Direct development in Atlantic Forest anurans: What can environmental and biotic influences explain about its evolution and occurrence?

Different environmental and biological factors can originate and support different alternative life histories in different taxonomic groups. Likewise, these factors are important for the processes that assemble and structure communities. Amphibians, besides being highly susceptible to environmental conditions, have various reproductive strategies, such as the direct development of individuals. Several hypotheses have been raised about possible selective pressures related to the emergence of direct development in anurans, as well as the relationship between environmental characteristics and the occurrence of these species. Such investigations, however, have mainly focused on specific clades and/or regions. Here, we use structural equation modelling to investigate the relationships between different abiotic (temperature, precipitation, humidity, and terrain slope) and biotic (phylogenetic composition and functional diversity) factors and the proportion of species with direct development in 766 anuran communities of the Atlantic Forest, a biome with a vast diversity of anuran species and high environmental complexity. Anuran communities with higher proportions of direct developing species were found to be mainly influenced by low potential evapotranspiration, low temperature seasonality, and high functional diversity. Phylogenetic composition and terrain slope were also found to be important in determining the occurrence of these species in Atlantic Forest communities. These results show the importance of these factors in the structuring of these communities and provide important contributions to the knowledge of direct development in anurans.

Pet distribution modelling: Untangling the invasive potential of Trachemys dorbigni (Emydidae) in the Americas.

Human activities have been changing the global biogeographic patterns by the introductions of invasive species. For reptiles, the invasion rate increase of non-native species is remarkably related to the pet trade, especially for freshwater turtles. Here we estimated the invasive potential of the South American turtle Trachemys dorbigni in the Americas using a combination of climatic and human activity variables. We built species distribution models based on data from the native and invasive ranges, using the ensemble model from five different algorithms (GAM, MAXENT, BRT, RF and GBM). We compared the two models' performance and predictions, one calibrated with only climatic variables (climate-driven), and the second also included a descriptive variable of human activity (climate plus human-driven). Suitable areas for T. dorbigni covered occurrence areas of its congeners and highly diversified ecoregions, such as the eastern USA, the islands of Central America, and the south eastern and eastern Brazilian coast. Our results indicate that human activities allow T. dorbigni to establish populations outside of its original climatic niche. Including human activity variables proved fundamental to refining the results to identify more susceptible areas to invasion and to allow the efficient targeting of prevention measures. Finally, we suggested a set of actions to prevent T. dorbigni becoming a highly impacting species in the areas identified as more prone to its invasion.

Anthropogenic substrate-borne vibrations impact anuran calling.

Anthropogenic disturbance is a major cause of the biodiversity crisis. Nevertheless, the role of anthropogenic substrate vibrations in disrupting animal behavior is poorly understood. Amphibians comprise the terrestrial vertebrates most sensitive to vibrations, and since communication is crucial to their survival and reproduction, they are a suitable model for investigating this timely subject. Playback tests were used to assess the effects of substrate vibrations produced by two sources of anthropogenic activity- road traffic and wind turbines- on the calling activity of a naïve population of terrestrial toads. In their natural habitat, a buried tactile sound transducer was used to emit simulated traffic and wind turbine vibrations, and changes in the toads' acoustic responses were analyzed by measuring parameters important for reproductive success: call rate, call duration and dominant frequency. Our results showed a significant call rate reduction by males of Alytes obstetricans in response to both seismic sources, whereas other parameters remained stable. Since females of several species prefer males with higher call rates, our results suggest that anthropogenically derived substrate-borne vibrations could reduce individual reproductive success. Our study demonstrates a clear negative effect of anthropogenic vibrations on anuran communication, and the urgent need for further investigation in this area.

Correction: Effects of traffic noise on the calling behavior of two Neotropical hylid frogs.

[This corrects the article DOI: 10.1371/journal.pone.0183342.].

Effects of traffic noise on the calling behavior of two Neotropical hylid frogs.

Anthropogenic disturbance has been pointed to as one of the major causes of the world´s biodiversity crisis. Among them, noise pollution is a potential underestimated threat, projected to increase in the next decades accompanying urban expansion. Rising levels of noise pollution may result in negative impacts on species highly dependent on acoustic communication. Amphibians have long served as model organisms for investigating animal acoustic communication because their reproduction depends on transmitting and receiving acoustic signals. A few studies have investigated the effects of anthropogenic noise on anurans, but there is still limited knowledge on how it affects them. In this study, we test the effect of two intensities of traffic noise on calling males of two Neotropical treefrogs species. We expect to record more changes in call parameters, to avoid masking effect, at higher intensity noise treatments, and in the species with higher call/noise frequency overlap. We performed a set of field playback experiments exposing male frogs to road noise at two different intensities (65dB and 75dB). Focal species are Boana bischoffi (high call/noise frequency overlap) and B. leptolineata (low call/noise frequency overlap). Both species changed acoustic parameters during or after the exposure to traffic noise. Advertisement call rate of B. bischoffi decreased during road noise, and dominant frequency decreased over time. Call length of B. leptolineata increased or decreased, depending on the order of noise intensity. We also observed spatial displacement in both species, which moved away from the noise source. Our results provide evidence that traffic noise affects anuran calling behavior, and noise intensity is an important factor affecting how species respond.

Invasive American bullfrogs and African Clawed Frogs in South America: High Suitability of Occurrence in Biodiversity Hotspots.

Fabiana G. Barbosa, Camila Both, and Miguel B. Araújo (2017) Invasion of protected areas by non-native species is currently one of the main threats to global biodiversity. Using an ensemble of bioclimatic envelope models we quantify the degree of exposure of South American protected areas to invasion by two invasive amphibian species. We focus on protected areas that coincide with global biodiversity hotspots. The species modeled, Lithobates catesbeianus and Xenopus laevis, have been reported to threaten local faunas in several non-native areas that they invaded, including areas in Asia, Europe, North America, and South America. We show that 87.5% of the protected areas within the Atlantic Forest may be most at risk of invasion by L. catesbeianus and X. laevis under current climate conditions, followed by areas in the Cerrado (51.7), Tropical Andes (37.6%), Tumbes-Choco-Magdalena (22.5%), and Chilean Winter Rainfall and Valdivian Forests (20.5%). Conservation plans for these regions should, therefore, consider latent threats from multiple sources including invasion by highly competitive non-native species such as the ones modeled in our study.

Reproductive phenology of the American Bullfrog in subtropical Brazil: photoperiod as a main determinant of seasonal activity.

The North American bullfrog Lithobates catesbeianus continues to invade ecosystems worldwide, potentially causing population declines and even extinctions. Within its native distribution, bullfrogs show prolonged reproductive seasons and high fertility. However, data on breeding biology of bullfrogs ex-situ in invaded localities mainly comes from anecdotal reports. Understanding how invasive species are adjusting their life histories to new colonized environments is important for conservation purposes. Here we describe temporal and spatial abundance, calling activity, spawning and tadpole distribution of bullfrogs in southern Brazil. Eighteen samplings occurred during one year. The abundance of individuals was positively related to longer photoperiods and higher temperatures. Reproductive activity was also positively associated with longer photoperiods. Calling sites, spawning and tadpoles were associated with microhabitats presenting hydrophytes, which may provide shelter and thermal stability to bullfrogs. The reproductive seasonal activity of bullfrogs can be highly variable across its growing geographical range, but in subtropical Brazil it is associated with photoperiod, a highly predictable abiotic determinant. In our study area, bullfrogs presented a breeding season twice as long as that observed in some native localities. We suggest that management strategies directed to bullfrog populations must consider the habitat structures and seasonal regimes determined by each invaded environment.

Can Protected Areas with Agricultural Edges Avoid Invasions? The Case of Bullfrogs in the Southern Atlantic Rainforest in Brazil.

Bruno Madalozzo, Camila Both, and Sonia Cechin (2016) The American bullfrog, Lithobates catesbeianus, is one of the 100 most harmful invasive species of the planet. Climatic and topographic models predict that the Atlantic Forest regions of southern Brazil are favorable for the establishment of invasive bullfrog populations. The predicted increase of temperature and concentration of gases associated with the greenhouse effect will augment the vulnerability of protected areas of the Atlantic forest to bullfrog invasions in the coming years. In this study we investigated to what extent protected areas of the Atlantic Forest surrounded by anthropogenic landscapes are vulnerable to bullfrog invasions. We conducted surveys in 36 waterbodies located either in a protected area or in anthropogenically modified adjacent locations on a forest-edge-agriculture gradient. We collected data on abundance and breeding to identify the main descriptors (local and landscape variables) that explain the distribution of bullfrogs along this gradient. The variance partitioning analysis showed a strongest association of bullfrog abundance with local waterbody descriptors (area-depth-hydroperiod) and secondarily with a forest-edge-agriculture gradient, i.e., the landscape. The observed distribution pattern suggests that protected areas are likely to be invaded by bullfrogs. Therefore, management strategies should focus on both scales: landscape and waterbody. Supervising the construction of large (permanent or deep) waterbodies in edge habitats of the park and adjacent areas can be effective and agriculture and forest management could importantly complement the prevention of invasions.

The Interplay between Environmental Filtering and Spatial Processes in Structuring Communities: The Case of Neotropical Snake Communities.

Both habitat filters and spatial processes can influence community structure. Space alone affects species immigration from the regional species pool, whereas habitat filters affect species distribution and inter-specific interactions. This study aimed to understand how the interplay between environmental and geographical processes influenced the structure of Neotropical snake communities in different habitat types. We selected six studies that sampled snakes in forests, four conducted in savannas and two in grasslands (the latter two are grouped in a non-forest category). We used the net relatedness and nearest taxon indices to assess phylogenetic structure within forest and non-forest areas. We also used the phylogenetic fuzzy-weighting algorithm to characterize phylogenetic structure across communities and the relation of phylogenetic composition patterns to habitat type, structure, and latitude. Finally, we tested for morphological trait convergence and phylogenetic niche conservatism using four forest and four non-forest areas for which morphological data were available. Community phylogenetic composition changed across forest and non-forest areas suggesting that environmental filtering influences community structure. Species traits were affected by habitat type, indicating convergence at the metacommunity level. Tail length, robustness, and number of ventral scales maximized community convergence among forest and non-forest areas. The observed patterns suggested environmental filtering, indicating that less vertically structured habitats represent a strong filter. Despite the fact that phylogenetic structure was not detected individually for each community, we observed a trend towards communities composed by more closely related species in higher latitudes and more overdispersed compositions in lower latitudes. Such pattern suggests that the limited distribution of major snake lineages constrained species distributions. Structure indices for each community were also related to habitat type, showing that communities from non-forest areas tend to be more clustered. Our study showed that both environmental filtering and spatial gradients play important roles in shaping the composition of Neotropical snake communities.

Quantifying anuran microhabitat use to infer the potential for parasite transmission between invasive cane toads and two species of Australian native frogs.

Parasites that are carried by invasive species can infect native taxa, with devastating consequences. In Australia, invading cane toads (Rhinella marina) carry lungworm parasites (Rhabdias pseudosphaerocephala) that (based on previous laboratory studies) can infect native treefrogs (Litoria caerulea and L. splendida). To assess the potential of parasite transmission from the invader to the native species (and from one infected native frog to another), we used surveys and radiotelemetry to quantify anuran microhabitat use, and proximity to other anurans, in two sites in tropical Australia. Unsurprisingly, treefrogs spent much of their time off the ground (especially by day, and in undisturbed forests) but terrestrial activity was common at night (especially in anthropogenically modified habitats). Microhabitat overlap between cane toads and frogs was generally low, except at night in disturbed areas, whereas overlap between the two frog species was high. The situations of highest overlap, and hence with the greatest danger of parasite transmission, involve aggregations of frogs within crevices by day, and use of open ground by all three anuran species at night. Overall, microhabitat divergence between toads and frogs should reduce, but not eliminate, the transmission of lungworms from invasive toads to vulnerable native frogs.

Land use explains the distribution of threatened New World amphibians better than climate.

BACKGROUND: We evaluated the direct and indirect influence of climate, land use, phylogenetic structure, species richness and endemism on the distribution of New World threatened amphibians. METHODOLOGY/PRINCIPAL FINDINGS: We used the WWF's New World ecoregions, the WWFs amphibian distributional data and the IUCN Red List Categories to obtain the number of threatened species per ecoregion. We analyzed three different scenarios urgent, moderate, and the most inclusive scenario. Using path analysis we evaluated the direct and indirect effects of climate, type of land use, phylogenetic structure, richness and endemism on the number of threatened amphibians in New World ecoregions. In all scenarios we found strong support for direct influences of endemism, the cover of villages and species richness on the number of threatened species in each ecoregion. The proportion of wild area had indirect effects in the moderate and the most inclusive scenario. Phylogenetic composition was important in determining the species richness and endemism in each ecoregion. Climate variables had complex and indirect effects on the number of threatened species. CONCLUSION/SIGNIFICANCE: Land use has a more direct influence than climate in determining the distribution of New World threatened amphibians. Independently of the scenario analyzed, the main variables influencing the distribution of threatened amphibians were consistent, with endemism having the largest magnitude path coefficient. The importance of phylogenetic composition could indicate that some clades may be more threatened than others, and their presence increases the number of threatened species. Our results highlight the importance of man-made land transformation, which is a local variable, as a critical factor underlying the distribution of threatened amphibians at a biogeographic scale.

Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs.

Invasive species are known to affect native species in a variety of ways, but the effect of acoustic invaders has not been examined previously. We simulated an invasion of the acoustic niche by exposing calling native male white-banded tree frogs (Hypsiboas albomarginatus) to recorded invasive American bullfrog (Lithobates catesbeianus) calls. In response, tree frogs immediately shifted calls to significantly higher frequencies. In the post-stimulus period, they continued to use higher frequencies while also decreasing signal duration. Acoustic signals are the primary basis of mate selection in many anurans, suggesting that such changes could negatively affect the reproductive success of native species. The effects of bullfrog vocalizations on acoustic communities are expected to be especially severe due to their broad frequency band, which masks the calls of multiple species simultaneously.