Quaternary climatic fluctuations influence the demographic history of two species of sky-island endemic amphibians in the Neotropics.

We evaluated the role of Quaternary climatic fluctuations on the demographic history and population structure of amphibian species endemic to the 'campo rupestre' in the Neotropics, evaluating their distributional shifts, demographic changes, and lineage formation from the end of Pleistocene to present. We chose two anurans endemic to the high-elevation 'campo rupestre' in the Espinhaço Range (ER) in northeastern and southeastern Brazil (Bokermannohyla alvarengai and Bokermannohyla oxente), as models to test the role of Quaternary climatic fluctuations over their distribution range in this region. We collected tissue samples throughout their distribution range and used statistical phylogeography to examine processes of divergence and population demography. We generated spatial-temporal reconstructions using Bayesian inference in a coalescent framework in combination with hind-cast projections of species distribution models (SDMs). We also used the results and literature information to test alternative diversification scenarios via approximate Bayesian computation (ABC). Our results show that Quaternary climatic fluctuations influenced the geographic ranges of both species showing population expansion during the last glacial maximum (LGM) and range contraction during interglacial periods, as inferred from selected ABC models and from past projections of SDMs. We recovered Pleistocene diversification for both species occuring in distinctly unique periods for each taxon. An older and range-restricted lineage was recovered in a geographically isolated geological massif, deserving conservation and further taxonomic study. The diversification and distribution of these amphibian species endemic to the Neotropical 'campo rupestre' were influenced by Quaternary climatic fluctuations. The expansion of cold adapted species restricted to higher elevations during glacial periods and their concomitant retraction during interglacial periods may have been crucial for producing patterns of species richness and endemism along elevation gradients in tropical and subtropical domains. Such processes may influence the evolution of the biota distributed in heterogeneous landscapes with varied topography.

A grave drum at rocky springs: the vocalization of Bokermannohyla alvarengai (Anura: Hylidae) from the Espinhaço Range, southeastern Brazil, with notes on its natural history.

Communication in anurans is mediated mainly by acoustic signals, which are relevant for mating, territoriality, and other social interactions (Wells 2007). Although these signals are usually conspicuous and relatively stereotyped, some Neotropical frogs display noticeable diversity and complexity in their calls. For instance, Bokermannohyla, a genus of gladiator treefrog from the Atlantic Forest, Cerrado, and Caatinga Biomes of Brazil, often have complex vocal repertoires (Carvalho et al. 2012; Nali Prado 2014), whilst some congeners have simple and stereotyped calls emitted continuously (Carvalho et al. 2013; Taucce et al. 2015; Giaretta et al. 2016; Rocha et al. 2016).

Modelling Highly Biodiverse Areas in Brazil.

Traditional conservation techniques for mapping highly biodiverse areas assume there to be satisfactory knowledge about the geographic distribution of biodiversity. There are, however, large gaps in biological sampling and hence knowledge shortfalls. This problem is even more pronounced in the tropics. Indeed, the use of only a few taxonomic groups or environmental surrogates for modelling biodiversity is not viable in mega-diverse countries, such as Brazil. To overcome these limitations, we developed a comprehensive spatial model that includes phylogenetic information and other several biodiversity dimensions aimed at mapping areas with high relevance for biodiversity conservation. Our model applies a genetic algorithm tool for identifying the smallest possible region within a unique biota that contains the most number of species and phylogenetic diversity, as well as the highest endemicity and phylogenetic endemism. The model successfully pinpoints small highly biodiverse areas alongside regions with knowledge shortfalls where further sampling should be conducted. Our results suggest that conservation strategies should consider several taxonomic groups, the multiple dimensions of biodiversity, and associated sampling uncertainties.

Almost a hundred years later, the advertisement call of Aparasphenodon brunoi Miranda-Ribeiro 1920 (Anura: Hylidae) from the Atlantic Forest.

The Neotropical genus Aparasphenodon Miranda-Ribeiro is composed of five recognized species commonly referred as "casque-headed frogs" (Frost 2018). Aparasphenodon brunoi Miranda-Ribeiro occurs in Atlantic Forest lowlands from the states of São Paulo to Bahia, Brazil (Feio et al. 1998; Mollo Neto Teixeira Jr. 2012; Ruas et al. 2013). The biology of most Aparasphenodon species is poorly known. Within the genus, until now only Aparasphenodon arapapa Pimenta, Napoli Haddad has its call formally described (Lourenço-de-Moraes et al., 2013, Forti et al., 2018, Guerra et al., 2018). Herein, we describe the advertisement call of Aparasphenodon brunoi Miranda-Ribeiro.

Modelling highly biodiverse areas in Brazil

Traditional conservation techniques for mapping highly biodiverse areas assume there to be satisfactory knowledge about the geographic distribution of biodiversity. There are, however, large gaps in biological sampling and hence knowledge shortfalls. This problem is even more pronounced in the tropics. Indeed, the use of only a few taxonomic groups or environmental surrogates for modelling biodiversity is not viable in mega-diverse countries, such as Brazil. To overcome these limitations, we developed a comprehensive spatial model that includes phylogenetic information and other several biodiversity dimensions aimed at mapping areas with high relevance for biodiversity conservation. Our model applies a genetic algorithm tool for identifying the smallest possible region within a unique biota that contains the most number of species and phylogenetic diversity, as well as the highest endemicity and phylogenetic endemism. The model successfully pinpoints small highly biodiverse areas alongside regions with knowledge shortfalls where further sampling should be conducted. Our results suggest that conservation strategies should consider several taxonomic groups, the multiple dimensions of biodiversity, and associated sampling uncertainties.

Modelling highly biodiverse areas in Brazil

Traditional conservation techniques for mapping highly biodiverse areas assume there to be satisfactory knowledge about the geographic distribution of biodiversity. There are, however, large gaps in biological sampling and hence knowledge shortfalls. This problem is even more pronounced in the tropics. Indeed, the use of only a few taxonomic groups or environmental surrogates for modelling biodiversity is not viable in mega-diverse countries, such as Brazil. To overcome these limitations, we developed a comprehensive spatial model that includes phylogenetic information and other several biodiversity dimensions aimed at mapping areas with high relevance for biodiversity conservation. Our model applies a genetic algorithm tool for identifying the smallest possible region within a unique biota that contains the most number of species and phylogenetic diversity, as well as the highest endemicity and phylogenetic endemism. The model successfully pinpoints small highly biodiverse areas alongside regions with knowledge shortfalls where further sampling should be conducted. Our results suggest that conservation strategies should consider several taxonomic groups, the multiple dimensions of biodiversity, and associated sampling uncertainties.

Past vicariance promoting deep genetic divergence in an endemic frog species of the Espinhaço Range in Brazil: The historical biogeography of Bokermannohyla saxicola (Hylidae).

The highland endemic frog Bokermannohyla saxicola occurs within the Espinhaço Range, the most extensive and continuous orogenic belt of the Brazilian territory, located in southeastern Brazil. We used mitochondrial DNA markers to test for spatial structure, to investigate the likely influence of past vicariant events, to evaluate demographic dynamics along the species range, and to understand the role of habitat discontinuities in promoting connectivity and diversity along the range. We found four major monophyletic lineages, each one associated with distinct mountain tops. The divergence time found between the four main clades clearly pre-dated the Pleistocene, except for the most recent separation. We observed no signs of population expansion for most of the sampling sites along the range, and a higher genetic diversity in the most continuous and central highland plateau, compared to smaller marginal regions. The Espinhaço Range harbors four deeply divergent lineages of B. saxicola within areas restricted by barriers for millions of years. These relatively isolated populations were kept apart by discontinuities represented by lowland habitats between mountain tops. Most of the lineage divergences occurred earlier than the Pleistocene, thus they cannot be solely explained by climatic oscillations of this epoch. However, within-lineage divergence times were all dated from the Pleistocene, suggesting an important effect in population dynamics. We also suggest that some marginal populations like those from Serra Negra and Serra de Itacambira can be the result of recent colonization events. Finally, in the southern Espinhaço region, the most continuous central highland area shows greater genetic diversity than the marginal discontinuous areas, where we have also observed a significant correlation between genetic and geographic distances. Bokermannohyla saxicola is a good model to study the biogeography of the Espinhaço Range because its high genetic structure reflects ancient as well as recent geological/climatic events, with important implications for conservation.

A new species of Pseudopaludicola Miranda-Ribeiro (Anura: Leptodactylidae: Leiuperinae) from eastern Brazil, with novel data on the advertisement call of Pseudopaludicola falcipes (Hensel).

The Neotropical genus Pseudopaludicola includes 21 species, which occur throughout South America. Recent studies suggested that the population of Andaraí, in the state of Bahia, is an undescribed species, related to P. pocoto. Herein we formally describe this new species from lowlands of eastern Brazil. Recognition of this new species is supported by adult morphology, advertisement call, karyotype, and molecular data. It is diagnosed mainly by its small size, terminal phalanges knobbed (lack any expansion of the digital tips), proportionally short hindlimbs, 11 pairs of chromosomes, and advertisement call composed of series of three-pulsed notes, emitted at a high rate. In addition, we report for the first time the presence of P. pocoto in the campo rupestre (rupestrian grasslands) of Chapada Diamantina, a population with a much darker dorsal coloration than the population from the type locality. We also redescribed the advertisement call of P. falcipes based on recordings from topotypic males.

Publisher Correction: Biodiversity conservation gaps in the Brazilian protected areas.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.

A new diploid species belonging to the Odontophrynus americanus species group (Anura: Odontophrynidae) from the Espinhaço range, Brazil.

The Odontophrynus americanus species group is a complex of diploid and tetraploid species hardly distinguished by morphological characters. It currently consists of three allopatric diploid species (i.e. O. cordobae, O. lavillai, and O. maisuma) and one widely distributed tetraploid species (i.e. O. americanus). We herein describe a new diploid allopatric species from campo rupestre, a typical phytophysiognomy of the Espinhaço Range, Brazil. The new species is distinguishable by the diploid complement of 2n = 2x = 22 chromosomes, small to medium-sized dorsal dark brown blotches with low contrast on a light brown background, light mid-dorsal stripe absent or greatly interrupted in most specimens with yellowish coloration as the background of both head and flanks of the body, advertisement call with dominant frequency of 840-1080 Hz, pulse rate of 90.5-106.7 pulses/s, and small tadpoles (TL = 24.30-35.69 mm).

Evolutionarily significant units of the critically endangered leaf frog Pithecopus ayeaye (Anura, Phyllomedusidae) are not effectively preserved by the Brazilian protected areas network.

Protected areas (PAs) are essential for biodiversity conservation, but their coverage is considered inefficient for the preservation of all species. Many species are subdivided into evolutionarily significant units (ESUs) and the effectiveness of PAs in protecting them needs to be investigated. We evaluated the usefulness of the Brazilian PAs network in protecting ESUs of the critically endangered Pithecopus ayeaye through ongoing climate change. This species occurs in a threatened mountaintop ecosystem known as campos rupestres. We used multilocus DNA sequences to delimit geographic clusters, which were further validated as ESUs with a coalescent approach. Ecological niche modeling was used to estimate spatial changes in ESUs' potential distributions, and a gap analysis was carried out to evaluate the effectiveness of the Brazilian PAs network to protect P. ayeaye in the face of climate changes. We tested the niche overlap between ESUs to gain insights for potential management alternatives for the species. Pithecopus ayeaye contains at least three ESUs isolated in distinct mountain regions, and one of them is not protected by any PA. There are no climatic niche differences between the units, and only 4% of the suitable potential area of the species is protected in present and future projections. The current PAs are not effective in preserving the intraspecific diversity of P. ayeaye in its present and future range distributions. The genetic structure of P. ayeaye could represent a typical pattern in campos rupestres endemics, which should be considered for evaluating its conservation status.

Biodiversity conservation gaps in the Brazilian protected areas.

Although Brazil is a megadiverse country and thus a conservation priority, no study has yet quantified conservation gaps in the Brazilian protected areas (PAs) using extensive empirical data. Here, we evaluate the degree of biodiversity protection and knowledge within all the Brazilian PAs through a gap analysis of vertebrate, arthropod and angiosperm occurrences and phylogenetic data. Our results show that the knowledge on biodiversity in most Brazilian PAs remain scant as 71% of PAs have less than 0.01 species records per km2. Almost 55% of Brazilian species and about 40% of evolutionary lineages are not found in PAs, while most species have less than 30% of their geographic distribution within PAs. Moreover, the current PA network fails to protect the majority of endemic species. Most importantly, these results are similar for all taxonomic groups analysed here. The methods and results of our countrywide assessment are suggested to help design further inventories in order to map and secure the key biodiversity of the Brazilian PAs. In addition, our study illustrates the most common biodiversity knowledge shortfalls in the tropics.

Biodiversity conservation gaps in the Brazilian protected areas

Although Brazil is a megadiverse country and thus a conservation priority, no study has yet quantified conservation gaps in the Brazilian protected areas (PAs) using extensive empirical data. Here, we evaluate the degree of biodiversity protection and knowledge within all the Brazilian PAs through a gap analysis of vertebrate, arthropod and angiosperm occurrences and phylogenetic data. Our results show that the knowledge on biodiversity in most Brazilian PAs remain scant as 71% of PAs have less than 0.01 species records per km(2). Almost 55% of Brazilian species and about 40% of evolutionary lineages are not found in PAs, while most species have less than 30% of their geographic distribution within PAs. Moreover, the current PA network fails to protect the majority of endemic species. Most importantly, these results are similar for all taxonomic groups analysed here. The methods and results of our countrywide assessment are suggested to help design further inventories in order to map and secure the key biodiversity of the Brazilian PAs. In addition, our study illustrates the most common biodiversity knowledge shortfalls in the tropics.

The advertisement call of Bokermannohyla flavopicta Leite, Pezzuti & Garcia, 2012 (Anura: Hylidae) from the mountains of Chapada Diamantina, Bahia, Brazil.

Bokermannohyla Faivovich, Haddad, Garcia, Frost, Campbell & Wheeler (2005) is a Brazilian treefrog genus currently composed of 32 species (Brandão et al. 2012; Leite et al. 2012; Frost 2015). The genus comprehends four, putatively monophyletic, species groups: B. circumdata, B. claresignata, B. martinsi, and B. pseudopseudis (sensu Faivovich et al. 2005). The B. pseudopseudis group includes nine species: B. alvarengai (Bokermann 1956), B. flavopicta Leite et al. 2012, B. ibitiguara (Cardoso 1983), B. itapoty Lugli & Haddad 2006a, B. oxente Lugli & Haddad 2006b, B. pseudopseudis (Miranda-Ribeiro 1937), B. sagarana Leite et al. 2011, B. sapiranga Brandão et al. 2012, and B. saxicola (Bokermann 1964).

A new species of Hatchet-faced Treefrog Sphaenorhynchus Tschudi (Anura: Hylidae) from Quadrilátero Ferrífero, Minas Gerais, southeastern Brazil.

A new species of Sphaenorhynchus is described from the Municipality of Mariana, State of Minas Gerais, Brazil. It is characterized by the vocal sac moderately developed, single, subgular, with longitudinal folds; white canthal and dorsolateral lines delimited below by a dorsolateral black line from the tip of snout extending beyond the eye to gradually disappearing up to the flanks; and premaxilla and maxilla almost completely edentulous, each bearing 1-5 extremely small teeth. It is most similar with Sphaenorhynchus orophilus, from which it can be distinguished by having a less robust forearm in males; glandular subcloacal dermal fold; premaxilla and maxilla almost completely edentulous; and larvae with large marginal papillae in the oral disc. The new species occurs in natural ponds over ironstone outcrops (known as canga) on flat terrain, where males call from the floating vegetation.

The tadpoles of two species of the Bokermannohyla circumdata group (Hylidae, Cophomantini).

We describe the external morphology and oral cavity of the tadpoles of Bokermannohyla caramaschii and B. diamantina respectively from the states of Espírito Santo and Bahia, Brazil. Larvae of both species are distinguished from each other by external characters such as body shape, labial tooth-row formula, number of marginal papillae, coloration and internal oral anatomy features. Some of the character states of the tadpoles of B. caramaschii and B. diamantina that are shared with all other described tadpoles of the Bokermannohyla circumdata group, such as the absence/reduction of small flaps with accessory labial teeth laterally in the oral disc, and the absence/reduction of submarginal papillae, may represent morphological synapomorphies of this species group, or at least of some internal clade. The general pattern of brownish coloration with longitudinal stripes on the caudal muscle is also common to most species of the group. We did not find character states of the oral cavity that are exclusively shared by species of the B. circumdata group, or by other groups of Bokermannohyla.

A new species of the Scinax catharinae group (Anura, Hylidae) from Serra da Canastra, southwestern state of Minas Gerais, Brazil.

We describe Scinax pombali sp. n. a new species of treefrog of the Scinax catharinae group from Serra da Canastra, municipality of Capitólio (20°36'03''S, 46°17'34.9''W, 987 m a.s.l.), located in the Cerrado domains of the State of Minas Gerais, Southeastern Brazil. The new species is characterized by its small size, blotches and color pattern on dorsal surface and hidden regions of flanks and thighs, canthus rostralis lightly concave and well marked, absent nuptial pad, and lack of externally differentiated inguinal gland. Additionally, we describe the tadpole of this new species, which is characterized by the large-sized oral disc and presence of a large number of marginal papillae (two to three rows on its dorsal portion and some rows in unorganized arrangement on its lateroventral portion).