Correction: Amphibians on the hotspot: Molecular biology and conservation in the South American Atlantic Rainforest.

[This corrects the article DOI: 10.1371/journal.pone.0224320.].

Amphibians on the hotspot: Molecular biology and conservation in the South American Atlantic Rainforest.

Amphibians are the focus of a recent debate and public attention owing to the global decline in their populations worldwide. Amphibians are one of the most threatened and poorly known groups of vertebrates in several geographic areas, even though they play a central role in their own ecosystems. At different levels, amphibians make their contribution to proper ecosystem functioning. They act as regulators of the food web and nutrient cycling, and they also provide several valuable ecosystem services, e.g., as a food source and as animal models for lab research. In this sense, it seems clear that the maintenance of amphibian diversity should be one of the major goals for the several countries where their population decline is observed. However, we are still struggling with the very first step of this process, i.e., the correct identification of the amphibian species diversity. Over the past few decades, research on molecular identification of amphibians using DNA barcoding has encountered some difficulties related to high variability in the mitochondrial genome of amphibians, and a research gap is noticeable in the literature. We herein evaluated both COI and 16S rRNA mitochondrial genes for the molecular identification of frogs and tadpoles in a large fragment of the South American Atlantic Rainforest in Rio de Janeiro, Brazil. Our results suggest that both COI and 16S rRNA are informative markers for the molecular identification of the amphibian specimens with all specimens unambiguously identified at the species level. We also made publicly available 12 new sequences of Atlantic Rainforest amphibian species for the first time, and we discussed some conservation issues related to amphibians within the Atlantic Rainforest domains in the state of Rio de Janeiro, Brazil.

Lizard assemblages on sandy coastal plains in southeastern Brazil: An analysis of occurrence and composition, and the role of habitat structure.

Data on the structure of lizard communities in the different biomes and ecosystems of Brazil are still limited. In this study, we related the species richness, abundance and the spatial occurrence of lizards to the structure of the vegetation found on the coast of the state of Espírito Santo, southeastern Brazil, to determine whether habitat influences the structure of lizard communities. We conducted fieldwork in 2012, 2013 and 2014, collecting data in standardized samples. We analyze whether variables of vegetation structure influenced species richness and abundance, using Generalized Linear Models (GLMs). We recorded 12 lizard species from eight families. In general, species richness and abundance were similar among sites. Locally, we recorded the highest species richness in shrubby vegetation, open Clusia vegetation, and the restinga forest zone. Bromeliads explained the occurrence of teiids, although there was no systematic relationship between species richness and vegetation structure. Our results provide important insights into the characteristics of the lizard communities found on sandy coastal plains and contribute to the conservation of these species in these ecosystems.

Helminth infections in a pair of sympatric congeneric lizard species.

We analyzed parameters of parasitism by helminths in a pair of sympatric congeneric lizard species (Tropidurus hispidus and Tropidurus semitaeniatus). Differences in their supracommunities (richness, composition, and abundance) and the influence of helminthic loads on minimum flight initiation distances and body temperatures were evaluated. We reported new findings of Piratuba digiticauda infecting T. hispidus and Oochoristica bresslaui infecting T. semitaeniatus. Parapharyngodon alvarengai was the most abundant helminth in both host species. Tropidurus hispidus individuals hosted a higher abundance and richness of helminths than T. semitaeniatus, with females of the former having larger helminthic loads than males. Dissimilarities between host species may be attributed to differences in their utilization of niche dimensions (time, food, and structural and thermal space), the occurrence of morphological differences that result in differential exposure to the sources and agents of infection, and/or differential immunological functions. Our data suggests that infection by P. alvarengai led to some limitations in locomotor performance of T. hispidus resulting in decreased minimum flight initiation distance as infection rates increased. Individuals opted for a prolonged period of immobility to avoid capture. There was a negative relationship between helminthic loads and body temperatures in T. semitaeniatus, possibly due to decreased activity and thermoregulation rates, and increased use of shelters by lizards with high infection levels to avoid predation.

Lizard assemblage from a sand dune habitat from southeastern Brazil: a niche overlap analysis.

Communities are structured by interactions of historical and ecological factors, which influence the use of different resources in time and space. We acquired data on time of activity, microhabitat use and diet of a lizard assemblage from a sand dune habitat in a coastal area, southeastern Brazil (Restinga de Jurubatiba). We analyzed the data of niche overlap among species in these three axes (temporal, spatial and trophic) using null models. We found a significant overlap within the trophic niche, whereas the overlap for the other axes did not differ from the expected. Based on this result, we discuss the factors acting on the structure of the local lizard community.

Ecology of the bromeligenous frog Phyllodytes luteolus (Anura, Hylidae) from three restinga remnants across Brazil's coast.

In this study, we analyzed diet, sexual dimorphism and bromeliad use in three populations of the hylid frog Phyllodytes luteolus from restinga habitats along the Brazilian coast. We found 13 arthropods categories in 161 stomachs. Ants and termites were the dominant prey items. The similar trophic niche across populations suggests this species has a conservative diet. We found sexual dimorphism regarding body size and jaw width. We recordedP. luteolus in five bromeliad species, but predominantly inAechmeablanchetiana (35.6% of individuals recorded). We recorded solitary individuals in 44% of occupied bromeliads, and never found two males sharing the same bromeliad. The data is suggestive that populations ofP. luteolus has a conservative diet independent of area, with ants and termites the being most relevant prey items. The sexual dimorphism in jaw and the solitary males may suggest that this species have territorial behavior.

Bromeliad treefrogs as phoretic hosts of ostracods.

Aquatic organisms can use many methods of dispersal among discrete freshwater habitats, and phoresy is an important but poorly understood mechanism. Tank bromeliads are small and unconnected habitats used by many animals, and some of them use phoresy for dispersal. Ostracods living in bromeliads used treefrogs as phoretic hosts for dispersal. We investigated the distribution of phoretic ostracods among body parts of treefrogs (Scinax littoreus and Scinax perpusillus), the prevalence and intensity of ostracods (Elpidium sp.) between Scinax species, and the prevalence and mean intensity of ostracods among the frogs in wet vs. dry seasons in two inselbergs areas at Rio de Janeiro State (Brazil). There were significant differences among the body parts occupied by ostracods and between the Scinax species. Seasonal differences were found only for S. littoreus showing greater abundance during the wet season. Additionally, we record Scinax cuspidatus and Thoropa miliaris as new phoretic hosts for Elpidium sp. to use phoresy.

Feeding habits of the leaf litter frog Haddadus binotatus (Anura, Craugastoridae) from two Atlantic Forest areas in southeastern Brazil.

Haddadus binotatus is an endemic anuran of the Brazilian Atlantic Forest and currently, there is no information about the diet of this species. We analyzed the diet of two populations of this anuran in two states in southeast Brazil. Samplings were carried out in 2004 in the state of Rio de Janeiro and in 2009 and 2010 in the state of Espírito Santo. Haddadus binotatus presented a rich diet composition, preying 19 prey types. Orthoptera, Coleoptera, and Blattodea were the most important preys in the Rio de Janeiro population, and Orthoptera, Araneae and Hemiptera were the most important in the Espírito Santo population. The diet composition differed numerically between the two localities, but not in terms of volume, which can reflect local differences in the prey availability in the two habitats. The jaw width limited the size of prey, which is expected for predators who swallow the preys without chewing. The proportion of individuals with empty stomachs was higher in the Rio de Janeiro population (39.2%) than in the Espírito Santo population (17.9%), suggesting that the former could be in a lower energy balance. The females of the species were larger than the males, which may result from the production of larger eggs.

Habitat structural effect on squamata fauna of the restinga ecosystem in northeastern Brazil.

In this work, we surveyed data on richness and composition of squamatan reptiles and habitat structural effect in nine areas of restinga ecosystem in the State of Bahia, northeastern Brazil. The "restinga" ecosystems are coastal sand dune habitats on the coast of Brazil. Our main hypothesis is that the Squamata fauna composition along these restinga areas would be modulated by habitat structural. After 90 days of field sampling we recorded approximately 5% of reptile species known in Brazil. The composition of Squamata assemblages varied mainly based on the presence or absence of lizards of the genera Ameivula and Tropidurus. Our data showed that habitat structure consistently affected the composition of local Squamata fauna, especially lizards.

Clutch size in populations and species of cnemidophorines (Squamata: Teiidae) on the eastern coast of Brazil.

We analyzed some reproductive aspects of 16 coastal populations, belonging to five lizard species (A. ocellifera, A. abaetensis, A. nativo, A. littoralis and C. lacertoides) from different restinga habitats along the eastern coast of Brazil. This study aimed to evaluate to what extent the reproductive aspects vary geographically and among species. For each female, we recorded the number of vitellogenic follicles, size and color of the largest follicle, presence and size of corpora lutea, and number and size of oviductal eggs. Clutch size of almost all coastal populations/species of Ameivula had little variation and most clutches were composed of two eggs. There was a significant relationship between female size and the mean clutch size when females from different species were pooled. Mean egg volume, among species, varied from 420 to 655 mm3. Relative clutch mass varied from 0.129 to 0.159 and did not differ significantly among species. We concluded that the five coastal species studied (four bisexuals and one parthenogenetic) had similar reproductive characteristics. Most of them presented multiple clutches, low clutch size and low relative clutch mass, similar to other species in the genus and to unisexual and bisexual species of the Teiidae family.

Cryptic genetic diversity is paramount in small-bodied amphibians of the genus Euparkerella (Anura: Craugastoridae) endemic to the Brazilian Atlantic forest.

Morphological similarity associated to restricted distributions and low dispersal abilities make the direct developing "Terrarana" frogs of the genus Euparkerella a good model for examining diversification processes. We here infer phylogenetic relationships within the genus Euparkerella, using DNA sequence data from one mitochondrial and four nuclear genes coupled with traditional Bayesian phylogenetic reconstruction approaches and more recent coalescent methods of species tree inference. We also used Bayesian clustering analysis and a recent Bayesian coalescent-based approach specifically to infer species delimitation. The analysis of 39 individuals from the four known Euparkerella species uncovered high levels of genetic diversity, especially within the two previously morphologically-defined E. cochranae and E. brasiliensis. Within these species, the gene trees at five independent loci and trees from combined data (concatenated dataset and the species tree) uncovered six deeply diverged and geographically coherent evolutionary units, which may have diverged between the Miocene and the Pleistocene. These six units were also uncovered in the Bayesian clustering analysis, and supported by the Bayesian coalescent-based species delimitation (BPP), and Genealogical Sorting Index (GSI), providing thus strong evidence for underestimation of the current levels of diversity within Euparkerella. The cryptic diversity now uncovered opens new opportunities to examine the origins and maintenance of microendemism in the context of spatial heterogeneity and/or human induced fragmentation of the highly threatened Brazilian Atlantic forest hotspot.

Diet and nematode infection in Proceratoprhys boiei from two Atlantic rainforest remnants in Southeastern Brazil.

Proceratophrys boiei is an endemic cycloramphid anuran inhabiting the leaf litter of Atlantic rainforests in Southeastern Brazil. We analyzed the whole digestive tract of 38 individuals of Proceratophrys boiei collected in two Atlantic Rainforest areas in the state of Rio de Janeiro, Brazil, to study the diet composition and the helminth fauna associated with this species. The main food items in P. boiei's diet were Coleoptera, Orthoptera and Blattaria. Five nematode species were found: Aplectana delirae, Cosmocerca parva, Oxyascaris oxyascaris, Physaloptera sp. (larval stage only) and an unidentified nematode. Overall prevalence was 71% and mean infection intensity was 7.3 ± 5.8 neatodes per individual.

Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic rainforest remnants in Southeastern Brazil

Proceratophrys boiei is an endemic cycloramphid anuran inhabiting the leaf litter of Atlantic rainforests in Southeastern Brazil. We analyzed the whole digestive tract of 38 individuals of Proceratophrys boiei collected in two Atlantic Rainforest areas in the state of Rio de Janeiro, Brazil, to study the diet composition and the helminth fauna associated with this species. The main food items in P. boiei's diet were Coleoptera, Orthoptera and Blattaria. Five nematode species were found: Aplectana delirae, Cosmocerca parva, Oxyascaris oxyascaris, Physaloptera sp. (larval stage only) and an unidentified nematode. Overall prevalence was 71 percent and mean infection intensity was 7.3 ± 5.8 neatodes per individual.

Proceratophrys boiei é um anuro da familia Cycloramphidae que vive no folhico e é endêmico de areas de floresta na Mata Atlantica do Sudeste do Brasil. Nós analisamos o trato digestivo de 38 indivíduos de Proceratophrys boiei provenientes de duas áreas de Mata Atlântica no Estado do Rio de Janeiro, Brasil, para estudar a composição da dieta e a fauna helmíntica associada a esta espécie. s principais itens alientares na dieta de P. boiei fora Coleoptera, rthoptera e Blattaria. Cinco espécies de nematóides foram encontradas: Aplectana delirae, Cosmocerca parva, Oxyascaris oxyascaris, Physaloptera sp. (apenas larvas) e uma espécie de nematóide não identificada. A prevalência total foi de 71 por cento e a intensidade media de infecção foi de 7,3 ± 5,8 nematóides por indivíduo.

Parameters from the community of leaf-litter frogs from Estação Ecológica Estadual Paraíso, Guapimirim, Rio de Janeiro State, southeastern Brazil

We studied the leaf-litter frog community of Estação Ecológica Estadual Paraíso, in Guapimirim, Rio de Janeiro State, southeastern Brazil. Herein we combined three sampling methods (large plots, visual encounter surveys and pit-fall traps) to present data on species composition, richness, relative abundance and densities. The local assemblage of frogs associated to the leaf-litter was composed by 14 species, belonging to nine families. Haddadus binotatus, a direct-developing frog, was the most abundant species in the community. The estimated density of the local leaf-litter frog assemblage based on plot sampling was 4.3 frogs/100 m². Haddadus binotatus had the highest density (1.1 ind/100 m²). Frogs were predominantly found at night. Thoropa miliaris had the largest values of SVL (39.0 ± 10.3 mm), whereas the smallest species were Euparkerella brasiliensis (16.7 ± 2.2 mm) and E. cochranae (16.0 ± 2.7 mm). Rhinella ornata had the highest mean body mass (12.1 ± 7.5 g), and E. cochranae the lowest (0.4 ± 0.2 g). The overall frog mass was 938.6 g/ha. Our data support that higher densities of leaf-litter frogs tend to occur in the Neotropical region compared to the OldWorld tropics, tending to be higher in Central America than in South America.

Estudamos a comunidade de anuros de folhiço da EstaçãoEcológica Estadual Paraíso, em Guapimirim, estado do Rio de Janeiro, no sudeste do Brasil. Combinamos três métodosde amostragem (plots, transectos e armadilhas de queda) para apresentar dados sobre a composição de espécies, riqueza,abundância relativa e densidade. A assembleia local foi composta por 14 espécies de anuros, pertencentes a nove famílias. Haddadus binotatus, espécie de desenvolvimento direto, foi a mais abundante durante o estudo. A densidade de anuros de folhiço estimada com base na amostragem por plots foi de4,3 ind/100m². Haddadus binotatus apresentou a maior densidade (1,1 ind/100m²). Os anuros foram registrados predominantemente durante a noite. Thoropa miliaris apresentou os maiores valores de CRC (39,0 ± 10,3 mm). As menores espécies foram Euparkerella brasiliensis (16,7 ± 2,2 mm) e E. cochranae (16,0 ± 2,7mm). Rhinella ornata apresentou a maior massa corporal média (12,1 ± 7,5 g) e E. cochranae (0,4 ± 0,2 g) a menor. A massa média total foi de 938,6 g/ha. Nossos resultados corroboram com a tendência de maiores densidades de anuros de folhiço na região Neotropical quando comparado com áreas Tropicais do Velho Mundo, tendendo a serem maiores na América Central do que na América do Sul.

Parameters from the community of leaf-litter frogs from Estação Ecológica Estadual Paraíso, Guapimirim, Rio de Janeiro State, southeastern Brazil.

We studied the leaf-litter frog community of Estação Ecológica Estadual Paraíso, in Guapimirim, Rio de Janeiro State, southeastern Brazil. Herein we combined three sampling methods (large plots, visual encounter surveys and pit-fall traps) to present data on species composition, richness, relative abundance and densities. The local assemblage of frogs associated to the leaf-litter was composed by 14 species, belonging to nine families. Haddadus binotatus, a direct-developing frog, was the most abundant species in the community. The estimated density of the local leaf-litter frog assemblage based on plot sampling was 4.3 frogs/100 m(2). Haddadus binotatus had the highest density (1.1 ind/100 m(2)). Frogs were predominantly found at night. Thoropa miliaris had the largest values of SVL (39.0 ± 10.3 mm), whereas the smallest species were Euparkerella brasiliensis (16.7 ± 2.2 mm) and E. cochranae (16.0 ± 2.7 mm). Rhinella ornata had the highest mean body mass (12.1 ± 7.5 g), and E. cochranae the lowest (0.4 ± 0.2 g). The overall frog mass was 938.6 g/ha. Our data support that higher densities of leaf-litter frogs tend to occur in the Neotropical region compared to the OldWorld tropics, tending to be higher in Central America than in South America.

Herpetofauna of an Atlantic rainforest area (Morro São João) in Rio de Janeiro State, Brazil

We studied the herpetofaunal community from the Atlantic forest of Morro São João, in Rio de Janeiro State, Brazil, and present data on species composition, richness, relative abundance and densities. We combined three sampling methods: plot sampling, visual encounter surveys and pit-fall traps. We recorded sixteen species of amphibians and nine of reptiles. The estimated densities (based on results of plot sampling) were 4.5 ind/100 m2 for amphibians and 0.8 ind/100 m² for lizards, and the overall density (amphibians and lizards) was 5.3 ind/100 m². For amphibians, Eleutherodactylus and Scinax were the most speciose genera with three species each, and Eleutherodactylus binotatus was the most abundant species (mean density of 3.0 frogs/100 m²). The reptile community of Morro São João was dominated by species of the families Gekkonidae and Gymnophtalmidae (Lacertilia) and Colubridae (Serpentes). The gymnophtalmid lizard Leposoma scincoides was the most abundant reptile species (mean density of 0.3 ind/100 m²). We compare densities obtained in our study data with those of other studied rainforest sites in various tropical regions of the world.

Estudamos a comunidade herpetofaunística da Mata Atlântica do Morro São João, Estado do Rio de Janeiro, Brasil, e apresentamos dados da composição, riqueza, abundância relativa e densidade das espécies. Combinamos três metodologias de amostragem: parcelas, encontros visuais e armadilhas de queda. Registramos 16 espécies de anfíbios e 9 espécies de répteis. As densidades estimadas (baseadas nos resultados da amostragem através de parcelas) foram 4.5 ind/100 m² para anfíbios, 0.8 ind/100 m² para lagartos, e a densidade total (anfíbios e répteis) foi 5.3 ind/100 m². Para anfíbios, Eleutherodactylus e Scinax foram os gêneros com maior número de espécies, com três espécies cada, e Eleutherodactylus binotatus foi a espécie mais abundante (densidade média de 3.0 anuros/100 m²). A comunidade de répteis do Morro São João foi dominada por espécies da família Gekkonidae e Gymnophtalmidae (Lacertilia) e Colubridae (Serpentes). O lagarto gimnoftalmídeo Leposoma scincoides foi a espécie de réptil mais abundante (densidade média de 0.3 ind/100 m). Comparamos os dados de densidade obtidos no nosso estudo com os de outros estudos em florestas de várias regiões tropicais do mundo.

Herpetofauna of an Atlantic rainforest area (Morro São João) in Rio de Janeiro State, Brazil.

We studied the herpetofaunal community from the Atlantic forest of Morro São João, in Rio de Janeiro State, Brazil, and present data on species composition, richness, relative abundance and densities. We combined three sampling methods: plot sampling, visual encounter surveys and pit-fall traps. We recorded sixteen species of amphibians and nine of reptiles. The estimated densities (based on results of plot sampling) were 4.5 ind/100 m2 for amphibians and 0.8 ind/100 m2 for lizards, and the overall density (amphibians and lizards) was 5.3 ind/100 m2. For amphibians, Eleutherodactylus and Scinax were the most speciose genera with three species each, and Eleutherodactylus binotatus was the most abundant species (mean density of 3.0 frogs/100 m2). The reptile community of Morro São João was dominated by species of the families Gekkonidae and Gymnophtalmidae (Lacertilia) and Colubridae (Serpentes). The gymnophtalmid lizard Leposoma scincoides was the most abundant reptile species (mean density of 0.3 ind/100 m2). We compare densities obtained in our study data with those of other studied rainforest sites in various tropical regions of the world.