Skip to main content
SpringerLink
Log in

Phylogeny of Didelphid marsupials (Didelphimorphia) from Acre, western Amazonia

  • Original Article
  • Published:
Mammalian Biology Aims and scope Submit manuscript

A Correction to this article was published on 10 November 2022

This article has been updated

Abstract

Within the Amazon basin, the lowlands of the western Amazon stand out due to their complex geomorphological history, with their crystalline arches and several rivers, which are currently actual or potential barriers to terrestrial vertebrates’ dispersion. The western Amazonas basin can be highlighted as being the world’s richest biological hotspot. The Brazilian state of Acre, a very poorly known region located entirely within the western Amazon lowlands, is drained by two important rivers in the Amazon, the Juruá and the Purus. Here, we present the results of a survey of the didelphid marsupials collected in seven localities along these rivers, with a phylogeographic analysis based on Cytochrome b DNA sequences. We recorded high diversity, including the genera Caluromys, Didelphis, Marmosops, Marmosa (Micoureus), Metachirus, Monodelphis and Philander. Our findings detected the monophyly of some subspecies recognized for Didelphis marsupialis, Caluromys philander and Metachirus myosuros, undescribed species of Caluromys, Metachirus and Monodelphis, and geographic structure in D. marsupialis, Marmosa domina, Marmosa rutteri, Marmosops noctivagus, Marmosops bishopi, and Monodelphis peruviana, whose evolution appears to have been influenced by the complex geography of the lowlands of the western Amazon. The analyses identified population structure in relation to western Amazon, with the individuals from the upper-middle Juruá basin being separated from the Purus-lower Juruá basins in some taxa, and other rivers separating congeneric species. These analyses also revealed that western Amazonia shares more species with the Cerrado than with the Amazonian Guiana region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

Data availability

The data sets generated during the current study are available in GenBank, collected specimens were housed in IOC/Fiocruz.

Change history

References

  • Abreu-Júnior EF, Freitas MA, Lapenta MJ, Venâncio NM, França DPF, Percequillo AR (2016) Marsupials and rodents (Didelphimorphia and Rodentia) of upper Rio Acre, with new data on Oxymycterus inca Thomas, 1900 from Brazil. Check List 12:1956. https://doi.org/10.15560/12.5.1956

    Article  Google Scholar 

  • Adams J (2009) Species richness, patterns in diversity of life. Springer-Verlag, Berlin Heidelberg, Germany

    Book  Google Scholar 

  • Albert JS, Val P, Hoorn C (2018) The changing course of the Amazon River in the Neogene: center stage for Neotropical diversification. Neot Ichthyol 16(3):e180033. https://doi.org/10.1590/1982-0224-20180033

    Article  Google Scholar 

  • Allen JA (1900) Descriptions of new American marsupials. Bull Amer Mus Nat Hist 13:191–199

    Google Scholar 

  • Allen JA (1901) A preliminary study of the North American opossums of the genus Didelphis. Bull Amer Mus Nat Hist 14:149–188

    Google Scholar 

  • Anthony HE (1922) Preliminary report on Ecuadorean mammals. Amer Mus Novit 32:1–6

    Google Scholar 

  • Antoine PO, Salas-Gismondi R, Pujos F, Ganerød M, Marivaux L (2016) Western Amazonia as a hotspot of mammalian biodiversity throughout the Cenozoic. J Mammal Evol 24:5–17. https://doi.org/10.1007/s10914-016-9333-1

    Article  Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Article  CAS  PubMed  Google Scholar 

  • Bangs O (1898) Descriptions of some new mammals from the Sierra Nevada de Sta. Marta. Colombia. Proc Biol Soc Washington 12:161–165

    Google Scholar 

  • Bernarde PS, Machado RA (2008) Mammalia, Didelphimorphia, Didelphidae, Glironia venusta Thomas, 1912: distribution extension to the state of Acre, Brazil. Check List 4:151. https://doi.org/10.15560/4.2.151

    Article  Google Scholar 

  • Bezerra AMR, Caramaschi FP, Bonvicino CR, Castiglia R (2018) Integrative taxonomy of the Amazonian red-sided opossum Monodelphis glirina (JA Wagner, 1842) (Didelphimorphia: Didelphidae). Zootaxa 4508:46. https://doi.org/10.11646/zootaxa.4508.1.2

    Article  Google Scholar 

  • Bonvicino CR, Weksler M (2012) Speciation in Amazonia, patterns and predictions of a network of hypotheses. In: Patterson BD, Costa EP (eds) Bone, clones and biomes, the history and geography of recent neotropical mammals. The University of Chicago Press, Chicago & London, pp 259–282

    Chapter  Google Scholar 

  • Cabanne GS, Santos FR, Miyaki CY (2007) Phylogeography of Xiphorhynchus fuscus (Passeriformes, Dendrocolaptidae): vicariance and recent demographic expansion in southern Atlantic forest. Biol J Linn Soc Lond 91:73–84. https://doi.org/10.1111/j.1095-8312.2007.00775.x

    Article  Google Scholar 

  • Cabrera A (1961) Catálogo de los mamíferos de América del Sur. Rev Mus Argentino Cienc Nat “bernardino Rivadavia” (zool) 4:309–732

    Google Scholar 

  • Cáceres NC, Carmignotto AP (2006) Caluromys lanatus. Mamm Species 803:1–6. https://doi.org/10.1644/803.1

    Article  Google Scholar 

  • Caputo MV, Soares EAA (2016) Eustatic and tectonic change effects in the reversion of the transcontinental Amazon River drainage system. Braz J Geol 46(2):301–328. https://doi.org/10.1590/2317-4889201620160066

    Article  Google Scholar 

  • Caramaschi FP. (2005) Variação geográfica em Caluromys philander (Linnaeus, 1758) no Brasil (Didelphimorphia: Didelphidae). Master dissertation. Museu Nacional/Universidade Federal do Rio de Janeiro

  • Caramaschi FP, Nascimento FF, Cerqueira R, Bonvicino CR (2011) Genetic diversity of wild populations of the grey short-tailed opossum, Monodelphis domestica (Didelphimorphia: Didelphidae), Brazilian landscapes. Biol J Linnean Soc 104(2):251–263

    Article  Google Scholar 

  • Cardillo M, Bininda-Emonds ORP, Boakes E, Purvis A (2004) A species-level phylogenetic supertree of marsupials. J Zool 264:11–31. https://doi.org/10.1017/S0952836904005539

    Article  Google Scholar 

  • Carvalho CT (1957) Alguns mamíferos do acre ocidental. Bol Mus Emilio Goeldi 6:1–22

    Google Scholar 

  • Carvalho AL, Nelson BW, Bianchini MC, Plagnol D, Kuplich TM, Daly DC (2013) Bamboo-dominated forests of the southwest amazon: detection, spatial extent, life cycle length and flowering waves. PLoS One 8(1):e54852. https://doi.org/10.1371/journal.pone.0054852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casado F, Bonvicino CR, Nagle C, Comas B, Manzur TD, Lahoz MM, Seuánez HN (2010) Mitochondrial divergence between 2 populations of the Hooded Capuchin, Cebus (Sapajus) cay (Platyrrhini, Primates). J Hered 101:261–269. https://doi.org/10.1093/jhered/esp119

    Article  CAS  PubMed  Google Scholar 

  • Cassens I, Vicario S, Waddell VG, Balchowsky H, Van Belle D, Ding W, Fan C, Lal Mohan RS, Simões-Lopes PC, Bastida R, Meyer A, Stanhope MJ, Milinkovitch MC (2000) Independent adaptation to riverine habitats allowed survival of ancient lineages. Proc Nat Acad Sci 97(21):11343–11347. https://doi.org/10.1073/pnas.97.21.11343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cerqueira R, Tribe CJ (2008) Genus Didelphis Linnaeus, 1758. In: Gardner AL (ed) Mammals of South America, Marsupials, Xenarthrans, Shrews and Bats, vol 1. University of Chicago Press, Chicago, pp 17–25

    Google Scholar 

  • Chambers EA, Hillis DM (2020) The multispecies coalescent over-splits species in the case of geographically widespread taxa. Syst Biol 69(1):184–193. https://doi.org/10.1093/sysbio/syz042

    Article  PubMed  Google Scholar 

  • Chernomor O, von Haeseler A, Minh BQ (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Syst Biol 65:997–1008. https://doi.org/10.1093/sysbio/syw037

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheviron ZA, Hackett SJ, Capparella AP (2005) Complex evolutionary history of a Neotropical lowland forest bird (Lepidothrix coronata) and its implications for historical hypotheses of the origin of Neotropical avian history. Mol Phylogen Evol 36(2):338–357. https://doi.org/10.1016/J.YMPEV.2005.01.015

    Article  CAS  Google Scholar 

  • Colombi VH, Lopes SR, Fagundes V (2010) Testing the Rio Doce as a riverine barrier in shaping the Atlantic rainforest population divergence in the rodent Akodon cursor. Gen Mol Biol 33(4):785–789. https://doi.org/10.1590/s1415-47572010000400029

    Article  Google Scholar 

  • Costa LP (2003) The historical bridge between the Amazon and the Atlantic forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30:71–86. https://doi.org/10.1046/j.1365-2699.2003.00792.x

    Article  Google Scholar 

  • Costa LP, Leite YL, Fonseca GAB, Fonseca MT (2000) Biogeography of South American forest mammals: endemism and diversity in the Atlantic forest. Biotropica 32:872–881. https://doi.org/10.1111/j.1744-7429.2000.tb00625.x

    Article  Google Scholar 

  • D’Apolito C (2016) Landscape evolution in western Amazonia: palynostratigraphy, palaeoenvironments and diversity of the Miocene Solimões formation, Brazil. Thesis, University of Birmingham, Birmingham

    Google Scholar 

  • De La Sancha NU, D’Elia G, Teta P (2012) Systematics of the subgenus of mouse opossums Marmosa (Micoureus) (Didelphimorphia, Didelphidae) with noteworthy records from Paraguay. Mamm Biol 77:229–236. https://doi.org/10.1016/j.mambio.2011.10.003

    Article  Google Scholar 

  • De Salle ROB (2006) Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conserv Biol 20(5):1545–1547. https://doi.org/10.1111/j.1523-1739.2006.00543.x

    Article  Google Scholar 

  • Desmarest AG (1820) Mammalogie ou description des espèces de mammifères. Encylopédie Méthodique. Agasse, Paris

  • Dias CAR, Perini FA (2018) Biogeography and early emergence of the genus Didelphis (Didelphimorphia, Mammalia). Zool Scr 47:645–654. https://doi.org/10.1111/zsc.12306

    Article  Google Scholar 

  • Dias IMG, Almeida FC, Amato G, De Salle R, Fonseca CG (2010) Delineating geographic boundaries of the woolly mouse opossums, Micoureus demerarae and Micoureus paraguayanus (Didelphimorphia: Didelphidae). Conserv Gen 11:1579–1585. https://doi.org/10.1007/s10592-009-9962-5

    Article  Google Scholar 

  • Diaz-Nieto JF, Jansa SA, Voss RS (2016) DNA sequencing reveals unexpected recent diversity and an ancient dichotomy in the American marsupial genus Marmosops (Didelphidae: Thylamyini). Zool J Linnean Soc 176:914–940. https://doi.org/10.1111/zoj.12343

    Article  Google Scholar 

  • Domingues AJP (1948) Contribuição à geologia do sudoeste da Bahia. Rev Bras Geogr 10:255–287

    Google Scholar 

  • Espurt N, Baby P, Brusset S, Roddaz M, Hermoza W, Regard V, Antoine PO, SalasGismondi R, Bolaños R (2007) How does the Nazca Ridge subduction influence the modern Amazonian foreland basin? Geology 35:515–518. https://doi.org/10.1130/G24355C.1

    Article  Google Scholar 

  • Faria MB, Nascimento FF, Oliveira JA, Bonvicino CR (2013) Biogeographic determinants of genetic diversification in the mouse opossum Gracilinanus agilis (Didelphimorphia: Didelphidae). J Hered 104(5):613–626. https://doi.org/10.1093/jhered/est0309

    Article  CAS  PubMed  Google Scholar 

  • Gardner AL (2008) Mammals of South America. Marsupials, xenarthrans, shrews and bats, vol 1. The University of Chicago Press, Chicago and London

    Book  Google Scholar 

  • Gardner AL, Creighton GK (2008) Genus Marmosops Matschie 1916. In: Gardner AL (ed) Mammals of South America. Marsupials, xenarthrans, shrews and bats. Chicago University Press, Chicago, IL, pp 61–74

    Chapter  Google Scholar 

  • Gascon C, Malcolm JR, Patton JL, da Silva MNF, Bogart JP, Lougheed SC, Peres CA, Neckel S, Boag PT (2000) Riverine barriers and the geographic distribution of Amazonian species. Proc Nat Aca Sci USA 97:13672–13677. https://doi.org/10.1073/pnas.230136397

    Article  CAS  Google Scholar 

  • Goldner A, Herold N, Huber M (2014) The challenge of simulating the warmth of the mid-Miocene climatic optimum in CESM1. Climate of the past 10:523–536. https://doi.org/10.5194/cp-10-523-2014

    Article  Google Scholar 

  • Goulding M, Barthem R, Ferreira EJG (2003) The smithsonian atlas of the Amazon. Smithsonian Institution Press, Washington DC

    Google Scholar 

  • Haffer J (2008) Hypotheses to explain the origin of species in Amazonia. Braz J Biol. https://doi.org/10.1590/S1519-69842008000500003

    Article  PubMed  Google Scholar 

  • Hajibabaei M, Singer GA, Hebert PD, Hickey DA (2007) DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet 23(4):167–172. https://doi.org/10.1016/j.tig.2007.02.001

    Article  CAS  PubMed  Google Scholar 

  • Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281

    Article  CAS  PubMed  Google Scholar 

  • Hoorn C, Wesselingh FP, Ter Steege H, Bermudez MA, Mora A, Sevink J, Sanmartín I, Sanchez-Meseguer A, Anderson CL, Figueiredo JP, Jaramillo C, Riff D, Negri FR, Hooghiemstra H, Lundberg J, Stadler T, Särkinen T, Antonelli A (2010) Amazonia through time: andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931. https://doi.org/10.1126/science.1194585

    Article  CAS  PubMed  Google Scholar 

  • IBAN (2020) Country codes ALPHA-2 & ALPHA-3. Available at https://www.iban.com/country-codes. Accessed 21 Sept 2020

  • Irwin D, Kocher T, Wilson A (1991) Evolution of the cytochrome-b gene of mammals. J Mol Evol 32(2):128–144. https://doi.org/10.1007/BF02515385

    Article  CAS  PubMed  Google Scholar 

  • Janiak MC, Silva FE, Beck RMD, de Vries D, Kuderna LFK, Torosin NS, Melin AD, Marquès- Bonet T, Goodhead IB, Messias M, da Silva MNF, Sampaio I, Farias IP, Rossi R, de Melo FR, Valsecchi J, Hrbek T, Boubli JP (2022) Two hundred and five newly assembled mitogenomes provide mixed evidence for rivers as drivers of speciation for Amazonian primates. Mol Ecol. https://doi.org/10.1111/mec.16554

    Article  PubMed  PubMed Central  Google Scholar 

  • Jansa SA, Barker FK, Voss RS (2014) The early diversification history of didelphid marsupials: a window into South America’s “splendid isolation.” Evolution 68:684–695. https://doi.org/10.1111/evo.12290

    Article  PubMed  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TK, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapli P, Lutteropp S, Zhang J, Kobert K, Pavlidis P, Stamatakis A, Flouri T (2017) Multi-rate poisson tree processes for single-locus species delimitation under maximum likelihood and markov chain monte carlo. Bioinformatics 33(11):1630–1638. https://doi.org/10.1093/bioinformatics/btx025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr R (1792) The animal kingdom or zoological system, of the celebrated Sir Charles Linnaeus. Class I. Mammalia. J Murray & R Faulder, London

  • King LC (1956) A geomorfologia do Brasil Oriental. Rev Bras Geogr 2:147–265

    Google Scholar 

  • Kinzey WG (1982) Distribution of primates and forest refuges. In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, New York, pp 455–482

    Google Scholar 

  • Lees AC, Davis BJW, de Oliveira AVG, Peres CA (2008) Avifauna of a structurally heterogeneous forest landscape in the Serra dos Caiabis, Mato Grosso, Brazil: a preliminary assessment. Cotinga 29:147–157

    Google Scholar 

  • Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Laurentii Salvii, Stockholm

  • Lund PW (1840) Fortsaettelse af Pattedyrene. K Danske Vidensk Selskab Naturv Math Afhandl 3:1–56

    Google Scholar 

  • Luo A, Ling C, Ho SYW, Zhu C-D (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Syst Biol 67:830–846. https://doi.org/10.1093/sysbio/syy011

    Article  PubMed  PubMed Central  Google Scholar 

  • Matschie P (1917) Einige neue Formen der Didelphis lanigera-Gruppe. Sitzungsber Gesells Naturf Freunde Berlin, pp 280–294

  • Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37(5):1530–1534. https://doi.org/10.1093/molbev/msaa015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miranda-Ribeiro A (1936) Didelphia ou Mammalia-Ovovivipara. Marsupiaes, Didelphos, Pedimanos ou Metatherios. Rev Mus Paulista 20:245–427

    Google Scholar 

  • Mondolfi E, Pérez-Hernández R (1984) Una nueva subespecie de zarigüeya del grupo Didelphis albiventris (Mammalia-Marsupialia). Acta Cient Venez 35:407–413

    Google Scholar 

  • Nascimento FF, Pereira LG, Geise L, Bezerra AMR, D’Andrea PS, Bonvicino CR (2011) Colonization process of the Brazilian common vesper mouse, Calomys expulsus (Cricetidae, Sigmodontinae): a biogeographic hypothesis. J Hered 102:260–268. https://doi.org/10.1093/jhered/esr012

    Article  PubMed  Google Scholar 

  • Nascimento FF, Lazar A, Menezes AN, Durans AM, Moreira JC, Salazar-Bravo J, D’Andrea PS, Bonvicino CR (2013) The role of historical barriers in the diversification process in open vegetation formation during the Miocene/Pliocene using an ancient rodent lineage as a model. PLoS ONE 8(4):e61924. https://doi.org/10.1371/journal.pone.0061924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nascimento DC, Campos BATP, Fraga EC, Barros MC (2019) Variabilidade genética de populações de gambá de orelha branca, Didelphis albiventris Lund 1840 (Didelphimorphia; Didelphidae) no Brasil. Braz J Biol 79(4):594–602. https://doi.org/10.1590/1519-6984.184842

    Article  CAS  PubMed  Google Scholar 

  • Patton JL, da Silva MNF (1998) Rivers, refuges, and ridges: the geography of speciation of Amazonian mammas. In: Howards DJ, Berlocher SH (eds) Endless forma: species and speciation. Oxford University Press, Oxford, pp 202–213

    Google Scholar 

  • Patton JL, da Silva MNF, Lara MC, Mustrangi MA (1997) Diversity, differentiation, and the historical biogeography on non-volant small mammals of the neotropical forests. In: Laurance WF, Bierregard RO (eds) Tropical forest remnants: ecology, management and conservation of fragmented communities. University of Chicago Press, Chicago, pp 455–546

    Google Scholar 

  • Patton JL, da Silva MNF, Malcolm JR (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bull Am Mus Nat Hist 244:1–306. https://doi.org/10.1206/0003-0090(2000)244%3c0001:MOTRJA%3e2.0.CO;2

    Article  Google Scholar 

  • Pavan SE (2019) A revision of the Monodelphis glirina group (Didelphidae: Marmosini), with a description of a new species from Roraima. Brazil J Mammal 100(1):103–117. https://doi.org/10.1093/jmammal/gyy165

    Article  Google Scholar 

  • Pavan SE, Jansa SA, Voss RS (2014) Molecular phylogeny of short-tailed opossums (Didelphidae: Monodelphis): taxonomic implications and tests of evolutionary hypotheses. Mol Phylogenet Evol 79:199–214. https://doi.org/10.1016/j.ympev.2014.05.029

    Article  PubMed  Google Scholar 

  • Rylands AB, Coimbra-Filho AF, Mittermeier RA (2009) The systematics and distributions of the Marmosets (Callithrix, Callibella, Cebuella and Mico) and Callimico (Callimico) (Callitrichidae, Primates). In: Ford SM, Porter LM, Davis LC (eds) The smallest Anthropoids: The Marmoset/Callimico radiation. Springer, Chicago, pp 25–61

    Chapter  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Silva LGDL, Ferreira DC, Rossi RV (2019) Species diversity of Marmosa subgenus Micoureus (Didelphimorphia, Didelphidae) and taxonomic evaluation of the white-bellied woolly mouse opossum, Marmosa constantiae. Zool J Linn Society 187:240–277. https://doi.org/10.1093/zoolinnean/zlz023

    Article  Google Scholar 

  • Silveira M (2001) A floresta aberta com bambu no sudoeste da Amazônia: padrões e processos em múltiplas escalas. Thesis, University of Brasília, Federal District

    Google Scholar 

  • Smith MF, Patton JL (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50(3):149–177. https://doi.org/10.1111/j.1095-8312.1993.tb00924.x

    Article  Google Scholar 

  • Soares FS, Zílio PPS, Santos SKF, Silva EP (2017) Caracterização física do terreno e mapeamento das tipologias florestais de uma porção do munícipio de Alta Floresta/MT. Agrarian Acad 4(7):103–114. https://doi.org/10.18677/Agrarian_Academy_2017a10

    Article  Google Scholar 

  • Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17(7):866–880. https://doi.org/10.1111/ele.12277

    Article  PubMed  Google Scholar 

  • Suguio K (1999) Geologia do Quaternário e Mudanças Ambientais: (passado + presente =futuro?). São Paulo: Paulo´s Comunicação e Artes Gráficas

  • Tate GHH (1931) Brief diagnoses of twenty-six apparently new forms of Marmosa (Marsupialia) from South America. Amer Mus Novit 493:1–14

    Google Scholar 

  • Thomas O (1904) Two new mammals from South America. Ann Mag Nat Hist 13:142–144

    Article  Google Scholar 

  • Thomas O (1905) New Neotropical Chrotopterus, Sciurus, Neacomys, Coendou, Proechimys, and Marmosa. Ann Mag Nat Hist 16:308–314

    Article  Google Scholar 

  • Thomas O (1913) The geographical races of the woolly opossum (Philander laniger). Ann Mag Nat Hist 12:358–361

    Article  Google Scholar 

  • Thomas O (1920) On mammals from the lower Amazons in the Goeldi Museum, Pará. Ann Mag Nat Hist 6:266–283

    Article  Google Scholar 

  • Thomas O (1924) On a collection of mammals made by Mr. Latham Rutter in the Peruvian Amazons. Ann Mag Nat Hist 13:530–538

    Article  Google Scholar 

  • Valadão RC (1998) Evolução de longo termo do relevo do Brasil Oriental: desnudação, superfícies de aplanamento e soerguimentos crustais. Thesis, Federal University of Bahia, Bahia state

    Google Scholar 

  • Vieira CLGC (2006) Sistemática do jupati Metachirus Burmeister, 1854 (Mammalia:Didelphimorphia). Thesis, Federal University of Espírito Santo, Espírito Santo state

    Google Scholar 

  • von Tschudi JJ (1845) Untersuchungen über die Fauna peruana. Therologie, St. Gallen, Scheitlin und Zollikofer

  • Voss RS, Giarla TC. (2021) A revision of the didelphid marsupial genus Marmosa Part 3. A new species from western Amazonia, with redescriptions of M. perplexa Anthony, 1922, and M. germana Thomas, 1904. Am Mus Novitates n.3969:1–28. http://digitallibrary.amnh.org/handle/2246/7262

  • Voss RS, Jansa SA (2009) Phylogenetic relationships and classification of didelphid marsupials, an extant radiation of new world metatherian mammals. Bull Am Mus Nat Hist 322:1–177. https://doi.org/10.1206/322.1

    Article  Google Scholar 

  • Voss RS, Díaz-Nieto JF, Jansa SA, Angermann R. (2018) A revision of Philander (Marsupialia, Didelphidae). Part 1, P.quica, P.canus, and a new species from Amazonia. Am Mus Novitates 3891. http://digitallibrary.amnh.org/handle/2246/6839

  • Voss RS, Fleck DW, Jansa SA (2019) Mammalian diversity and matses ethnomammalogy in Amazonian Peru. Part 3: Marsupial (Didelphimorphia). Bull Am Mus Nat Hist 432:1–87. https://doi.org/10.1206/0003-0090.432.1.1

    Article  Google Scholar 

  • Voss RS, Giarla TC, Díaz-Nieto JF, Jansa SA (2020) A revision of the didelphid marsupial genus Marmosa Part 2. Species of the Rapposa Group (Subgenus Micoureus). Bull Am Mus Nat Hist 439(1):1–62. https://doi.org/10.1206/0003-0090.439.1.1

    Article  Google Scholar 

  • Wagner JA (1842) Diagnosen neuer Arten brasilischer Säugthiere. Arch Naturgesch 8(1):356–362

    Google Scholar 

  • Wallace AR (1853) On the monkeys of the Amazon. Ann Mag Nat Hist 14(3):451–454. https://doi.org/10.1080/037454809494374

    Article  Google Scholar 

  • Wanderley Filho JR (1991) Evolução Estrutural da Bacia do Amazônia e sua relação com o embasamento. Universidade Federal do Pará, Pará

    Google Scholar 

  • Wesselingh FP, Salo JA (2006) A Miocene perspective on the evolution of the Amazonian biota. Scr Geol 133:439–458

    Google Scholar 

  • Wesselingh FP, Räsänen ME, Irion G, Vonhof HB, Kaandorp R, Renema W, Romero Pittman L, Gingras M (2002) Lake Pebas: a palaeoecological reconstruction of a Miocene, long-lived lake complex in western Amazonia. Cainozoic Res 1(1/2):35–68

    Google Scholar 

  • Wesselingh FP, Hoorn MC, Guerrero J, Räsänen ME, Pittmann LR, Salo J. (2006) The stratigraphy and regional structure of Miocene deposits in western Amazonia (Peru, Colombia and Brazil), with implications for late Neogene landscape evolution. Scr Geol 133:291–322. https://hdl.handle.net/20.500.12544/665

  • Xu X, Kuntner M, Bond JE, Ono H, Ho SY, Liu F, You L, Li D (2020) Molecular species delimitation in the primitively segmented spider genus Heptathela endemic to Japanese islands. Mol Phylogen Evol 151:106900. https://doi.org/10.1016/j.ympev.2020.106900

    Article  Google Scholar 

  • Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):2869–2876. https://doi.org/10.1093/bioinformatics/btt499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer K, Parker TA, Isler M, Isler P (1997) Survey of a southern Amazonian avifauna: the Alta Floresta region, Mato Grosso, Brazil. Ornithol Monogr 48:887–918

    Article  Google Scholar 

  • zu Wied-Neuwied MP (1826) Beiträge zur Naturgeschichte von Brasilien. Verzeichniss der Amphibien, Säugthiere und Vögel, welche auf einer Reise zwischen dem 13ten und dem 23sten Grade südlicher Breite im östlichen Brasilien beobachtet wurden. II. Abtheilung, Mammalia. Landes−Industrie−Comptoirs, Weimar

Download references

Acknowledgements

We are grateful to Rayque Lanes for helping with the maps, and the field team of Luciana Medeiros-Federal University of Acre-UFAC, Ana Maria Jansen-LABTRIP/IOC/Fiocruz, LABPMR/Fiocruz, Federal Institute of Acre-PPBIO/AC for their help with fieldwork. We are also grateful to Robin M. D. Beck for valuable suggestions in a previous version of this manuscript. The permit for the collection of specimens (SISBIO-l.13373) was issued by Instituto Chico Mendes de Conservação da Biodiversidade-ICMBio.

Funding

Work supported by grants of IOC–Fiocruz/IFAc Institutional Agreement and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), to Paulo S. D’Andrea (Universal/. Processo: 439208/2018-1), L Medeiros (CNPq-2853813237160052-2016, PPSUS/Fundação de Ampara à Pesquisa do Acre-FAPAC-001/2015), CR Bonvicino (CNPq-304498/2014-9, Fundação Carlos Chagas de Amparo à Pesquisa do Rio de Janeiro-FAPERJ-E26/201.200/2014), E Morato and M Silveira (PPBio/CNPq-457540/2012-5).

Author information

Authors and Affiliations

  1. Genetics Division, José Gomes de Alencar National Cancer Institute, Rua André Cavalcanti, 37, 4º. andar, Rio de Janeiro, RJ, 20231-050, Brazil

    Cibele R. Bonvicino

  2. Department of Vertebrates, Museu Nacional, Universidade Federal do Rio de Janeiro (UFRJ), São Cristóvão, Rio de Janeiro, RJ, 20940-040, Brazil

    Ana Lazar

  3. Instituto de Biologia, Programa de pós-graduação em Genética, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil

    Cintia Povill

  4. Colégio Pedro II, Rio de Janeiro, Brazil

    Fabiana P. Caramaschi

  5. Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil, 4365, Manguinhos, Rio de Janeiro, RJ, 21040-360, Brazil

    Cibele R. Bonvicino, Tatiana P. T. de Freitas & Paulo S. D’Andrea

  6. Programa de pós-graduação em Biodiversidade e Saúde, IOC/Fiocruz, Rio de Janeiro, Brazil

    Charle F. Crisóstomo & Paulo S. D’Andrea

  7. Instituto Federal do Acre, Rio Branco, Acre, Brazil

    Charle F. Crisóstomo & André L. M. Botelho

  8. Programa de Pesquisa em Biodiversidade–PPBio, Núcleo Regional Acre, Rio Branco, Acre, Brazil

    André L. M. Botelho

Authors
  1. Cibele R. Bonvicino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Lazar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cintia Povill
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabiana P. Caramaschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tatiana P. T. de Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Charle F. Crisóstomo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. André L. M. Botelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paulo S. D’Andrea
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cibele R. Bonvicino.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Ethical approval

CEUA/IOC L-036/2018.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: Author’s affiliation was updated.

Handling editor: Allan McDevitt.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 66 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bonvicino, C.R., Lazar, A., Povill, C. et al. Phylogeny of Didelphid marsupials (Didelphimorphia) from Acre, western Amazonia. Mamm Biol 102, 1997–2015 (2022). https://doi.org/10.1007/s42991-022-00314-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42991-022-00314-7

Keywords

Search

Navigation