Yuri L. R. Leite

Neotropical forest expansion during the last glacial period challenges refuge hypothesis

Significance The tropical forests of South America are among the most diverse and unique habitats in the world in terms of plant and animal species. One of the most popular explanations for this diversity and endemism is the idea that forests retracted and fragmented during glacial periods, forming ecological refuges, surrounded by dry lands or savannas. These historically stable forest refuges would have been responsible for maintaining the pattern of diversity and endemism observed today. Here, we show that the Atlantic Forest of eastern South America probably expanded, rather than contracted, during the last glacial period. In addition, the emerged Brazilian continental shelf played a major, yet neglected, role on the evolution of this biodiversity hotspot during the last glacial period. The forest refuge hypothesis (FRH) has long been a paradigm for explaining the extreme biological diversity of tropical forests. According to this hypothesis, forest retraction and fragmentation during glacial periods would have promoted reproductive isolation and consequently speciation in forest patches (ecological refuges) surrounded by open habitats. The recent use of paleoclimatic models of species and habitat distributions revitalized the FRH, not by considering refuges as the main drivers of allopatric speciation, but instead by suggesting that high contemporary diversity is associated with historically stable forest areas. However, the role of the emerged continental shelf on the Atlantic Forest biodiversity hotspot of eastern South America during glacial periods has been ignored in the literature. Here, we combined results of species distribution models with coalescent simulations based on DNA sequences to explore the congruence between scenarios of forest dynamics through time and the genetic structure of mammal species cooccurring in the central region of the Atlantic Forest. Contrary to the FRH predictions, we found more fragmentation of suitable habitats during the last interglacial (LIG) and the present than in the last glacial maximum (LGM), probably due to topography. We also detected expansion of suitable climatic conditions onto the emerged continental shelf during the LGM, which would have allowed forests and forest-adapted species to expand. The interplay of sea level and land distribution must have been crucial in the biogeographic history of the Atlantic Forest, and forest refuges played only a minor role, if any, in this biodiversity hotspot during glacial periods.

A Review of the Named Forms of Phyllomys (Rodentia: Echimyidae) with the Description of a New Species from Coastal Brazil

Abstract To clarify the taxonomy and serve as a foundation for future systematic studies, we searched for the type material associated with all named forms of Brazilian Atlantic tree rats of the genus Phyllomys. For the following ten taxa we found either the originally designated holotypes, syntype series, or contemporary specimens likely to have been seen by the authors: P. blainvilii, P. brasiliensis, P. fossilis, P. nigrispinus, P. unicolor, P. dasythrix, P. lamarum, P. medius, P. thomasi, and P. kerri. For five species the holotype was unambiguously identified. For five other named forms no holotype was originally designated but we found several candidate specimens and for all of these we designate lectotypes. We identify the type localities for all named Phyllomys species and amend those which are ambiguous. We review the taxonomy, diagnosing and redescribing all the named forms of the genus. After examining the type material, we concluded that the rusty-sided tree rat from coastal Brazil, usually identified in the literature as P. brasiliensis, belongs to an unnamed species. We describe and name it here. RESUMEN Com o objetivo de esclarecer a taxonomia e servir de base para futuros estudos sistemáticos, nós procuramos identificar os tipos associados a todas as formas descritas dos ratos arbóreos do gênero Phyllomys. Encontramos, para as seguintes 10 espécies, o holótipo designado originalmente, ou séries de síntipos, ou ainda espécimes contemporâneos provavelmente vistos pelos autores: P. blainvilii, P. brasiliensis, P. fossilis, P. nigrispinus, P. unicolor, P. dasythrix, P. lamarum, P. medius, P. thomasi e P. kerri. Para cinco delas o holótipo foi identificado sem nenhuma dúvida, enquanto que vários espécimes candidatos foram encontrados para cinco outras onde nenhum holótipo foi designado originalmente. Para todos esses nós designamos lectótipos. Nós identificamos as localidades tipo de todas as espécies descritas, corrigindo e restringindo as que eram ambíguas. Também revimos a taxonomia, diagnosticando e descrevendo todas as espécies nomeadas do gênero. Após examinarmos os tipos, concluimos que o rato de espinho ferrugíneo da costa do Brasil, geralmente identificado na literatura como Phyllomys brasiliensis, pertence à uma espécie distinta que ainda não tem nome. Nesse artigo, nós descrevemos e nomeamos essa espécie.

Primates of the Atlantic Forest

The Atlantic forest extends from the north-east of Brazil, state of Rio Grande do Norte, and including inland forests (brejos) in the state of Ceara, south along eastern Brazil, through the southernmost state, Rio Grande do Sul, into the northeastern tip of Argentina in the province of Misiones and between the Rios Parana, Uruguai and Iguacu. In contrast to the Amazon, the Atlantic forest (sensu strictu) is typically upland, stretching along the coastal mountain chain, known as the Serra do Mar in the south between the states of Santa Catarina and northern Rio de Janeiro where it is very close to the sea, and the Serra da Mantiqueira and eastern slopes of the Serra do Espinhaco inland. It comprises a complex of vegetation types, which could be referred to as the “Atlantic forest complex ”, and includes principally: 1) evergreen humid tropical forest, divided into a) cool, humid, montane forest (altitudes 800 to 1,500–1,700 m), and b) lower-montane forest (altitudes 300–800 m) with deeper soils, a marked dry season, and lower humidity (except in the valleys and near to the coast where they receive orographic rainfall); and 2) inland semideciduous or dry forests (Rizzini, 1979; Rizzini et al., 1988; Joly et al, 1991).

Small mammals in the diet of barn owls, Tyto alba (Aves: Strigiformes) along the mid-Araguaia river in central Brazil

We collected and analyzed 286 Barn owl, Tyto alba (Scopoli, 1769), pellets from two nests in different environments along the mid-Araguaia River in central Brazil. Our analyses revealed that these owls feed mainly on small mammals, especially rodents. Owls from the riverbanks at Fazenda Santa Fe had a more diverse diet, preying mainly on rodents that typically inhabit riparian grasslands - Holochilus sciureus Wagner, 1842 - and forests - Hylaeamys megacephalus (Fischer, 1814) and Oecomys spp., which probably also occur in forest borders or clearings. On the other hand, owls from an agroecosystem at Fazenda Lago Verde preyed mostly on rodent species common in these agrarian fields, Calomys tocantinsi Bonvicino, Lima & Almeida, 2003. Additionally, we compared small mammal richness estimates based on the analysis of owl pellets with estimates from live-trapping in the same areas. Owl pellets revealed two rodent species undetected by live traps - Euryoryzomys sp. and Rattus rattus (Linnaeus, 1758) - and four rodent species were trapped, but not found in owl pellets - Oecomys roberti Thomas, 1904, Pseudoryzomys simplex (Winge, 1887), Rhipidomys ipukensis Rocha, B.M.A. Costa & L.P. Costa, 2011, and Makalata didelphoides (Desmarest, 1817). Traps yielded higher species richness, but these two methods complement each other for surveying small rodents.

A New Species of Atlantic Forest Tree Rat, Genus Phyllomys (Rodentia, Echimyidae) from Southern Brazil

Abstract Phyllomys is the most diverse genus of the subfamily Echimyinae, and is represented by 12 described species endemic to the Atlantic forest of eastern South America. We name and describe a new species of Phyllomys based on specimens collected in southern Brazil. This species is closely related to P. dasythrix and has been referred to as “Phyllomys aff. dasythrix” in the literature. Chromosomal restructuring was probably involved in their speciation because genetic and morphological similarities of the 2 contrast with their karyotypic distinctiveness. The new species of Phyllomys is diagnosed by a unique combination of external, cranial, and karyotypic characters. We propose the conservation status of “Least Concern” for Phyllomys sp. nov., but “Vulnerable” for P. dasythrix. We present an identification key to the living species of Phyllomys.

Mitogenomic phylogeny, diversification, and biogeography of South American spiny rats

Echimyidae is one of the most speciose and ecologically diverse rodent families in the world, occupying a wide range of habitats in the Neotropics. However, a resolved phylogeny at the genus-level is still lacking for these 22 genera of South American spiny rats, including the coypu (Myocastorinae), and 5 genera of West Indian hutias (Capromyidae) relatives. Here, we used Illumina shotgun sequencing to assemble 38 new complete mitogenomes, establishing Echimyidae, and Capromyidae as the first major rodent families to be completely sequenced at the genus-level for their mitochondrial DNA. Combining mitogenomes and nuclear exons, we inferred a robust phylogenetic framework that reveals several newly supported nodes as well as the tempo of the higher level diversification of these rodents. Incorporating the full generic diversity of extant echimyids leads us to propose a new higher level classification of two subfamilies: Euryzygomatomyinae and Echimyinae. Of note, the enigmatic Carterodon displays fast-evolving mitochondrial and nuclear sequences, with a long branch that destabilizes the deepest divergences of the echimyid tree, thereby challenging the sister-group relationship between Capromyidae and Euryzygomatomyinae. Biogeographical analyses involving higher level taxa show that several vicariant and dispersal events impacted the evolutionary history of echimyids. The diversification history of Echimyidae seems to have been influenced by two major historical factors, namely (1) recurrent connections between Atlantic and Amazonian Forests and (2) the Northern uplift of the Andes.

Phylogeographic Structure and Karyotypic Diversity of the Brazilian Shrew Mouse (Blarinomys breviceps, Sigmodontinae) in the Atlantic Forest

Blarinomys breviceps possesses cryptic and burrowing habits with poorly documented genetics and life history traits. Due to its rarity, only a few specimens and DNA sequences have been deposited in collections worldwide. Here, we present the most comprehensive cytogenetic and molecular characterization of this rare genus. Phylogenetic analyses based on partial cytochrome b sequences were performed, attempting to establish the relationships among individuals with distinct karyotypes along the geographic distribution of the genus in the Atlantic Forest. Classical and molecular cytogenetics, using banding patterns and FISH of telomeric and whole chromosome X-specific painting probes (obtained from the Akodontini Akodon cursor) were used to characterize and compare the chromosomal complements. Molecular phylogenetic analyses recovered 2 main geographically structured clades, northeastern and southeastern with pairwise sequence divergences among specimens varying between 4.9 and 8.4%. Eight distinct karyomorphs are described: (A) 2n = 52 (50A, XX), (B) 2n = 52 (48A, XY+2Bs), (C) 2n = 45 (42A, XY+1B), (D) 2n = 43 (37A, XX+4Bs), (E) 2n = 37 (34A, XY+1B), (F) 2n = 34 (32A, XX), (G) 2n = 31 (27A, XX+2Bs), (H) 2n = 28 (26A, XY), all with the same number of autosomal arms (FNA = 50). Variation of 0–4 supernumerary chromosomes (Bs) presenting heterogeneity in morphology and distribution of interstitial telomeric sequences (ITSs) is reported. ITSs are also found in some metacentric autosomes. The phylogeographic separation between 2 major lineages with high levels of genetic divergence, and the wide karyotypic diversity indicate that B. breviceps is a diverse group that warrants taxonomic re-evaluation.

Molecular Diagnosis of Atlantic Forest Mammals Using Mitochondrial DNA Sequences: Didelphid Marsupials

Most living species of New World marsupials are classified in the family Didelphidae, with 98 species and 18 genera currently recognized. We sequenced fragments of two mitochondrial genes of didelphid marsupials from the At- lantic Forest of eastern South America, a biodiversity hotspot. We evaluated sequence divergences within and among spe- cies and contrasted the efficiency of cytochrome c oxidase subunit I (COI) with cytochrome b (CytB) in species-level di- agnosis. The average intraspecific genetic divergence of COI and CytB was 2.0% and 1.9%, respectively; which was about five times lower than the comparison among species of the same genus (11.2 and 10.8%). In both genes, divergence levels among closely related species are usually higher than within species. The barcoding gap is similar in COI and CytB, indicating that either gene can be used in molecular diagnoses of didelphid species. DNA barcodes are a welcome addition to traditional taxonomic methods when viewed as additional diagnostic characters in the context of integrative taxonomy.

The phylogenetic position of the enigmatic Atlantic forest-endemic spiny mouse Abrawayaomys (Rodentia: Sigmodontinae)

BackgroundThe phylogenetic position of the sigmodontine genus Abrawayaomys, historically assigned to the tribe Thomasomyini or considered a sigmodontine incertae sedis, was assessed on the basis of nuclear and mitochondrial DNA sequences obtained from four individuals from different localities in the Atlantic forest of Brazil. Sequences of Abrawayaomys were analyzed in the context of broad taxonomic matrices by means of maximum-likelihood (ML) and Bayesian analyses (BA).ResultsThe phylogenetic position of Abrawayaomys differed depending on the gene analyzed and the analysis performed (interphotoreceptor retinoid-binding protein (IRBP) ML: sister to Thomasomyini; IRBP BA: sister to Akodontini; cytochrome (Cyt) b ML: sister to Neotomys; and Cyt b BA: sister to Reithrodontini). With the sole exception of the BA based on Cyt b sequences, where the Abrawayaomys-Reithrodon clade had strong support, all sister-group relationships involving Abrawayaomys lacked any significant support.ConclusionsAs such, Abrawayaomys constitutes the only representative so far known of one of the main lineages of the sigmodontine radiation, differing from all other Atlantic forest sigmodontine rodents by having a unique combination of morphological character states. Therefore, in formal classifications, it should be regarded as a Sigmodontinae incertae sedis.

Morphological diagnosis and geographic distribution of Atlantic Forest red-rumped mice of the genus Juliomys (Rodentia: Sigmodontinae)

Recognition and identification of red-rumped mice of the genus Juliomys Gonzalez, 2000 has been a problem among many mammalogists, and specimens of this genus are commonly confused with other Atlantic Forest sigmodontine rodents. Herein we provide an expanded diagnosis for the genus based on the analyses of the three living species of Juliomys, and provide morphological comparisons to the small bodied and bright colored rodents Rhagomys rufescens (Thomas, 1886) and Oligoryzomys flavescens (Waterhouse, 1837), which occur in sympatry with Juliomys spp. in forested areas of southeastern Brazil. These taxa are superficially similar, and are therefore commonly misidentified in the field and museum collections. We also provide morphometric data and a key to the living species of Juliomys, and an updated distribution map of the genus and its species.