A REVISION OF THE DIDELPHID MARSUPIAL GENUS MARMOSA

PART 1. THE SPECIES IN TATE’S “MEXICANA AND MITIS “SECTIONS AND OTHER -CLOSELY RELATED FORMS

ROGERIO V. ROSSI, ROBERT S. VOSS, AND DARRIN P. LUNDE

BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY

A REVISION OF THE DIDELPHID MARSUPIAL GENUS MARMOSA

PART 1. THE SPECIES IN TATE’S ‘MEXICANA’ AND ‘MITIS’ SECTIONS AND OTHER CLOSELY RELATED FORMS

ROGERIO V. ROSSI

Universidade Federal de Mato Grosso Instituto de Biociéncias Departamento de Biologia e Zoologia Ay. Fernando Corréa da Costa s/n, Cuiaba, MT, Brazil, CEP. 7&060-900

ROBERT S. VOSS

Department of Mammalogy American Museum of Natural History

DARRIN P. LUNDE

Department of Mammalogy American Museum of Natural History

BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY Number 334, 83 pp., 30 figures, 8 tables Issued June 3, 2010

Copyright © American Museum of Natural History 2010 ISSN 0003-0090

CONTENTS

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Appendix

ABSTRACT

We revise the nominal species of mouse opossums currently synonymized with Marmosa mexicana Merriam, 1897, and M. robinsoni Bangs, 1898, which include all of the trans-Andean taxa currently assigned to the nominotypical subgenus of Marmosa. In addition, we redescribe two other species that appear to be closely related to M. mexicana and M. robinsoni based on morphological or molecular citeria: M. rubra Tate, 1931, and M. xerophila Handley and Gordon, 1979. Based on first-hand examination of holotypes and other material (about 1500 specimens in total), we additionally recognize M. isthmica Goldman, 1912, and M. simonsi Thomas, 1899 (both currently synonymized with M. robinsoni), and M. zeledoni Goldman, 1917 (currently synonymized with M. mexicana), as valid species. For each of the seven species recognized as valid herein (M. mexicana, M. zeledoni, M. isthmica, M. robinsoni, M. xerophila, M. simonsi, M. rubra), we describe and illustrate diagnostic external and craniodental characters, tabulate measurement data from adult specimens, list all known examples of sympatry, and map geographic ranges based on specimens examined. The species newly recognized as valid herein, all of which occur in Central America and/or northwestern South America, substantially increase the known diversity of trans-Andean mouse opossums, but it is not currently known

whether or not these represent a distinct radiation within the genus Marmosa.

INTRODUCTION

Species of the genus Marmosa, commonly known as mouse opossums (fig. 1), are long- tailed, black-masked, pouchless didelphid marsupials that inhabit a wide range of tropical and subtropical habitats from Mex- ico to Argentina. Marmosa was last revised by Tate (1933), who recognized several species groups that have subsequently been elevated to generic rank (table 1). In the classification proposed by Gardner and Creighton (1989), the species in Tate’s ‘““Cinerea Group” were referred to the genus Micoureus Lesson, 1842; those in his ‘“‘Mur- ina Group” to Marmosa Gray, 1821; those in his “Noctivaga Group” to Marmosops Matschie, 1916; and those in his “‘Elegans Group” to Thylamys Gray, 1843. Most of the species in Tate’s ““Microtarsus Group” were placed in a new genus, Gracilinanus Gardner and Creighton, 1989.

Recent phylogenetic research based on molecular sequence data (e.g., Patton et al., 1996; Jansa and Voss, 2000; Steiner et al., 2005) has convincingly indicated that Mar- mosa (sensu Tate) was polyphyletic, and the same studies have consistently supported the monophyly of Marmosops, Micoureus, and Thylamys as those taxa were recognized by Gardner and Creighton (1989). However, a new genus was proposed for ‘“‘Marmosa”’ canescens by Voss and Jansa (2003), and other new genera were later described for two clades formerly concealed by synonymies

within Gracilinanus (see Voss et al., 2004, 2005).

Despite these refinements, the taxonomic status of Marmosa remains problematic because all molecular phylogenies published to date indicate that the genus (as understood by Gardner and Creighton, 1989) is para- phyletic with respect to Micoureus (fig. 2). Obviously, several alternative classifications would be consistent with such results: either (1) Micoureus could be regarded as a junior synonym of Marmosa; or (2) Micoureus could be regarded as a valid subgenus of Marmosa; or (3) Marmosa could be restricted to M. murina (the type species). Of these, the first option would result in the loss of a useful and familiar name for a well-supported clade (Micoureus), whereas the second and third alternatives would require that additional subgenera or genera be resurrected from synonymy or described as needed to contain the other species currently referred to Mar- mosa.

The interim solution proposed by Voss and Jansa (2009), which we adopt herein, is to recognize Micoureus as a subgenus of Marmosa, and to refer all of the species formerly included in Marmosa to the nomi- notypical subgenus. In effect, this tactic simply moves the problem of paraphyly from the generic level (where it affects binomial usage) to the subgeneric level (where it does not). Although clearly suboptimal, no further progress in the classification of this complex

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Fig. 1.

Marmosa zeledoni, photographed at La Selva Biological Station, Heredia province, Costa Rica,

in August 2005 by Marco Tschapka. Zeledon’s mouse opossum, formerly synonymized with M. mexicana, is resurrected as a valid species in this report. The local population at La Selva was previously reported as M. mexicana by Timm et al. (1989), Voss and Emmons (1996) and Sperr et al. (2009).

is possible until the phylogenetic relation- ships among all of the included species are worked out. To date, only five of the nine currently recognized species in the subgenus Marmosa are represented in published trees, and there is reason to believe that additional valid species may be concealed among the putative synonyms of several geographically widespread forms (table 2). Two of the latter are the primary focus of this report.

As currently recognized, Marmosa robin- soni includes 13 nominal taxa, of which Tate (1933) treated four as valid species belonging to his “‘Mitis Section”: M. chapmani, M.

mitis, M. ruatanica, and M. simonsi. All of these were swept into synonymy by Hersh- kovitz (1951), who alleged that the diagnostic characters mentioned by Tate were artifacts of sexual dimorphism, age, imperfect preser- vation, or clinal variation. Although Hersh- kovitz provided no analyses of data to support these claims, his conclusions were accepted by subsequent compilers of influen- tial checklists (e.g., Cabrera, 1958; Hall and Kelson, 1959). The nominal taxa of Tate’s Mitis Section (for which M. robinsoni is the oldest available binomen; Cabrera, 1958) extend from Honduras southward to Pana-

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TABLE 1 Tate’s (1933) Groups and Sections of Marmosa and Their Current Classification*

Tate’s name Current name

Cinerea Group Marmosa (Micoureus)

Murina Group

Marmosa (Marmosa, part) Marmosa (Marmosa, part) Marmosa (Marmosa, part) Tlacuatzin

Murina Section Mitis Section Mexicana Section Canescens Section

Noctivaga Group Marmosops (part)

Microtarsus Group

Cryptonanus, Gracilinanus

Marmosa (Marmosa, part), Marmosops (part)

Microtarsus Section Lepida Section

Elegans Group Chacodelphys, Thylamys

* After Voss and Jansa (2009).

ma, Peru, Venezuela, and the Lesser Antilles (Hall, 1981; O’Connell, 1983; Creighton and Gardner, 2008).

According to recent phylogenetic results (fig. 2), Marmosa mexicana 1s closely related to M. robinsoni. Like the latter, it also includes several nominal taxa that are cur- rently treated as synonyms or subspecies, but in this case the current taxonomy follows Tate’s (1933) revision. The distribution of M. mexicana is less extensive than that of M. robinsoni, but it still extends over 2000 km, from Mexico to Panama (Hall, 1981).

Few nonvolant small mammals have geographic distributions in Central and South America as extensive as those currently attributed to Marmosa robinsoni and M. mexicana. The range of habitats occupied by each of these species is likewise remark- able, and even a superficial examination of allegedly conspecific skins and skulls reveals a surprising degree of morphological varia- tion. Preliminary sorting of specimens at the American Museum of Natural History by D.P.L. during a recuration project in the early 1990s suggested that at least some of the species in Tate’s (1933) Mitis Section were valid (contra Hershkovitz, 1951), and this conclusion was independently reached by R.V.R. after a much more extensive study of material in other museums.

ROSSI ET AL.: REVISION OF MARMOSA 5

This report, which is largely based on R.V.R.’s thesis research at the Universidade de Sao Paulo (Rossi, 2005), summarizes our conclusions regarding the taxonomy of spe- cies belonging to Tate’s (1933) Mitis Section and his “Mexicana Section.’ To this we append redescriptions of Marmosa xerophila Handley and Gordon, 1979, and M. rubra Tate, 1931. The former is a northern South American form that is morphologically similar to M. robinsoni, whereas the latter is a western Amazonian species that consistent- ly appears as the sister taxon of M. robinsoni + M. mexicana in phylogenetic analyses of molecular sequence data (e.g., Voss and Jansa, 2003, 2009; Jansa et al., 2006; Jansa and Voss, 2005). Despite these indications, it is not our assumption that all of the species treated in this report form a natural group. Among other pertinent issues, the monophy- ly of Tate’s “sections” has not been tested, but distinguishing the valid species that each contains is a necessary step toward a genuinely phylogenetic classification of mouse opossums.

Materials and Methods

SPECIMENS: We examined 1481 specimens for this report, most of which are preserved as skins and skulls in the following institutional collections: AMNH, American Museum of Natural History (New York); BMNH, Nat- ural History Museum (London); FMNH, Field Museum of Natural History (Chicago); MCZ, Museum of Comparative Zoology, Harvard University (Cambridge); MSB, Mu- seum of Southwestern Biology, University of New Mexico (Albuquerque); MVZ, Museum of Vertebrate Zoology, University of Califor- nia (Berkeley); ROM, Royal Ontario Muse- um (Toronto); and USNM, National Muse- um of Natural History (Washington, D.C.).

ANATOMICAL TERMINOLOGY: Our names for external and craniodental structures of Marmosa follow Voss and Jansa (2009), whose anatomical descriptors are largely consistent with standard usage (Brown, 1971; Brown and Yalden, 1973; Bown and Kraus, 1979; Wible, 2003). Principal features of the skull are illustrated in figures 3 and 4. We follow Clemens (1966) in using positional criteria for naming cusps on the stylar shelf

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other didelphids

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Marmosa mexicana Marmosa isthmica Marmosa rubra Micoureus demerarae Micoureus paraguayanus Micoureus regina Marmosa murina

Marmosa lepida

Fig. 2. Phylogenetic relationships of Marmosa (sensu Gardner and Creighton, 1989) and Micoureus (treated as a subgenus of Marmosa in this report) based on a maximum-parsimony analysis of 7449 characters (including morphology, karyotypes, and sequence data from five nuclear genes; Voss and Jansa, 2009) scored for 43 species of Recent didelphids and seven nondidelphid outgroups. The numbers above and below each branch represent nonparametric bootstrap frequencies and Bremer support values, respectively. Marmosa isthmica (revalidated in this report) is the correct name for the terminal taxon labelled Marmosa robinsoni in previous analyses of these data. Marmosa murina is the type species

of Marmosa.

of the upper molars (not treated in detail by Voss and Jansa, 2009) as follows:

Stylar cusp A (styA): A small cusp (often indistinct) at the anterior end of the stylar shelf anterolabial to the paracone, to which it is Sometimes connected by the preparacrista (= “‘parastyle’’ of authors).

Stylar cusp B (styB): A much larger cusp (almost always distinct) posterior to styA (if present) and labial to the paracone, to which it is sometimes connected by the prepara- crista (= “‘stylocone’’ of authors).

Stylar cusp(s) C (styC): One or two small cusps (sometimes indistinct or absent) poster- olabial to the paracone and anterolabial to the metacone.

Stylar cusp D (styD): Usually single and sometimes indistinct in Marmosa, this cusp is posterolabial to the metacone, to which it is never directly connected.

Stylar cusp E (styE): A small cusp (often indistinct) at the posterior end of the stylar shelf posterolabial to the metacone, to which it is always connected by the postmetacrista (= “metastyle,” “‘distostyle,” ‘“‘metastylar spur,” or “‘metastylar corner” of authors).

MEASUREMENTS: We recorded external measurements (in millimeters, mm) and weight (in grams, g) from specimen labels.

The former include total length (TL), length of tail (LT), length of hind foot (HF), and length of ear (Ear). Length of head-and-body (HBL) was calculated by subtracting LT from TL.

We measured the following 29 cranioden- tal dimensions to the nearest 0.01 mm with digital calipers while specimens were viewed at low magnification under a stereomicro- scope. Except as noted, anatomical endpoints are illustrated in figures 5 and 6.

Greatest Length of Skull (GLS): From the anteriormost point of the premaxillae to the posteriormost point of the braincase.

Condylobasal Length (CBL): From the occipital condyles to the anteriormost point of the premaxillae.

Rostral Length (RL): From the anterior- most point of the nasals to the ventralmost lacrimal foramen.

Nasal Length (NL): The greatest length of either the right or left nasal bone (whichever is longest).

Palatal Length (PL): From the anterior- most point of the premaxillae to the postero- lateral corner of the postpalatine torus.

Length of Maxillary Tooth Row (MTR): From the anterior surface of the base of the upper canine to the posterior margin of M4.

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TABLE 2

Currently Recognized Species of Marmosa (Marmosa)*

M. andersoni Pine, 1972

M. lepida (Thomas, 1888) Synonym: grandis Tate, 1931 M. mexicana Merriam, 1897

mayensis Osgood, 1913 savannarum Goldman, 1917 zeledoni Goldman, 1917°

Synonyms:

M. murina (Linnaeus, 1758)

bombascarae Anthony, 1922

chloe Thomas, 1907

dorsigera (Linnaeus, 1758)

duidae Tate, 1931

guianensis (Kerr, 1792)

klagesi J.A. Allen, 1900

macrotarsus (Wagner, 1842)

madeirensis Cabrera, 1913

maranti Thomas, 1924

meridionalis Miranda-Ribeiro, 1936

moreiri Miranda-Ribeiro, 1936

muscula (Cabanis, 1848)

parata Thomas, 1911

roraimae Tate, 1931

tobagi Tate, 1931

waterhousei (Tomes, 1860)

M. quichua Thomas, 1899 Synonym: M. robinsoni Bangs, 1898

Synonyms:

Synonyms:

musicola Osgood, 1913

casta Thomas, 1911 chapmani J.A. Allen, 1900 fulviventer Bangs, 1901 grenadae Thomas, 1911 isthmica Goldman, 1912” luridivolta Goodwin, 1961 mimetra Thomas, 1921° mitis Bangs, 1898

nesaea Thomas, 1911 pallidiventris Osgood, 1912 ruatanica Goldman, 19114 simonsi Thomas, 1899°

M. rubra Tate, 1931 M. tyleriana Tate, 1931 M. xerophila Handley and Gordon, 1979

* After Gardner (2005); synonyms include “‘subspecies.” > Recognized as a valid species in this report.

© Synonymized with M. isthmica in this report.

4 Synonymized with M. mexicana in this report.

Length of Upper Molar Series (UMS): Crown length of the upper molars, from the anterolabial margin of M1 to the posterior margin of M4.

Length of M4 (LM4): Length (anteropos- terior or mesiodistal dimension) of the fourth upper molar crown across the paracone and metacone.

Width of M2 (WM2): Greatest width (transverse dimension) of the second upper molar, from the labial margin of the crown at or near the stylar A position to the lingual apex of the protocone.

Width of M4 (WM4): Greatest width (transverse dimension) of the fourth upper molar, from the labial margin of the crown at or near the stylar A position to the lingual apex of the protocone.

Height of Upper Canine (HC): Height (vertical dimension) of Cl, from the exposed labial base to the tip of the tooth.

Palatal Breadth (PB): Measured across the labial margins of the fourth molar (M4) roots.

Postpalatal Breadth (PPB): Least breadth across the anterior processes of the left and right alisphenoids (not illustrated).

Breadth of Basicranium (BB): The least distance between the anteromedial margins of the right and left alisphenoid tympanic processes.

Breadth across Tympanic Bullae (BTB): The greatest distance across the lateral margins of the right and left alisphenoid tympanic processes.

Length of Tympanic Bulla (LTB): From the anterior curvature of the alisphenoid tympanic process to the posteriormost point of the petrosal pars cochlearis.

Tympanic Bulla Opening (TBO): The distance between the alisphenoid tympanic process and the rostral tympanic process of the petrosal, measured across the medial margin of ectotympanic.

Width of Ectotympanic (WET): Greatest width of the ectotympanic (not illustrated).

Nasal Breadth (NB): Measured across the triple-point sutures of the nasal, frontal, and maxillary bones on each side.

Breadth of Rostrum across Canines (BRC): Measured across the labial bases of the upper canines.

Breadth of Rostrum between Jugals (BRJ): Measured across the triple-point sutures of

za

Frg: 3.

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Dorsal and ventral cranial views of Marmosa murina showing principal osteological features

mentioned in the text. Abbreviations: als, alisphenoid; atp, alisphenoid tympanic process; bo, basioccipital; bs, basisphenoid; ec, carotid canal; ect, ectotympanic; fm, foramen magnum; fpj, frontal process of jugal; fro, frontal; gf, glenoid fossa; gpa, glenoid process of alisphenoid; ip, interparietal; jug, jugal; lac, lacrimal; max, maxillary; mp, mastoid process (of petrosal); nas, nasal; occ, occipital condyle (of exoccipital); of, orbital fossa; pal, palatine; par, parietal; pef, paracanine fossa; pogp, postglenoid process (of squamosal); pop, postorbital process; pre, premaxillary; prgp, preglenoid process (of jugal); pro, promontorium (of petrosal); ps, presphenoid; pt, pterygoid; rtp, rostral tympanic process (of petrosal); sq, squamosal; tef, transverse canal foramen; tf, temporal fossa; za, zygomatic arch.

the jugal, lacrimal, and maxillary bones on each side.

Least Interorbital Breadth (LIB): Mea- sured at the narrowest point across the frontals between the orbits (anterior to the postorbital processes, if any).

Postorbital Constriction (POC): Measured at the narrowest point across the frontals between the temporal fossae (posterior to the postorbital processes, if present).

Breadth of Braincase (BBC): Measured immediately above the zygomatic process of the squamosal on each side.

Zygomatic Breath (ZB): Greatest breadth across the zygomatic arches.

Length of Mandible (LM): Measured from the anteriormost point of the mandible (medial to the alveolus of il) to the posteri- ormost point of the angular process.

Length of Lower Molar Series (LMS): Crown length of the lower molars, from the anterolingual margin of ml to the poster- olingual margin of m4.

Length of m4 (Lm4): Length (anteropos- terior or mesiodistal dimension) of m4, from the paraconid to the hypoconulid.

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ROSSI ET AL.: REVISION OF MARMOSA 9

mef

Fig. 4. Left lateral cranial and mandibular views of Marmosa murina showing principal osteological features mentioned in the text. Abbreviations: als, alisphenoid; ap, angular process; atp, alisphenoid tympanic process; conp, condylar process; corp, coronoid process; ect, ectotympanic; exo, exoccipital; fpj, frontal process of jugal; fr, foramen rotundum; fro, frontal; hpp, hamular process of pterygoid; iof, infraorbital foramen; ip, interparietal; jug, jugal; lac, lacrimal; Ie, lambdoid crest; If, lacrimal foramina; maf, masseteric fossa; max, maxillary; mef, mental foramina; nas, nasal; pal, palatine; par, parietal; pe, pars cochlearis (of petrosal); pef, paracanine fossa; pm, pars mastoideus (of petrosal); pop, postorbital process; pre, premaxillary; rmf, retromolar fossa; sq, squamosal; ssf, subsquamosal foramen; sup, supraoccipital;

zps, zygomatic process of squamosal.

Width of m2 (Wm2): Greatest width (transverse dimension) of m2, measured across the hypoconid and entoconid (not illustrated).

AGE CRITERIA: The age classification employed in this report is a refinement of that proposed by Tribe (1990), which was based on the pattern of tooth eruption that he observed in Marmosops incanus and other small didelphids (including Marmosa). In these taxa, the deciduous third upper premo- lar (dP3) is not replaced until M4 has erupted; therefore, P3 is the last upper tooth to erupt. Animals belonging to Tribe’s age class 5 have a completely erupted upper molar dentition (M1-4), but dP3 is either unreplaced or P3 is just starting to erupt. Animals belonging to Tribe’s age class 6 have shed dP3, P3 is almost completely erupted, and M4 is slightly worn; specimens in Tribe’s age class 7 have P3 fully erupted, and M4 is considerably worn.

In the course of this study, we observed substantial ontogenetic variation among con- specific specimens assignable to Tribe’s age classes 6 and 7. In order to take this variation into account for the purpose of taxonomic comparisons, we found it useful to redefine age classes 6 and 7 and to recognize two additional age classes as follows.

Age class 6: Labial cingulum of P3 emergent but slightly dorsal to labial cingu- lum of P2 (indicating the penultimate stage of P3 eruption); M3 and M4 cristae unworn or with very narrow and discontinuous strips of exposed dentine.

Age class 7: Labial cingulum of P3 aligned with or ventral to labial cingulum of P2 (indicating the complete eruption of P3); dentine narrowly exposed on all or most M3 and M4 cristae.

Age class 8: Labial cingulum of P3 aligned with or ventral to labial cingulum of P2; dentine broadly exposed along preparacrista

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MTR

Fig. 5.

of M3 but narrowly and discontinuously exposed on at least some of the other cristae of M3 and M4.

Age class 9: Labial cingulum of P3 aligned with or ventral to labial cingulum of P2; dentine broadly and continuously exposed on most M3 and M4 cristae.

Hereafter, specimens belonging to age class 5 are called subadults, and specimens belonging to age classes 6 to 9 are called

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149

VIM

Anatomical endpoints of 21 craniodental measurements of Marmosa defined in the text.

adults. We additionally distinguish “‘young adults’ (specimens in age class 6) from ‘““mature adults’’ (in age classes 7 to 9).

ONTOGENETIC VARIATION AND SEXUAL DIMORPHISM

Like other didelphid marsupials (Gardner, 1973; Abdala et al., 2001; Flores et al., 2003), young mouse opossums are weaned long

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ROSSI ET AL.: REVISION OF MARMOSA 1

Fig. 6. Anatomical endpoints of five additional craniodental measurements of Marmosa defined in

the text.

before they are morphologically mature, with the result that mixed-age series of conspecific individuals often include specimens that differ conspicuously in size and size-correlat- ed (allometric) proportions. Because imma- ture (juvenile and subadult) individuals seldom exhibit all the diagnostic traits that allow confident taxonomic identifications of adults, careful attention to dental indicators of morphological maturity is important. However, substantial morphometric varia- tion exists even among conspecific adults that differ in age and sex.

Statistical tests for age and sex effects on craniodental measurements of adult speci- mens reveal similar patterns of nongeo- graphic variation in all species for which large samples were analyzed (Rossi, 2005). In particular, statistically significant age effects

were detected for most measured dimensions, with the usual exception of molar measure- ments (e.g., UMS, LM4, WM2, WM4, LMS, Lm4, Wm2) and measurements of auditory structures (e.g., LTB, TBO, WET). Almost all dimensions with significant age effects show progressive increases in measurement means from age class 6 to age class 9, indicating that older specimens are, on average, larger than younger specimens. (An exception is Postorbital Constriction [POC], which sometimes exhibits a statistically sig- nificant decrease in mean values with age.) In general, the largest age-correlated increases are seen in measurements spanning the rostrum (e.g., GLS, CBL, RL, PL, BRC, BRJ) and the zygomatic arches (ZB), but Least Interorbital Breadth (LIB), and Length of Mandible (LM) sometimes also exhibit

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strong age effects. Height of Canine (HC) often exhibits a much stronger age effect in males than in females.

Statistical tests for sexual dimorphism are often significant when sample sizes are large (Rossi, 2005), but mean differences between conspecific males and females are minimal for molar and auditory dimensions, some basicranial measurements (e.g., PPB), and Postorbital Constriction (POC). Males are larger, on average, than females in all measurements that exhibit pronounced sexu- al dimorphism—which tend to be those that also show strong age _ effects—especially rostral dimensions, zygomatic breadth, and canine height.

The net result of ontogenetic variation and sexual dimorphism in mouse opossums is that valid taxonomic comparisons of affected craniodental dimensions must take age and sex into account. Although this is often true of other mammals, the magnitude of onto- genetic variation and sexual dimorphism in didelphids are sometimes large enough that conspecific samples differing in age and sex can have nonoverlapping ranges of variation. Condylobasal Length (CBL), for example, ranges from 32.1 to 38.6 mm in young adult (age class 6) female Marmosa isthmica, but the observed range in this dimension among old adult (age class 9) male M. isthmica is 39.8 to 43.6 mm. Additionally, because some dimensions are strongly affected by growth and sexual dimorphism while others are not, cranial proportions also vary among conspe- cific individuals. Thus, mature adult males tend to have proportionately smaller molars and auditory structures but much _ larger canines, longer rostrums, and more flaring zygomatic arches than young adult females.

Although multivariate statistical methods are available to adjust morphometric com- parisons of species for age and sex effects, such methods are cumbersome for the purpose of identifying specimens. Instead, taxonomic identifications are more readily based on qualitative characters, which may vary with age and sex but do not require measurement or statistical analysis. In this report, measurement data play a secondary role because they are seldom necessary or sufficient for distinguishing the species of interest.

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COMPARATIVE MORPHOLOGY

The qualitative external and craniodental characters analyzed in the course of this study are described below. To avoid unnec- essary confusion, we refer to species of Marmosa as subsequently diagnosed herein (i.e., treating M. isthmica, M. simonsi, and M. zeledoni as valid binomials). Unrevised con- geners, however, are referred to, when necessary, by their currently accepted names (as in table 2). Except as noted otherwise, all examined species of Marmosa conform to the morphological description of the genus pro- vided by Voss and Jansa (2009), which should be consulted for information about taxonomically invariant external and cranio- dental features that are not mentioned in the following accounts.

External Characters

External morphology provides several use- ful characters for diagnosing species of the subgenus Marmosa. Although most details of pelage pigmentation are effectively preserved on dry skins, some colors that are vivid in life fade away and eventually disappear on museum specimens (Pine et al., 1985). Be- cause this report is based largely on exami- nation of museum specimens, we seldom had the opportunity to record such “fugitive” colors, which are not further considered here.

HEAD PELAGE: The middorsal fur of the rostrum (between the dark circumocular masks) is conspicuously paler than the fur of the crown of the head (between the ears) in some species of Marmosa. Among the species treated herein, this pigmental contrast is usually sharpest in M. mexicana, M. robin- soni, M. simonsi, and M. rubra. It is weakest and least often developed in M. zeledoni, and it is variably present or absent in M. isthmica and M. xerophila.

A dark median stripe that extends from the rhinarium to between the eyes—bisecting the pale midrostral fur—is consistently present in M. rubra (fig. 7, right). Somewhat resembling the median stripe of dark rostral fur de- scribed by Voss and Jansa (2003: character 2) for Caluromys, this trait is usually absent or inconspicuous in other species of Marmosa (e.g., M. zeledoni; fig. 7, left).

2010

ROSSI ET AL.: REVISION OF MARMOSA 13

Fig. 7.

Dorsal views of skins illustrating taxonomic variation in rostral pelage markings. A dark

middorsal rostral stripe is absent in Marmosa zeledoni (left, FMNH 128398) but present in M. rubra (right,

AMNH 68137). Scale bar = 1 cm.

The fur surrounding the eye is dark brown or blackish in all species of Marmosa, resulting in a masklike marking that con- trasts abruptly with the paler (brownish, grayish, or whitish) coloration of the mid- rostrum, crown, and cheeks. In most exam- ined specimens, this circumocular mask extends anteriorly among the bases of the mystacial vibrissae, where the dark fur gradually narrows and fades away, becoming less and less distinct toward the rhinarium. In some species, dark fur extends only a few millimeters behind the eye; in such forms (e.g., M. isthmica, M. robinsoni, M. rubra, M. xerophila), several millimeters of paler, brownish fur separate the mask from the base of the ear (fig. 8, bottom). In other species, however, dark fur extends much farther posteriorly, so that the mask reaches the base of the ear; among the species treated herein, this trait is best developed in M. mexicana (fig. 8, top), but it is also seen to a variable extent in M. zeledoniand M. simonsi.

BopDy PELAGE: Although species of Mar- mosa (Marmosa) vary subtly in fur texture, perceived differences in pelage density and softness are somewhat subjective and do not provide a satisfactory basis for identification. Regardless of texture, the coat consists of cover hairs and guard hairs. The former are more abundant, wavy, and range from 7 to

11 mm in length. On the dorsal surface of the body, coat hairs are tricolored, with a basal gray band that makes up some 60% to 90% of the total length of each hair; a short buffy, yellowish, or reddish subterminal band; and a tiny dark-brown terminal band. Guard hairs are sparser and straighter than coat hairs, and range from 9 to 14 mm in length. Dorsal guard hairs are bicolored, grayish basally and paler near the tip.

Dorsal fur color is taxonomically variable in the subgenus Marmosa, but species differ- ences are difficult to characterize by objective standards. Whereas much of the older litera- ture made frequent reference to Ridgway’s (1912) color standards, Ridgway’s esoteric

nomenclature—‘‘Sayal Brown,” “Hair by)

Brown,” ‘‘Mars Brown,” ‘“‘Pecan Brown,”

by) ) by)

“Mikado Brown,” ‘“‘Natal Brown,” ‘“‘San-

ford’s Brown,’ and “Burnt Sienna’ are examples of color names that Tate (1933) used to describe the dorsal pelage of Mar- mosa—is not helpful without a copy of this rare book in hand,’ so more easily compre- hensible vernacular descriptors (e.g., “‘reddish brown’’) are preferable in most circumstanc-

* Without examining Ridgway’s plates, for example, it is not clear that “Burnt Sienna” and “‘Sanford’s Brown” are almost indistinguishably similar shades of reddish brown. The degree to which the color swatches in this book have faded in the ninety- odd years since it was published is unknown.

14 BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY

Fig. 8. taxonomic variation in facial markings. The dark circumocular mask extends posteriorly to the base of the ear in Marmosa mexicana (top, MVZ 130251), but not in M. robinsoni (bottom, AMNH 130579). Scale bar = 1 cm.

Lateral views of skins illustrating

es. Taxonomic color differences are primarily useful in side-by-side comparisons, where they are sometimes decisive for identification.

Among the species treated in this report, M. simonsi has much grayer fur than the others, whereas most specimens of WM. mexicana, M. zeledoni, and M. rubra are distinctly reddish. Marmosa xerophila could appropriately be described as pale grayish brown, M. robinsoni as yellowish brown, and M. isthmica as orangish brown. Typically, the dorsal fur is darker and more richly colored on the middle of the back than along the flanks, which tend to be slightly paler. Juvenile and subadult specimens usually have grayer and/or darker dorsal fur than adults. Young adults often have longer, softer, more brightly colored, and glossier coats than old adults, which often have dull and shabby- looking fur.

The ventral pelage of most species consists of both self-colored (unicolored) and gray- based (bicolored) fur. In most of the species treated in this report, self-colored fur—which

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may be orange, yellowish, or whitish— extends continuously along the ventral mid- line from the chin to the anus. Usually, however, the width of this pale self-colored median streak (when present) is narrowed by darker lateral zones of gray-based ventral hairs, the tips of which are either colored like the flanks or like the self-colored median streak. The lateral zones of gray-based ventral hairs may be restricted to the abdomen (as in M. isthmica and M. xero- phila), or they may extend from the throat or chest to the inguinal region, including the ventral surfaces of the fore- and hind limbs (as in M. mexicana, M. zeledoni, M. robin- soni, and M. rubra). Indeed, the median streak of self-colored fur is sometimes dis- continuous in M. rubra because it is inter- rupted by gray-based abdominal fur. By contrast, the entire ventral surface (except for the chin and throat) is covered with gray- based hairs in M. simonsi.

In reproductively active adult females, the fur of the inguinal-abdominal region be- comes remarkably modified. Ordinary ven- tral fur in such animals is replaced by a distinctively short, thin, sparse, brownish mammary pelage. Although the color and extent of the mammary pelage varies among conspecific specimens, some taxonomic dif- ferences are also apparent (table 3).

EARS: The external ear or pinna is a prominent, membranous organ in Marmosa. Among the species treated herein, the ears are largest in M. isthmica, M. robinsoni, M. simonsi, and M. xerophila (averaging 25-— 26 mm in adult males; 24-25 mm in adult females; tables 4, 5) and smallest in ™. mexicana, M. zeledoni, and M. rubra (22- 23 mm in males, 20—22 mm in females). The internal and external surfaces of the ears are macroscopically naked, but a sparse covering of short hairs is visible under low magnifica- tion. The exposed auricular skin ranges in color from pale brown to dark brown, and it is usually more heavily pigmented distally than basally.

GULAR GLAND: In most species of Mar- mosa there is a distinct median patch of glandular (naked or sparsely haired) skin between the chest and the throat (Tate, 1933; Barnes, 1977). Although this gland is usually best developed in adult males, it is also visible in

2010 ROSSI ET AL.: REVISION OF MARMOSA 15 TABLE 3 Reproductive Features of Female Marmosa* Mammae? Litter size° Color of mammary fur

M. mexicana 5-1-5 = 11 (2) 12 Intensely golden to reddish brown

6-1-6 = 13 (1)

7-1-7 = 15 (1) M. zeledoni 4-1-4 = 9 (1)

5-1-5 = 11 (1) M. isthmica 8.5 (6-12) Light or dark reddish brown M. robinsoni 6-1-6 = 13 (1) 11 (2-19) Intensely golden to reddish brown M. xerophila 5-1-5 = 11 (1) 9 (6-12) Golden M. simonsi M. rubra 3-1-3 = 7 (1)

4-1-4 = 9 (1)

* Mammary formula as defined in the text.

> Data gathered from stuffed or fluid-preserved specimens. In parentheses, the number of specimens examined. © Median (minimum—maximum) number of nursing young, recorded by collectors on specimen labels.

most subadult and female specimens. Among the species treated in this report, only M. rubra consistently lacks any external evidence of glandular activity in the gular region. CARPAL TUBERCLES: Large tubercles, supported internally by carpal ossifications, project from the lateral and medial surfaces of the wrist in mature adult male specimens of all the Marmosa species treated in this report (other species, such as M. murina, lack carpal tubercles). The medial (or “‘radial’’) tubercle, which is supported internally by the prepollex (Lunde and Schutt, 1999), exhibits noteworthy taxonomic variation that can be recorded from suitably preserved dried skins. In M. mexicana (fig. 9A), the medial carpal tubercle is long, extending to the base of the pollex (manual digit I), and uniform in thickness (without distinguishable segments). By contrast, the long medial carpal tubercles of M. zeledoni (fig. 9B) and M. isthmica are divided by a shallow sulcus into similar but consistently recognizable proximal and distal parts. In the remaining species treated here— M. robinsoni, M. simonsi (fig. 9C), ™. xerophila, and M. rubra—medial carpal tubercles can be long or short (not reaching the base of pollex), but they are more conspicuously segmented into globular prox- imal and comma-shaped distal parts. MAMMAE: Because species of Marmosa are pouchless, the mammae of lactating

females are exposed. Confined to the abdom- inal/inguinal region, these form a more or less circular abdominal/inguinal pattern that en- closes an unpaired median teat (see Tate, 1933 [fig. 3] for an illustration of the mammae in M. mexicana). By convention, didelphid mammary complements are sum- marized by formulae representing the right- side (R), median (M), left-side (L), and total (T) teat counts in the format R-M-L = T. Mammary formulae vary taxonomically, but they also exhibit variation among conspecific individuals (table 3). In M. mexicana, from which we obtained mammary counts of four individuals, the number of teats ranges from 11 to 15, a range of variation that overlaps the teat numbers observed from most of the other species treated herein. Only M. rubra (with 7 to 9 mammae) seems like an outlier, but no definite conclusions are possible with such small sample sizes. Although we were not able to find any stuffed or fluid specimen of M. isthmica with countable mammae, a skin label recording 12 nursing young sug- gests a mammary count of at least 6-1-6 = 13 for this species. No information is available about mammary formulae or litter sizes for M. simonsi.

TAIL: A slender, muscular organ in Mar- mosa, the tail is always longer than the combined length of the head and body, but the ratio of tail length to head-and-body

TABLE 4 Summary Statistics" for External Measurements (mm) and Weights (g) of Adult Male Specimens of Seven Species of Marmosa

16

zeledoni isthmica robinsoni xerophila simonsi rubra

mexicana

BULLETIN AMERICAN MUSEUM OF NATURAL HISTORY

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