Pleistocene expansion and connectivity of mesic forests inside the South American Dry Diagonal supported by the phylogeography of a small lizard*

Traditionally focused on Amazonian and Atlantic rainforests, studies on the origins of high Neotropical biodiversity have recently shifted to also investigate biodiversity processes in the South American dry diagonal, encompassing Chaco, Cerrado savannas, and Caatinga seasonally dry tropical forests. The plateau/depression hypothesis states that riparian forests in the Brazilian Shield in central Brazil are inhabited by Pleistocene lineages, with shallow divergences and signatures of population expansion. Moreover, riparian forests may have acted as a vegetation network in the Pleistocene, allowing gene/species flow across the South American dry diagonal. We tested these hypotheses using Colobosaura modesta, a small gymnophthalmid lizard from forested habitats in the Cerrado savannas and montane/submontane forests in the Caatinga. We conducted phylogeographic analyses using a multi-locus dataset, tested alternative demographic scenarios with Approximate Bayesian Computation, and also employed species delimitation tests. We recovered a history of recent colonization and expansion along riparian forests, associated with Pleistocene climate shifts, and the existence of a new species of Colobosaura restricted to the Serra do Cachimbo region. We also present evidence that riparian forests have provided an interconnected network for forest organisms within the South American dry diagonal and that Pleistocene events played an important role in their evolutionary history.     

Tiny steps towards greater knowledge: An osteological review with novel data on the Atlantic Forest toadlets of the Brachycephalus ephippium species group

Brachycephalus is a small, endemic genus of anurans that occur throughout the Brazilian Atlantic Forest. Recent analyses corroborated the monophyly of two species groups within this genus (B. ephippium and B. pernix), whereas the B. didactylus group appears to be polyphyletic. Herein, we compare and describe the skeletal system of all species from the Brachycephalus ephippium species group. We investigated diagnostic characters that are potentially useful to delimit similar species, confirmed the previously proposed genus definition and added six extra characters. We propose an osteological diagnosis for each species of the B. ephippium group, evaluating and describing intraspecific variations. Our results suggest that adults of B. ephippium group have ornamented parotic plates, ornamented post-orbital crests, absence of quadratojugal and neopalatines, distal end of the otic ramus of squamosal expanded towards the parotic plate, reduced zygomatic ramus of the squamosals, posterolateral projection of the crista parotica, presence of ornamented spinal plates (except B. alipioi) and ornamented paravertebral plates. We highlighted the importance of including more than one specimen per species when dealing with miniaturized taxa. A comparison with other Brachycephalus species groups and with Ischnocnema was also provided. Lastly, we suggest some characters to be included in future phylogenetic analysis.     

Evolutionary diversification of spiny rats (genus Trinomys, Rodentia: Echimyidae) in the Atlantic Forest of Brazil

Phylogenetic and phylogeographic relationships within and among species of the Atlantic Forest spiny rat Trinomys (family Echimyidae) were examined using cytochrome b sequence data. Levels of sequence divergence among species of Trinomys are as high as those found among taxa of echimyids that are recognized as different genera. Trinomys contains three distinct monophyletic clades that show a striking concordance with vegetational distribution. Haplotypes of clade 1 are distributed along the coastal margins of southeastern Brazil, following the moist tropical forest. Members of clade 2 are found in the semi-deciduous tropical forest. T. albispinus represents clade 3 and is found in a more xeric vegetation. Estimates of divergence times separating the three clades are very deep and range from 1.6 to 7.4 millions of years, predating the climatic fluctuations of the Pleistocene. Therefore, the proposed Late Pleistocene refugia in the Atlantic Forest cannot account for the divergence of the clades of Trinomys , but most likely shaped the modern distribution of species. The current taxonomy of this group does not reflect the diversity and phylogenetic relationships of the named species. However, morphological characters are congruent with the phylogeny uncovered by the molecular data. An extensive taxonomic rearrangement is suggested, reflecting phylogenetic relationships of monophyletic entities within the genus Trinomys , degree of sequence differences, and morphological diagnosability.     

Climatic oscillations shape the phylogeographical structure of Atlantic Forest fire‐eye antbirds (Aves: Thamnophilidae)

In the present study, mitochondrial (mt)DNA sequence data were used to examine the genetic structure of fire‐eye antbirds (genus Pyriglena) along the Atlantic Forest and the predictions derived from the river hypothesis and from a Last Glacial Maximum Pleistocene refuge paleomodel were compared to explain the patterns of genetic variation observed in these populations. A total of 266 individuals from 45 populations were sampled over a latitudinal transect and a number of phylogeographical and population genetics analytical approaches were employed to address these questions. The pattern of mtDNA variation observed in fire‐eye antbirds provides little support for the view that populations were isolated by the modern course of major Atlantic Forest rivers. Instead, the data provide stronger support for the predictions of the refuge model. These results add to the mounting evidence that climatic oscillations appear to have played a substantial role in shaping the phylogeographical structure and possibly the diversification of many taxa in this region. However, the results also illustrate the potential for more complex climatic history and historical changes in the geographical distribution of Atlantic Forest than envisioned by the refuge model. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 900–824.     

Phylogeography of the Petunia integrifolia complex in southern Brazil

In this study, we evaluated the genetic diversity of the Petunia integrifolia species group using a phylogeographical approach, and attempted to understand better its diversification and taxonomy. Plants from five morphological groups were collected, covering a large part of the geographical distribution of most of the species. Two major clades were found in the phylogenetic tree, and an additional lineage, corresponding to P. inflata, was found in the haplotype network obtained for plastid markers. All three lineages are clearly delimited geographically, but, with the exception of P. inflata, the morphological groups were not genetically distinct. Our results suggest that a population expansion after a size reduction resulted in the establishment of two distinct and allopatric groups c. 0.5 Mya, one group occurring in a geologically ancient area, and the other occurring in areas that were under the influence of a series of marine transgressions/regressions at the end of the Pleistocene. These two clades are evolutionarily significant units with significantly different allele frequencies in their nuclear genome and reciprocal monophyly in maternal, uniparentally inherited markers. All our results suggest that the morphology‐based taxonomy in this group does not reflect its evolutionary history, and revision of its species limits should incorporate the distribution of the genetic diversity. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 199–213.     

Phylogeography and cryptic introduction of the ragworm Hediste diversicolor (Annelida,Nereididae) in the Northwest Atlantic

Many benthic marine invertebrates show striking range disjunctions across broad spatial scales. Without direct evidence for endemism or introduction, these species remain cryptogenic. The common ragworm Hediste diversicolor plays a pivotal role in sedimentary littoral ecosystems of the North Atlantic as an abundant prey item and ecosystem engineer, but exhibits a restricted dispersal capacity that may limit connectivity at both evolutionary and ecological time scales. In Europe, H. diversicolor is subdivided into cryptic taxa and genetic lineages whose distributions have been modified by recent invasions. Its origin in the northwest Atlantic has not been adequately addressed. To trace the age and origin of North American ragworm populations, we analyzed mtDNA sequence data (COI) from the Gulf of Maine and Bay of Fundy (n=73 individuals) and compared our findings with published data from the northeast Atlantic. Our results together with previous data indicate that two species of the H. diversicolor complex have independently colonized the northwest Atlantic at least three different times, resulting in two distinct conspecific assemblages in the Bay of Fundy and Gulf of Maine (respectively) that are different from the species found in the Gulf of St. Lawrence. North American populations had significantly lower genetic diversity compared with populations in the northeast Atlantic, and based on patterns of shared identity, populations in the Bay of Fundy originated from the Baltic Sea and North Sea. Populations from the Gulf of Maine were phylogenetically distinct and most likely originated from unsampled European populations. Analyses of the North American populations revealed patterns of post‐colonization gene flow among populations within the Gulf of Maine and Bay of Fundy. However, we failed to detect shared haplotypes between the two regions, and this pattern of complete isolation corroborates a strong phylogeographic break observed in other species.     

Phylogeography of the cactophilic species Drosophila gouveai: demographic events and divergence timing in dry vegetation enclaves in eastern Brazil

Aim  The aim of this study was to assess the causal mechanisms underlying populational subdivision in Drosophila gouveai , a cactophilic species associated with xeric vegetation enclaves in eastern Brazil. A secondary aim was to investigate the genetic effects of Pleistocene climatic fluctuations on these environments.
Location  Dry vegetation enclaves within the limits of the Cerrado domain in eastern Brazil.
Methods  We determined the mitochondrial DNA haplotypes of 55 individuals (representing 12 populations) based on sequence data of a 483-bp fragment from the cytochrome c oxidase subunit II (COII) gene. Phylogenetic and coalescent analyses were used to test for the occurrence of demographic events and to infer the time of divergence amongst genetically independent groups.
Results  Our analyses revealed the existence of two divergent subclades (G1 and G2) plus an introgressed clade restricted to the southernmost range of D. gouveai . Subclades G1 and G2 displayed genetic footprints of range expansion and segregated geographical distributions in south-eastern and some central highland regions, east and west of the Paraná River valley. Molecular dating indicated that the main demographic and diversification events occurred in the late to middle Pleistocene.
Main conclusions  The phylogeographical and genetic patterns observed for D. gouveai in this study are consistent with changes in the distribution of dry vegetation in eastern Brazil. All of the estimates obtained by molecular dating indicate that range expansion and isolation pre-dated the Last Glacial Maximum, occurring during the late to middle Pleistocene, and were probably triggered by climatic changes during the Pleistocene. The current patchy geographical distribution and population subdivision in D. gouveai is apparently closely linked to these past events.     

Phylogeography and species limits in the Gymnodactylus darwinii complex (Gekkonidae, Squamata): genetic structure coincides with river systems in the Brazilian Atlantic Forest

Phylogenetic analyses based on mtDNA cytochrome  b were performed in 42 lizards of the Gymnodactylus darwinii complex from three regions within Brazil's Atlantic Forest. Mainland regions and continental shelf islands in the south-eastern range and mainland areas from the north-east were sampled. The criteria of maximum parsimony (MP), maximum likelihood (ML) and Bayesian methods were explored, with the robustness for nodes assessed by bootstrapping (MP and ML) and posterior probabilities (Bayesian searches). By all methods, three distinctive phylogroups were recovered: a south-eastern clade (SE) and two clades from northern regions (NE₁ and NE₂). The pattern of genetic structure of the major clades coincided with the presence of river systems in the Atlantic Forest, and based on corrected genetic distances between those clades, divergence times were tentatively estimated using mtDNA rates calibrated for squamate reptiles. The putative role of Atlantic Forest rivers in generating differentiation is discussed. We present a hypothesis of species limits for G. darwinii , based on concordant lines of evidence including cytogenetic and mtDNA analyses. Two chromosome races (cytotype A, 2n = 38; and cytotype B, 2n = 40) had distributions concordant with clades SE and NE₁ + NE₂, respectively. These races are interpreted to be full species on the basis of a number of empirical criteria.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 13–26.     

Habitat fragmentation,EFN‐bearing trees and ant communities: Ecological cascades in Atlantic Forest of northeastern Brazil

Habitat fragmentation has a marked impact on the functional composition of tropical forest tree assemblages, and such change is likely to cascade through other trophic levels. Here, we investigate how habitat fragmentation affects extrafloral nectary (EFN)‐bearing plants and ant functional groups known to attend EFNs in a fragmented landscape of the Atlantic Forest. Extrafloral nectary‐bearing trees were identified in 50 0.1‐ha plots located in forest fragments, edge and interior patches. Ants were surveyed in 30 1‐m² litter samples in each of 17 forest fragments and in forest interior. Extrafloral nectary‐bearing plants accounted for 19.9% of individuals and 10.5% of species and included both pioneer and shade‐tolerant species similarly rich in the three habitat types. However, shade‐tolerant individuals accounted for >80% of EFN‐bearing plants in forest interior, compared with 2% in forest edge and 29% in fragments. Forest edge and fragment plots had a third fewer EFN‐bearing individuals and species compared with forest interior. This appeared to have important implications for local ant communities as the density of EFN‐bearing trees was the most important variable explaining the species richness of arboreal dominant ants. Our results show that plant loser–winner replacements promoted by forest fragmentation can cascade through higher trophic levels, with implications for forest dynamics and biodiversity conservation.     

Favolaschia in remnants of the Atlantic Forest,Brazil

The examination of recent collections of Favolaschia from remnants of the Atlantic Forest, Brazil, resulted in the identification of F. aurantiaca, F. cinnabarina and F. luteoaurantiaca sp. nov. Internal transcribed spacer (ITS) sequences obtained from these collections were introduced into the previously published phylogenetic tree of the genus to assess the position of these species within the Favolaschia clade. A maximum likelihood analysis generated a phylogenetic tree with a better resolution, especially for the clade that contains species belonging to section Favolaschia subsection Auriscalpium, where the three specimens collected in Brazil also were clustered in.     

Response of the ant community to attributes of fragments and vegetation in a northeastern Atlantic Rain Forest area, Brazil

The objective of this study was to determine the effects of forest fragmentation on ant richness in a landscape of Atlantic Forest in Northeast Brazil. More specifically, the ant richness was related to the attributes of fragments (area and distance from the fragment central point to the edge), landscape (forest cover surrounding the fragments), and tree community (plant density, richness, and percentage of shade tolerant species). The surveys were carried out in 19 fragments located in Alagoas State from October 2007 to March 2008. Samples were collected through a 300 m transect established in the center of each fragment, where 30 1-m2 leaf litter samples were collected at 10 m intervals. A total of 146 ant species was collected, which belonged to 42 genera, 24 tribes and nine subfamilies. The attributes of fragments and landscape did not influence ant richness. On the other hand, tree density explained ca. 23% of ant richness. In relation to functional groups, both density and richness of trees explained the richness of general myrmicines (the whole model explained ca. 42% of the variation in this group) and percentage of shade tolerant trees explained the richness of specialist predator ants (30% for the whole model). These results indicate that ant fauna is more influenced by vegetation integrity than by fragment size, distance to edge or forest cover surrounding fragments.     

Fragmentation causes rarity in common marmosets in the Atlantic forest of northeastern Brazil

The purpose of this study was to investigate the population status of the common marmosets, Callithrix jacchus, in one of their main habitats, the northeastern Atlantic forest of Brazil, where only 2% of its original area remains as small and isolated forest fragments, to determine long-term viable populations. The study was carried out in 15 forest fragments, measuring from 3,478.3 ha (the largest) to 6 ha, which were invariably subjected to high human impact. Line transect surveys were carried out between January 2002 and December 2004, along transects measuring from 350 to 4,000 m, between 0500 h and 0900 h. Common marmosets were registered in 73% (n = 11) of the forest fragments, were not recorded in the largest one, the Coimbra Forest, and group sizes varied from 1 to 4 individuals. A negative significant relationship was detected between the size of the fragment and the number of sightings of common marmosets. It is shown that the number of groups of common marmosets dwelling in this highly impacted landscape is nowadays lower than necessary for long-term survival. Additionally, smaller fragments having more groups suggests that they live in total association with humans, which assure their subsistence through the supply of introduced and exotic foods.     

Endophytic and mycorrhizal fungi associated with roots of endangered native orchids from the Atlantic Forest, Brazil

The composition and diversity of fungal communities associated with three endangered orchid species, Hadrolaelia jongheana, Hoffmannseggella caulescens, and Hoffmannseggella cinnabarina, found in different vegetation formations of the Atlantic Forest were determined by constructing clone libraries and by applying diversity and richness indices. Our results demonstrated the presence of Basidiomycetes. Sebacinales (81.61 %) and Cantharellales (12.10 %) were the dominant orders and are potential candidates for orchid mycorrhizal fungi. The Ascomycetes identified included the Helotiales (29.31 %), Capnodiales (18.10 %), and Sordariales (10.34 %), among others. These orders may represent potentially endophytic fungi. A Shannon–Wiener diversity index (H′) analysis showed a relatively high fungal community diversity associated with these tropical orchids. This diversity may offer greater flexibility in terms of the adaptation of the plants to changing environmental conditions and the potential facilitation of reintroduction programs. The Simpson diversity index values showed that all of the libraries included dominant species, and a LIBSHUFF analysis showed that the fungal communities were structurally different from each other, suggesting an influence of local factors on this diversity. This study offers important information for the development of conservation strategies for threatened and endemic species of Brazilian flora in an important and threatened hotspot.     

New material of Pachyarmatherium from the late Pleistocene of northeastern Brazil: insights into its morphology and systematics

A study of recently collected and other undescribed material of Pachyarmatherium brasiliense from the State of Pernambuco, Brazil, was performed, and its type material was revised, improving our understanding of this species and providing additional information on its affinities. Two fused osteoderms representing the posteriormost osteoderm row of the pectoral buckler are described for the first time in the Pachyarmatherium. Several additional specimens included buckler, border, and at least one caudal osteoderm. The relationships of Pachyarmatherium have been subject to different interpretations. We propose that the presence of some osteoderm features suggests a closer affinity with Dasypodinae/cf. Dasypodini armadillos. A key feature supporting this conclusion is the presence of complementary small figures in adjoining buckler osteoderms of Pachyarmatherium, indicating that a single scale covered portions of three contiguous osteoderms. Other features observed are related to the histological microstructure, which includes a central cortex characterized by a poorly developed cancellous bone and a deep cortex with mineralized collagen fiber bundles that are oriented roughly parallel to the deep osteoderm surface. Likewise, these histological features support its exclusion from glyptodonts and pampatheres, which show a different histological arrangement in their osteoderms.     

Biotic and abiotic determinants of Batrachochytrium dendrobatidis infections in amphibians of the Brazilian Atlantic Forest

Latitudinal gradients are linked to the dynamics of infectious diseases. Both prevalence and infection intensity of the amphibian-killing fungus, Batrachochytrium dendrobatidis (Bd), vary with latitude. Here, we tested whether abiotic and biotic factors are associated with Bd infection prevalence and intensity along a large latitudinal gradient across the Brazilian Atlantic Forest. We detected a positive association between infection prevalence and infection intensity with latitude; elevation, temperature and precipitation best explained infection prevalence, while temperature best explained infection intensity. We also detected a positive association between species richness and Bd infections and associations between Bd infections with host reproductive biology and habitat type. This represents the longest and most thoroughly sampled latitudinal gradient of Bd in anuran populations. Our results corroborate earlier findings that abiotic factors are a major determinant of Bd infections and highlight the need for a better understanding of the role that species diversity plays in disease outcomes.     

Birds and army ants in a fragment of the Atlantic Forest of Brazil

ABSTRACT Little is known about the birds associated with army‐ant swarms in the Brazilian Atlantic forest. Our objectives were to locate and monitor army‐ant swarms in the Atlantic rainforest of Brazil and to identify the species of birds that attended the swarms and exhibited bivouac‐checking behavior. From July 2004 to August 2005, we located 49 swarms of army ants, including 28 Eciton burchelli, 19 Labidus praedator, and 2 Eciton vagans swarms. No birds were present at 17 (35%) swarms. At 32 swarms where birds were present, 22 (69%) were E. burchelli swarms and 10 (31%) were L. praedator swarms. No birds were observed at the two E. vagans swarms. We identified 66 species of birds attending the swarms, but only 43 species were observed foraging on prey flushed by the ants. Eighteen of these species had not been previously reported to forage in association with army‐ant swarms. Most birds observed during our study attended army‐ant swarms opportunistically, with White‐shouldered Fire‐eyes (Pyriglena leucoptera) the only obligate ant follower. Our observations suggest that the arthropods and other organisms flushed by army ants represent an important food resource for several species of birds in the Atlantic forest ecosystem.     

Molecular phylogeny and biogeography of the eastern Tapaculos (Aves: Rhinocryptidae: Scytalopus, Eleoscytalopus): Cryptic diversification in Brazilian Atlantic Forest

Scytalopus and the recently erected Eleoscytalopus are among the Neotropical groups of birds whose taxonomy is most difficult to resolve given their very conservative morphology. We investigated the phylogeny and species limits of Eleoscytalopus and the eastern Scytalopus using two mitochondrial genes and two nuclear introns of multiple individuals from all species of these groups. The eastern Scytalopus are separated in three well defined clades also supported by morphological or vocal characteristics, although the relationships between these clades could not be resolved. We found several allopatric and very divergent lineages in these genera whose characteristics are consistent with species-level divergence, especially in S. speluncae. The great divergence between E. psychopompus and its sister species supports the former as a valid species. Our results corroborate the importance of the Bahia refuge as an avian center of endemism.