anteromedian flexid and anteromedian fossettid flexus absent (1); or anterocone undivided, absent on first lower molar (0); or anteromedian anteromedian flexus and internal fold of procin- flexid absent but anteromedian fossettid present gulum absent (2). Aegialomys xanthaeolus and (1); or anteromedian flexid present and antero- Eremoryzomys polius do not have divided anteromedian fossettid absent (2). Oreoryzomys balnea- cones; they are scored as ‘2’ because their internal tor does not have a deep and persistent cleft in folds are not homologous to the one described in the anteroconid as seen in Microryzomys)Itis state ‘1’ (M. Weksler, unpubl. data). instead coded as absent or indistinct (i.e. state 58. Anteroloph on M1 well developed and discrete, ‘1’). reaching the labial cingulum, anteroflexus 70. Anterolabial cingulum on m1 absent (0); or long present (0); or anteroloph present but small, not anterolabial cingulum present (1). The anterola- reaching the labial cingulum, anteroflexus absent bial cingulum of m1 is present in Euryoryzomys (1); or anteroloph fused with anterocone labially, lamia (Weksler et al., 2006). anteroflexus present as small fossette (2); or 71. Ectolophid and ectostylid on m1 absent (0); or anteroloph and anteroflexus absent (3). present (1). 59. Protostyle on M1 absent (0); or present (1). 72. Mesolophids present and well developed on m1 60. Paracone of M1 connected to protocone by enamel and m2 (0); or mesolophids present in unworn bridge situated at posterior-most end of protocone dentition but small, not extending to lingual cin- (0); or paracone connected to protocone by enamel gulum (1); or mesolophids completely absent (2). bridge situated at anterior portion of protocone 73. Anterolabial cingulum present on m2 (0); or (1); or protocone and paracone forming single absent (1).

74. Anterolophid absent or weakly expressed on m2 85. Large bacular cartilaginous apparatus with and m3 (0); or anterolophid and companion central digit more robust than lateral digits (0); metaflexid distinct (1). or reduced cartilaginous apparatus with slim 75. Anterolabial margin of m3 with shelf-like cingu- central digit (1); bifid cartilaginous apparatus lum, separated from protoconid by protoflexid (0); with central digit absent (2). Sigmodontomys or anterolabial margin of m3 smoothly rounded, aphrastus has reduced cartilaginous apparatus without cingulum, protoflexid absent (1). The with slim central digit (‘1’). Cerradomys subflavus anterolabial cingulum of m3 is present in some has a bifid apparatus as described in new state specimens of Mindomys hammondi (see Weksler ‘2’. et al., 2006), and was scored as ‘A’ [i.e. (01)]; the 86. Nonspinous tissue of crater rim does not conceal anterolophid is observed on m2 and m3 of young bacular mounds (0); or nonspinous tissue conceals and some subadult individuals of D. albimacula- bacular mounds (1). tus. 87. Dorsal papilla of glans penis spineless (0); or 76. Posteroflexid on m3 present, well developed (0); spinous (1). The apex of dorsal papilla presents or posteroflexid present as a small groove, a spine, similar to Sigmodontomys alfari (see obvious only in juveniles, obliterated with wear Hooper & Musser, 1964: fig. 2l), but is otherwise (1); or posteroflexid absent (2). spineless (scored as ‘0’). 88. Subapical lobule on ventral surface of urethral processes absent (0); or present (1). The urethral POSTCRANIAL SKELETON process of the glans penis of D. albimaculatus 77. Thirteen ribs present (0); or 12 ribs (1). presents a large lateral lobule, distinct from the 78. Tuberculum of first rib articulates with trans- subapical lobule present in Oryzomys species and verse process of first thoracic vertebra only (0); or Holochilus brasiliensis (i.e. state ‘1’). Scored as ‘0’. first rib contacts transverse processes of both the 89. Two pairs of preputial glands present (0); or one first thoracic and seventh cervical vertebrae (1). pair present (1); or preputial glands absent (2). 79. Anapophyses present on the 17th thoracico- The preputial glands of D. albimaculatus are lumbar vertebra (0); or anapophyses absent or extremely developed, greatly enlarging the base vestigial (1). of the prepuce on external appearance. 80. Haemal arches absent between caudal vertebrae 90. Two pairs of ventral prostate glands present (0); 2 and 3 (0); or haemal arches present, with or ventral prostate glands absent (1). simple posterior border (1); or present, with 91. Anterior prostate glands present (0); or absent spinous posterior border (2). (1). 81. Entepicondylar foramen of humerus present (0); 92. Vesicular glands present, large, shaped like a or absent (1). cane or inverted ‘J’ (0); or vesicular glands 82. Supratrochlear foramen in humerus absent (0); or present, shaped like small diverticula (1); or present (1). vesicular glands absent (2). 83. Trochlear process of calcaneum at the same level 93. Preputial glands extend to or beyond the ventral as posterior articular facet, trochlear process flexure of the penis (0); or do not extend to the broad and shelf-like (0); or gap between proximal ventral flexure of the penis (1). edge of trochlear process and posterior articular 94. Dorsal prostates absent (0); or one pair present facet, process shorter and less shelf-like (1). (1); or two pairs present (2). The condition observed in D. albimaculatus is 95. Ampullary glands forming tufts of tubules that intermediary to those proposed in Weksler (2006) extend cranially from the base of the vas deferens and similar to that illustrated by Carleton (1980). (0); or ampullary glands compact, not elaborate There is no large gap between the trochlear (1). process and the posterior articular surface of 96. Subterminal flexure of vesicular gland rounded calcaneum. and smooth (0); or irregularly lobed and notched (1); or small and finger-shaped (2). 97. Gall bladder present (0); or absent (1). REPRODUCTIVE AND VISCERAL ANATOMY 98. Gastric glandular epithelium of stomach limited 84. Lateral bacular mounds absent or diminutive (0); to antrum, not extending beyond incisura angu- or present as large protuberances (1). Sigmodon- laris (0); or gastric glandular epithelium covers tomys aphrastus has large lateral bacular antrum and proximal portion of corpus near mounds (‘1’). oesophageal opening (1).