Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2020-12-02

Taxonomic review of the slender mouse opossums of the “Parvidens” group from Brazil (Didelphimorphia: Didelphidae: Marmosops), with description of a new species

Laboratório de Mastozoologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Av. Fernando Corrêa da Costa, 2367, Cuiabá, Mato Grosso 78060–900, Brazil Programa de Pós-Graduação em Zoologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Cuiabá, Mato Grosso, Brazil
Laboratório de Ecologia e Zoologia de Vertebrados – Mastozoologia, ICB, Universidade Federal do Pará, Belém, Pará, Brazil
Laboratório de Mastozoologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Av. Fernando Corrêa da Costa, 2367, Cuiabá, Mato Grosso 78060–900, Brazil
Laboratório de Mastozoologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Av. Fernando Corrêa da Costa, 2367, Cuiabá, Mato Grosso 78060–900, Brazil Programa de Pós-Graduação em Zoologia, Instituto de Biociências, Universidade Federal de Mato Grosso, Cuiabá, Mato Grosso, Brazil
Mammalia Marsupial Taxonomy Amazonia Cerrado

Abstract

The genus Marmosops comprises small marsupials of the family Didelphidae (≤ 200 g), widely distributed in a variety of lowland rainforest and montane forest habitats, extending from Panama to southern Bolivia and southeastern Brazil. The smallest species of the genus are included in the “Parvidens” group, which includes M. pakaraimae, M. parvidens and M. pinheiroi. Although the monophyly of this group and species relationships are well defined, molecular studies have indicated that M. pinheiroi may represent a species complex, which has never been tested based on morphological analysis. In this study, we present the taxonomic review of M. pinheiroi based on the largest sample ever analyzed of this species. The external and craniodental morphology of 613 specimens of M. parvidens and M. pinheiroi from the northern, eastern, central and southern Brazilian Amazonia and northern Cerrado were examined. Besides, 28 craniodental dimensions were measured from adult specimens to support univariate and multivariate statistical analyses. Our results corroborate the validity of M. parvidens and indicate that M. pinheiroi is a complex formed by three species – M. pinheiroi (s. s.), distributed to the north of the Amazon River, from eastern Venezuela to the state of Amapá in Brazil; M. woodalli, which occurs east of the Xingu river and in the Marajó Island, state of Pará, extending to the east in the states of Tocantins and Maranhão; and a new species that occurs from the left bank of the Madeira River to the left bank of the Xingu River, herein described. Although the great morphometric similarity, species of the M. pinheiroi complex tended to be more different from each other than to M. parvidens in both univariate and multivariate analyses. Morphologically, these species may be positively distinguished by unique combinations of characters, such as dorsal and ventral fur coloration, arrangement of gray based hairs on the venter, supraoccipital shape, development of anterior and posterior portions of the M3 stylar shelf, continuity or not between the preprotocrista and anterior labial cingulum along the anterior margin of the upper molars, development of the metaconule in the upper molars, and number of cusps of the m4 talonid. The present work provides new perspectives for studies based on molecular data in order to test the species hypotheses recognized here and evaluate to what extent the Tapajós, Madeira, and Araguaia-Tocantins rivers actually isolate Marmosops populations.

 

References

  1. Astúa, D. (2010) Cranial sexual dimorphism in New World marsupials and a test of Rensch’s rule in Didelphidae. Journal of Mammalogy, 91 (4), 1011–1024.

    https://doi.org/10.1644/09-MAMM-A-018.1

    Ávila-Pires, T.C.S. (1995) Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen, 299, 1–706.

    Bates, J.M., Haffer, J. & Grismer, E. (2004) Avian mitochondrial DNA sequence divergence across a headwater stream of the Rio Tapajós, a major Amazonian river. Journal of Ornithology, 145, 199–205.

    https://doi.org/10.1007/s10336-004-0039-4

    Burney, C.W. & Brumfield, R.T. (2009) Ecology predicts levels of genetic differentiation in neotropical birds. The American Naturalist, 174, 358–368.

    https://doi.org/10.1086/603613

    Cracraft, J. (1983) Species concepts and speciation analysis. In: Johnston R.F. (Ed.), Current Ornithology. Vol. 1. Springer, New York, New York, pp. 159–187.

    https://doi.org/10.1007/978-1-4615-6781-3_6

    Cracraft, J. (1985) Historical biogeography and patterns of differentiation within the South American avifauna: areas of endemism. Ornithological Monographs, 36, 49–84.

    https://doi.org/10.2307/40168278

    Creighton, G.K. (1984) Systematic studies opossums (Didelphidae) and rodents (Cricetidae). Unpublished Ph. D. dissertation, University of Michigan, Ann Arbor, Michigan, xi + 220 pp.

    Da Silva, N.J. Jr. & Sites, J.W. Jr. (1995) Patterns of diversity of neotropical squamate reptiles species with emphasis on the Brazilian Amazon and the conservation potential of indigenous reserves. Conservation Biology, 9 (4), 873–901.

    https://doi.org/10.1046/j.1523-1739.1995.09040873.x

    Díaz-Nieto, J.F. & Voss, R.S. (2016) A revision of the didelphid marsupial genus Marmosops, part 1. Species of the subgenus Sciophanes. Bulletin of the American Museum of Natural History, 402 (334), 1–70.

    https://doi.org/10.1206/0003-0090-402.1.1

    Díaz-Nieto, J.F., Jansa, S.A. & Voss, R.S. (2016) DNA sequencing reveals unexpected Recent diversity and an ancient dichotomy in the American marsupial genus Marmosops (Didelphidae: Thylamyini). Zoological Journal of the Linnean Society, 176 (4), 914–940.

    https://doi.org/10.1111/zoj.12343

    Fouquet, A., Courtois, E.A., Baudain, D. & Lima, J.D. (2015) The trans-riverine genetic structure of 28 Amazonian frog species is dependent on life history. Journal of Tropical Ecology, 31 (4), 361–373.

    https://doi.org/10.1017/S0266467415000206

    Flores, D.A. (2004) [Review of] Atlas of New World marsupials. Mastozoologia Neotropical, 11 (1), 133–136.

    Gardner, A.L. & Creighton, G.K. (1989) A new generic name for Tate’s (1933) Microtarsus group of South American mouse opossums (Marsupialia: Didelphidae). Proceedings of the Biological Society of Washington, 102 (1), 3–7.

    https://www.biodiversitylibrary.org/part/45891

    Gardner, A.L. (1993) Order Didelphimorphia. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal species of the world. 2nd Edition. The Smithsonian Institution Press, Washington, D.C., pp. 15–24.

    Gardner, A.L. & Creighton, G.K. (2008) Genus Marmosops Matschie, 1916. In: Gardner, A.L. (Org.), Mammals of South America. Vol. 1. Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press, Chicago and London, pp. 61–73.

    Gascon, C., Lougheed, S.C. & Bogart, J.P. (1998) Patterns of genetic population differentiation in four species of Amazonian frogs: a test of the Riverine Barrier Hypothesis. Biotropica, 30 (1), 104–119.

    https://doi.org/10.1111/j.1744-7429.1998.tb00373.x

    Gascon, C., Malcolm, J.R., Patton, J.L., da Silva, M.N.F., Bogart, J.P., Lougheed, S.C., Peres, C.A., Neckel, S. & Boag, P.T. (2000) Riverine barriers and the geographic distribution of Amazonian species. Proceedings of the National Academy of Sciences USA, 97, 13672–113677.

    https://doi.org/10.1073/pnas.230136397

    Gruber, K.F., Voss, R.S. & Jansa, S.A. (2007) Base-compositional heterogeneity in the RAG1 locus among Didelphid marsupials: implications for phylogenetic inference and the evolution of GC content. Systematic Biology, 56 (1), 83–96.

    https://doi.org/10.1080/10635150601182939

    Hayes, F.E. & Sewlal, J.A.N. (2004) The Amazon River as a dispersal barrier to passerine birds: effects of river width, habitat and taxonomy. Journal Biogeography, 31, 1809–1818.

    https://doi.org/10.1111/j.1365-2699.2004.01139.x

    Jansa, S.A. & Voss, R.S. (2000) Phylogenetic studies on didelphid marsupials I. Introduction and preliminary results from nuclear IRBP gene sequences. Journal of Mammalian Evolution, 7 (1), 43–77.

    https://doi.org/10.1023/A:1009465716811

    Jansa, S.A. & Voss, R.S. (2005) Phylogenetic relationships of the marsupial genus Hyladelphys based on nuclear gene sequences and morphology. Journal of Mammalogy, 86 (5), 853–865.

    https://doi.org/10.1644/1545-1542(2005)86[853:PROTMG]2.0.CO;2

    Jansa, S.A., Forsman, J.F. & Voss, R.S. (2006) Different patterns of selection on the nuclear genes IRBP and DMP-1 affect the efficiency but not the outcome of phylogeny estimation for didelphid marsupials. Molecular Phylogenetics and Evolution, 38 (2), 363–380.

    https://doi.org/10.1016/j.ympev.2005.06.007

    Kirsch, J.A.W. & Palma, R.E. (1995) DNA/DNA hybridization studies of carnivorous marsupials. V. A further estimate of relationships among Opossums (Marsupialia: Didelphidae). Mammalia, 59 (3), 403–425.

    https://doi.org/10.1515/mamm.1995.59.3.403

    Morais, L.J.C.L., Pavan, D., Barros, M.C. & Ribas, C.C. (2016) The combined influence of riverine barriers and flooding gradients on biogeographical patterns for amphibians and squamates in south-eastern Amazonia. Jornal of Biogeography, 43, 2113–2124.

    https://doi.org/10.1111/jbi.12756

    Mustrangi, M.A. & Patton, JL. (1997) Phylogeography and systematics of the slender mouse opossum Marmosops (Marsupialia, Didelphidae). University of California Publications, Zoology, 130, 1–86.

    Nascimento, D.C., Olímpio, A.P.M., Conceição, E., Campos, B.A., Fraga, E.C. & Barros, M.C. (2015) Phylogeny of Marmosops and the occurrence of Marmosops pinheiroi (Pine, 1981) (Didelphimorphia, Didelphidae) in the cerrado savanna of Maranhão, Brazil. Genetics and Molecular Research, 14 (1), 304–313.

    https://doi.org/10.4238/2015.January.23.4

    Oliveira, U., Vasconcelos, M.F. & Santos, A.J. (2017) Biogeography of Amazon birds: rivers limit species composition, but not areas of endemism. Scientific Reports, 7, 2992.

    https://doi.org/10.1038/s41598-017-03098-w

    Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, C.J., Allnutt, T.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P. & Kassem, K.R. (2001) Terrestrial Ecoregions of the World: A New Map of Life on Earth. BioScience, 51 (11), 933–938.

    https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Patton, J.L., dos Reis, S.F. & Silva, M.N.F. (1996) Relationships among didelphid marsupials based on sequence variation in the mitochondrial cytochrome B gene. Journal of Mammalian Evolution, 3 (1), 3–29.

    https://doi.org/10.1007/BF01454252

    Patton, J.L., Silva, M.N.F. & Malcom, J.R. (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History, 244, 1–306.

    https://doi.org/10.1206/0003-0090(2000)244<0001:MOTRJA>2.0.CO;2

    Pine, R.H. (1981) Reviews of the mouse opossums Marmosa parvidens Tate and Marmosa invicta Goldman (Mammalia: Marsupialia: Didelphidae) with description of a new species. Mammalia, 45, 55–70.

    https://doi.org/10.1515/mamm.1981.45.1.55

    Reig, O.A., Kirsch, J.A.W. & Marshall, L.G. (1985) New conclusions on the relationships of the opossum-like marsupials, with an annotated classification of the Didelphimorphia. Ameghiniana, 21, 335–343.

    Ribas, C.C., Aleixo, A., Nogueira, A.C.R., Miyaki, C.Y. & Cracraft, J. (2012) A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society B: Biological Sciences, 279 (1729), 681–689.

    https://doi.org/10.1098/rspb.2011.1120

    Rossi, R.V., Voss, R.S. & Lunde, D.P. (2010) A revision of the didelphid marsupial genus Marmosa. Part 1. The species in Tate’s “Mexicana” and “Mitis” sections and other closely related forms. Bulletin of the American Museum of Natural History, 334, 1–83.

    http://dx.doi.org/10.1206/334.1

    Rocha, R.G., Ferreira, E., Fonseca, C., Justino, J., Leite, Y.L.R. & Costa, L.P. (2014) Seasonal flooding regime and ecological traits influence genetic structure of two small rodents. Ecology and Evolution 4 (24), 4598–4608.

    https://doi.org/10.1002/ece3.1336

    Serrano-Villavicencio, J.E., Hurtado, C.M., Vendramel, R.L. & Nascimento, F.O. (2019) Reconsidering the taxonomy of the Pithecia irrorata species group (Primates: Pitheciidae). Journal of Mammalogy, 100 (1), 130–141.

    https://doi.org/10.1093/jmammal/gyy167

    Sioli, H. (1968) Hydrochemistry and geology in the Brazilian Amazon region. Amazoniana, 1, 267–277.

    Smith, B.T., Mccormack, J.E., Cuervo, A.M., Hickerson, M.J., Aleixo, A., Cadena, C.D., Pérez-Emán, J., Burney, C.W., Xie, X., Harvey, M.G., Faircloth, B.C., Glenn, T.C., Derryberry, E.P., Prejean, J., Fields, S. & Brumfield, R.T. (2014) The drivers of tropical speciation. Nature, 515, 406–409.

    https://doi.org/10.1038/nature13687

    Tate, G.H.H. (1933) A systematic revision of the marsupial genus Marmosa. Bulletin of American Museum of Natural History, 66, 1–250.

    Voss, R.S., Lunde, D.P. & Simmons, N.B. (2001) The Mammals of Paracou, French Guiana a Neotropical Lowland Rainforest Fauna Part 2. Nonvolant Species. Bulletin of the American Museum of Natural History, 263 (263), 3–236.

    http://dx.doi.org/10.1206/0003-0090(2001)263<0003:TMOPFG>2.0.CO;2

    Voss, R.S. & Jansa, S.A. (2003) Phylogenetic studies on didelphid marsupials II. Nonmolecular data and new IRBP sequences: separate and combined analyses of didelphine relationships with denser taxon sampling. Bulletin of the American Museum of Natural History, 276, 1–82.

    https://doi.org/10.1206/0003-0090(2003)276<0001:PSODMI>2.0.CO;2

    Voss, R.S., Tarifa, T. & Yensen, E. (2004) An introduction to Marmosops (Marsupialia: Didelphidae), with the description of a new species from Bolivia and notes on the taxonomy and distribution of other Bolivian forms. American Museum Novitates, 3466, 1–40.

    http://dx.doi.org/10.1206/0003-0082(2004)466<0001:AITMMD>2.0.CO;2

    Voss, R.S. & Jansa, S.A. (2009) Phylogenetic relationships and classification of didelphid marsupials, an extant radiation of New World metatherian mammals. Bulletin of the American Museum of Natural History, 322, 1–177.

    http://dx.doi.org/10.1206/322.1

    Voss, R.S., Lim, B.K., Díaz-Nieto, J.F. & Jansa, S.A. (2013) A new species of Marmosops (Marsupialia: Didelphidae) from the Pakaraima highlands of Guyana, with remarks on the origin of the endemic Pantepui mammal fauna. American Museum Novitates, 3778, 1–28.

    https://doi.org/10.1206/3778.2

    Wallace, A.R. (1854) On the monkeys of the Amazon. The Annals and magazine of natural history, Series 2, 14, 451–454.

    https://doi.org/10.1080/037454809494374