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New record of the rare Atlantic Forest rodent Phyllomys lundi (Mammalia: Rodentia)

Michel B. Faria Moisés L.G. Siqueira Cibele R. Bonvicino About the authors

ABSTRACT

The arboreal echimyid rodent of the genus Phyllomys Lund, 1839 is found in the eastern Brazilian Atlantic forest, from the state of Ceará to the state of Rio Grande do Sul, reaching the São Francisco and Paraná river basins in the west. There are 13 species in the genus. Phyllomys lundi Leite, 2003, which until now was known from only two localities, is one of the four endemic Atlantic Forest species of Phyllomys with very restricted distribution. We provide additional data on the morphology, distribution and phylogeography (based on cytochrome b sequences) of the rare P. lundi . Our new record broadens the northern limit of the distribution P. lundi by approximately 250 km with respect to previous records.

KEY WORDS:
Echimyidae; geographic distribution; Lund's Atlantic tree rat

The Brazilian Atlantic rainforest is considered one of the most diverse and threatened biomes on the planet (Galindo-Leal & Camara 2005Galindo-Leal C, Câmara IG (2005) Status do hotspot Mata Atlântica: uma síntese, p. 3-11. In: Galindo Leal C, Câmara IG (Eds.) Mata Atlântica: Biodiversidade, Ameaças e Perspectivas. Belo Horizonte, Conservação Internacional.). Its level of endemism is up to 90% for some groups of organisms, and its overall 50% average endemism is surpassed only by the Amazon forest (Costa et al. 2003Costa L (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. Journal of Biogeography 30: 71-86. doi: 10.1046/j.1365-2699.2003.00792.x
https://doi.org/10.1046/j.1365-2699.2003...
). Among the endemic Atlantic Forest mammals, there are several species of Echimyidae, the most diverse hystricognath rodent family in South America (Patton et al. 2015Patton JL, Pardiñas UFJ, D'Elía G (2015) Mammals of South America. Chicago, The University of Chicago Press, vol. 2.). The Atlantic Forest echimyids are grouped into five genera. Three are monoespecific, [Kannabateomys amblyonyx (Wagner, 1845), Callistomys pictus (Pictet, 1843) and Euryzygomatomys spinosus (G. Fisher, 1814)], while the other two are speciose (Phyllomys Lund, 1839 and Trinomys Thomas, 1921) (Loss & Leite 2011Loss AC, Leite YLR (2011) Evolutionary diversification of Phyllomys (Rodentia: Echimyidae) in the Brazilian Atlantic Forest. Journal of Mammalogy 92: 1352-1366. doi: 10.1644/10-MAMM-A-320.1
https://doi.org/10.1644/10-MAMM-A-320.1...
).

Phyllomys belongs to an arboreal radiation of echimyid rodents distributed in forested areas in eastern Brazil, from the states of Paraíba and Ceará (ca. 7°S) in the Northeast, to Rio Grande do Sul (ca. 30°S) in the South, reaching the São Francisco and Paraná river basins to the west at approximately 54°W (Leite 2003Leite YL (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Berkeley, University of California Press, University of California Publications in Zoology, vol. 132, XV+118p.). Throughout this large distribution, Phyllomys dwells predominantly in the broadleaf evergreen forests of the coastal Atlantic Forest and associated habitats such as Araucaria forests and mangroves. Additionally, it inhabits the semi deciduous forests of the Caatinga and Cerrado (Leite 2003Leite YL (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Berkeley, University of California Press, University of California Publications in Zoology, vol. 132, XV+118p., Campos & Percequillo 2007Campos BATP, Percequillo AR (2007) Mammalia, Rodentia, Echimyidae, Phyllomys blainvilii (Jourdan, 1837): range extension and new geographic distribution map. Check List 3: 18-20). There are 13 described species of Phyllomys , four of which, based on records of very few specimens, seem to have restricted distribution: Phyllomys kerri (Moojen, 1950), with three collected specimens in 1941 at Ubatuba, state of São Paulo, Phyllomys lundi Leite, 2003 with two collected specimens, and Phyllomys mantiqueirensis Leite, 2003 and Phyllomys. unicolor (Wagner, 1842), both known only from their respective holotypes (Loss & Leite 2011Loss AC, Leite YLR (2011) Evolutionary diversification of Phyllomys (Rodentia: Echimyidae) in the Brazilian Atlantic Forest. Journal of Mammalogy 92: 1352-1366. doi: 10.1644/10-MAMM-A-320.1
https://doi.org/10.1644/10-MAMM-A-320.1...
). The limited numbers of collected specimens result from the fact that collecting these arboreal and elusive species is difficult. Herein we report on the capture of the third known specimen of P. lundi , and present the results of a phylogenetic analysis of Phyllomys .

One adult female specimen (field number MBF 340) of P. lundi was captured in the municipality of Alto Jequitibá, at the protected area "Reserva Particular do Patrimônio Natural (RPPN) Refúgio dos Sauás", in eastern Minas Gerais, southeastern Brazil, near the border with Espírito Santo and Rio de Janeiro, latitude -20.4868 and longitude -42.0399, altitude around 400 m (Fig. 1). The animal was collected using a Sherman live trap placed 1.5 meters high in the forest understory. It was deposited in the Museu de Zoologia Newton Baião de Azevedo (MZNB), Universidade do Estado de Minas Gerais (EUMG) in Carangola, Minas Gerais, Brazil, catalog number 271. This specimen was collected under permit number 41959-1, issued by Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), and handled according to recommended safety procedures. A total of 23 measurements were taken with a digital caliper following previous work (Leite 2003Leite YL (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Berkeley, University of California Press, University of California Publications in Zoology, vol. 132, XV+118p., Table 1).

Figure 1
Collecting localities of P. lundi including the type locality (circle) and new locality of occurrence (square). Gray area corresponds to Atlantic Forest.

Table 1
Cranial measurements of Phyllomys lundi. Measurements of holotype (MN62392) are from Leite (2003Leite YL (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Berkeley, University of California Press, University of California Publications in Zoology, vol. 132, XV+118p.).

To confirm the morphological identification, a phylogenetic analysis was carried out using DNA cytochrome b sequences of the captured specimen and GenBank sequences (GenBank number KU756488) of P. lundi (EF608183), Phyllomys nigrispinus (Wagner, 1842) (EF608184), Phyllomys dasythrix Hensel, 1872 (EF608185), Phyllomys blainvilii (Jourdan, 1837) (JF297836), Phyllomys brasiliensis Lund, 1840 (EF608182), Phyllomys lamarum (Thomas, 1916) (EF608181), Phyllomys pattoni Emmons, Leite, Kock and Costa, 2002 (JF297839), P. mantiqueirensis (EF608179), P. unicolor (EF608188). Sequences of Echimys chrysurus (Zimmermann, 1780) (L23341) and Makalata didelphoides (Desmarest, 1817) (GI996078) were used as outgroups.

DNA was isolated from liver tissue preserved in 100% ethanol with the standard phenol-chloroform protocol (Sambrook & Russel 2001Sambrook KJ, Russel DW (2001) Molecular Cloning. A Laboratory Manual. New York, Cold Spring Harbor Laboratory Press, 3rd ed., 2344p.). The complete (1,143 bp) mitochondrial Cytochrome b gene (mt-Cytb) was PCR-amplified using the primers L14724 (Irwin et al. 1991Irwin DM, TD Kocher, AC Wilson (1991) Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution 32: 128-144. doi: 10.1007/BF02515385
https://doi.org/10.1007/BF02515385...
) and mt-Cytb Rev (Casado et al. 2010Casado 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). Journal of Heredity 101: 261-269. doi: 10.1093/jhered/esp119.
https://doi.org/10.1093/jhered/esp119....
), following a pre-denaturation step at 94°C for 2 min and 35 cycles 94°C for 1 min, annealing at 52°C for 1 min, 72°C for 1:30 min, and final extension of 72°C for 5 min. Amplicons were purified using the GFX PCR DNA and Gel Band Purification Kit (GE Healthcare) and labeled with the PCR primers and the internal primers SOT in1 and SOT in2 (Cassens et al. 2000Cassens I, S Vacario, Waddell VG, Balchowsky H, Van Belle D, Ding W, Fan C, Lal Mohan RS, Simões-Lopesi PC, Bastida R, Meyer A, Stanhope MJ, Milinkovitch MC (2000) Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proceedings of the National Academy of Sciences of the United States of America 97: 11343-11347. doi: 10.1073/pnas.97.21.11343
https://doi.org/10.1073/pnas.97.21.11343...
) and mt-CytbAOT (Menezes et al. 2010Menezes NA, Bonvicino CR, Seuánez HN (2010) Identification, classification and evolution of Owl Monkeys (Aotus, Illiger 1811). BMC Evolucionary Biology 10: 248. doi: 10.1186/1471-2148-10-248
https://doi.org/10.1186/1471-2148-10-248...
). Electropherograms were manually checked in Chromas version 1.45 (Maccarthy 1998Mccarthy C (1998) Chromas 1.45. Gold Coast, Queensland, School of Health Science, Griffith University.), Chromas PRO version 1.41 (Technelysium Pty Ltd.) and MEGA version 6.0 (Tamura et al. 2007Tamura K, Dudley J, NEI M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599. doi: 10.1093/molbev/msm092
https://doi.org/10.1093/molbev/msm092...
). The sequences were manually aligned in MEGA version 6 (Tamura et al. 2007Tamura K, Dudley J, NEI M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599. doi: 10.1093/molbev/msm092
https://doi.org/10.1093/molbev/msm092...
). Genetic distances were estimated with MEGA using the Kimura 2-parameter. The DNA substitution models were selected using MODELGENERATOR version 0.85 (Keane et al. 2006Keane TM, CJ Creevey, MM Pentony, TJ Naughton, JO Mclnerney (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6: 29 doi: 10.1186/1471-2148-6-29
https://doi.org/10.1186/1471-2148-6-29...
). The phylogenetic reconstructions by maximum likelihood (ML) and Bayesian inference (BI) based on the mt-Cytb were constructed using the HKY model (Hasegawa et al. 1985Hasegawa M, Kishino H, Yano TA (1985) Dating of the human ape splitting by a molecular clock of mitochondrial-DNA. Journal of Molecular Evolution 22: 160-174. doi: 10.1007/BF02101694
https://doi.org/10.1007/BF02101694...
), with a proportion of invariable sites and gamma distributed rates. ML was carried out with PhyML version 3.0 (Guindon & Gascuel 2003Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate larges phylogenies by maximum likelihood. Systematic Biology 52: 696-704. doi: 10.1080/10635150390235520
https://doi.org/10.1080/1063515039023552...
), and branch support was calculated using the approximate likelihood ratio test (SH-aLRT) with Shimodaira-Hasegawa-like interpretation (Anisimova & Gascuel 2006Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55: 539-552. doi: 10.1080/10635150600755453
https://doi.org/10.1080/1063515060075545...
). BI was carried out using MrBayes, version 3.1.2 (Ronquist & Huelsenbeck 2003Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. doi: 10.1093/bioinformatics/btg180
https://doi.org/10.1093/bioinformatics/b...
). For BI, two chains were run for 1.000.000 generations, and one tree per 100 generations was sampled. Convergence and mixing were evaluated using TRACER version 1.5 (Rambaut & Drummond 2007Rambaut A, Drummond AJ (2007) Tracer. Version. 1.5, available online at: 5, available online at: http://beast.bio.ed.ac.uk/Tracer [Accessed: 10/11/2012]
http://beast.bio.ed.ac.uk/Tracer...
), with initial 10% runs discarded (burn-in). A majority rule consensus phylogram was subsequently constructed.

The specimen collected by us presented the general morphological characters, as described for the species (Fig. 2), and the following external measurements in mm: head-body 398, tail 208, feet with 38 and without claws 35, ear 12; and weight 174,6 g. Dorsal pelage coloration is predominantly orange intermixed with black and the neck, thighs markedly orange, and spines conspicuous from neck to tail. Ventral hairs cream with white base, providing an overall washed aspect. Tail brown and hairy from base to tip; forefeet covered with brown yellow hairs, except for gray-white fingers. Dorsal surfaces of hind feet covered with golden-creamy hairs and toes with silver hair. Skull delicate, with relatively narrow and long rostrum, and wide and convex interorbital region. Mandible with short coronoid process and a shallow sigmoid notch. There was some variation in characters of the skull with respect to previous description of the species (Leite 2003Leite YL (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Berkeley, University of California Press, University of California Publications in Zoology, vol. 132, XV+118p.), such as rostrum narrow and elongated, with distal and proximal regions of similar width, and anterior part of the zygomatic plate surpassing the suture between nasal and frontal (Fig. 2). The skull measurements of the collected specimen are in Table 1.

Figure 2
Dorsal, ventral and lateral views of skull and skin of P. lundi female MZNB 271. Scale bars: 1 cm.

The topologies obtained with maximum likelihood (ML) and Bayesian inference (BI) were similar (Fig. 3) and confirmed the morphological identification of the specimen collected by us, clustering it together with the other of P. lundi , with 0.4% of genetic distance between them (Table 2). The position of the P. lundi clade as sister to the clade [P. blainvilli (P. brasiliensis , P. lamarum) ] is moderately supported (76% Bootstrap and 0.7 posterior probably), corroborating previous work (Loss & Leite 2011Loss AC, Leite YLR (2011) Evolutionary diversification of Phyllomys (Rodentia: Echimyidae) in the Brazilian Atlantic Forest. Journal of Mammalogy 92: 1352-1366. doi: 10.1644/10-MAMM-A-320.1
https://doi.org/10.1644/10-MAMM-A-320.1...
), and contrasting with the parsimony analysis that grouped P. lundi with P. nigrispinus (Leite 2003Leite YL (2003) Evolution and systematics of the Atlantic tree rats, genus Phyllomys (Rodentia, Echimyidae), with description of two new species. Berkeley, University of California Press, University of California Publications in Zoology, vol. 132, XV+118p.), but in agreement with the ML analysis of this same paper.

Figure 3
Maximum likelihood topology based on cytochrome b sequences. Numbers near branches are bootstrap values ≥ 70 for ML (above) and posterior probabilities for BI (below).

Table 2
Genetic distance estimates (K2p), in percentage, between Phyllomys species with mt-Cytb data.

The Atlantic Forest is an area with complex topography over short geographical distances, and is generally characterized by strong seasonality, sharp environmental gradients, and the presence of the high mountain ranges of Serra do Mar and Serra da Mantiqueira (IBGE 1993IBGE (1993) Mapa da vegetação do Brasil. 1:5.000.000. Rio de Janeiro, Instituto Brasileiro de Geografia e Estatística.). Serra da Mantiqueira and the complex topography of its Atlantic Forest apparently limit the distribution of P. lundi to the north and west, and the Atlantic Ocean limits it, to the south and east. This species occurs from the lowlands at Poço das Antas, state of Rio de Janeiro, to 680 m at the type locality (Fazenda do Boné, Passa Vinte, state of Minas Gerais, Brazil, Table 3). This is in accordance with the Montane Isolate Hypothesis, which postulates that the isolation of montane rainforest remnants during climatic dry periods led to divergence and speciation, with new species subsequently expanding their range to the lowlands (Moreau 1966Moreau RE (1966) The bird faunas of Africa and its islands. New York, Academic Press, 424p.). The role of Serra da Mantiqueira mountain range in determining population structure, and even speciation in vertebrates is well documented for reptiles (Grazziotin et al. 2006Grazziotin FG, Monzel M, Echeverrigaray S, Bonatto SL (2006) Phylogeography of the Bothrops jararaca complex (Serpentes: Viperidae): past fragmentation and island colonization in the Brazilian Atlantic Forest. Molecular Ecology 15: 3969-3982. doi: 10.1111/j.1365-294X.2006.03057.x
https://doi.org/10.1111/j.1365-294X.2006...
), birds (Cabanne et al. 2007Cabanne GS, Santos FR, Miyaki CY (2007) Phylogeography of Xiphorhynchus fuscus (Passeriformes, Dendrocolaptidae): vicariance and recent demographic expansion in southern Atlantic forest. Biological Journal of the Linnean Society 91: 73-84. doi: 10.1111/j.1095-8312.2007.00775.x
https://doi.org/10.1111/j.1095-8312.2007...
, 2008Cabanne GS, d'Horta FM, Sari EHR, Santos FR, Miyaki CY (2008) Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): biogeography and systematic implications. Molecular Phylogenetic and Evolution 49: 760-773. doi: 10.1016/j.ympev.2008.09.013
https://doi.org/10.1016/j.ympev.2008.09....
, d'Horta et al. 2011d'Horta FM, Cabanne GS, Meyer D, Miyaki CY (2011) The genetic effects of late quaternary climatic changes over a tropical latitudinal gradient: diversification of an Atlantic forest passerine. Molecular Ecology 20: 1923-1935. doi: 10.1111/j.1365-294X.2011.05063.x
https://doi.org/10.1111/j.1365-294X.2011...
), amphibians (Fitzpatrick et al. 2009Fitzpatrick SW, Brasileiro CA, Haddad CF, Zamudio KR (2009) Geographical variation in genetic structure of an Atlantic coastal forest frog reveals regional differences in habitat stability. Molecular Ecology 18: 2877-2896. doi: 10.1111/j.1365-294X.2009.04245.x
https://doi.org/10.1111/j.1365-294X.2009...
), and invertebrates (Batalha-Filho et al. 2010Batalha-Filho H, Waldschmidt AM, Campos LAO, Tavares MG, Fernandes-Salomão TM (2010) Phylogeography and histori cal demography of the Neotropical stingless bee Melipona quadrifasciata (Hymenoptera, Apidae): incongruence between morphology and mitochondrial DNA. Apidologie 41: 534-547. doi: 10.1051/apido/2010001
https://doi.org/10.1051/apido/2010001...
).

Table 3
Phyllomys lundi specimens in mammal collections, with catalog number, and collecting localities. MN = Museu Nacional, Universidade Federal do Rio de Janeiro, UFMG = Departamento de Zoologia, Universidade Federal de Minas Gerais, MZNB = Museu de Zoologia Newton Baião de Azevedo. The Brazilian states are Minas Gerais (MG) and Rio de Janeiro (RJ).

Phyllomys lundi was listed as endangered because it occurs at an area that is less than 5,000 km2, all known individuals were collected in fewer than five locations, and there has been a continuing decline in the extent and quality of its habitat (Leite & Patterson 2008Leite Y, Patterson B (2008) Phyllomys lundi . The IUCN Red List of Threatened Species. Version 2015.2, available online at: 2, available online at: http://www.iucnredlist.org/details/136400/0 [Accessed: 28/08/2015] doi: 10.2305/IUCN.UK.2008.RLTS.T136400A4286789.en
http://www.iucnredlist.org/details/13640...
). It is now known from three localities (Table 3) 250 to 340 km far from one another in fragmented forests. This finding increases the northern limit of P. lundi by approximately 250 km (Fig. 1), and also expands its occurrence to an area of 23,757 km2, which is more than the threshold used to categorize threatened species (20,000 km2) using IUCN's B criterion (geographic range). It does not, however, change the conservation status of the species, which is still known from less than five localities, all of which continue to shrink and decline in habitat quality.

ACKNOWLEDGEMENTS

We are grateful to "Fundação Vida & Meio Ambiente", Carlos Monteiro, and Rita de Cassia for providing us with work facilities and permission to collect at Fazenda Harmonia; to the members of Museu de Zoologia Newton Baião de Azevedo for help with field work. This work was supported through grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (process 304498/2014-9) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro - FAPERJ (process E-26/201.200/2014) to CRB. MBF received a fellowship from CNPq. We are also grateful for comments of two unknown revisers.

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Data availability

Data citations

Leite Y, Patterson B (2008) Phyllomys lundi . The IUCN Red List of Threatened Species. Version 2015.2, available online at: 2, available online at: http://www.iucnredlist.org/details/136400/0 [Accessed: 28/08/2015] doi: 10.2305/IUCN.UK.2008.RLTS.T136400A4286789.en

Publication Dates

  • Publication in this collection
    2016

History

  • Received
    23 Dec 2015
  • Reviewed
    18 Apr 2016
  • Accepted
    11 May 2016
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