Biodiversity hotspots, representing regions with high species endemism and conservation threat, have been mapped globally. Yet, biodiversity distribution data from within hotspots are too sparse for ...effective conservation in the face of rapid environmental change. Using frogs as indicators, ecological niche models under paleoclimates, and simultaneous Bayesian analyses of multispecies molecular data, we compare alternative hypotheses of assemblage-scale response to late Quaternary climate change. This reveals a hotspot within the Brazilian Atlantic forest hotspot. We show that the southern Atlantic forest was climatically unstable relative to the central region, which served as a large climatic refugium for neotropical species in the late Pleistocene. This sets new priorities for conservation in Brazil and establishes a validated approach to biodiversity prediction in other understudied, species-rich regions.
Vocalizations of anuran amphibians have received much attention in studies of behavioral ecology and physiology, but also provide informative characters for identifying and delimiting species. We ...here review the terminology and variation of frog calls from a perspective of integrative taxonomy, and provide hands-on protocols for recording, analyzing, comparing, interpreting and describing these sounds. Our focus is on advertisement calls, which serve as premating isolation mechanisms and, therefore, convey important taxonomic information. We provide recommendations for terminology of frog vocalizations, with call, note and pulse being the fundamental subunits to be used in descriptions and comparisons. However, due to the complexity and diversity of these signals, an unequivocal application of the terms call and note can be challenging. We therefore provide two coherent concepts that either follow a note-centered approach (defining uninterrupted units of sound as notes, and their entirety as call) or a call-centered approach (defining uninterrupted units as call whenever they are separated by long silent intervals) in terminology. Based on surveys of literature, we show that numerous call traits can be highly variable within and between individuals of one species. Despite idiosyncrasies of species and higher taxa, the duration of calls or notes, pulse rate within notes, and number of pulses per note appear to be more static within individuals and somewhat less affected by temperature. Therefore, these variables might often be preferable as taxonomic characters over call rate or note rate, which are heavily influenced by various factors. Dominant frequency is also comparatively static and only weakly affected by temperature, but depends strongly on body size. As with other taxonomic characters, strong call divergence is typically indicative of species-level differences, whereas call similarities of two populations are no evidence for them being conspecific. Taxonomic conclusions can especially be drawn when the general advertisement call structure of two candidate species is radically different and qualitative call differences are thus observed. On the other hand, quantitative differences in call traits might substantially vary within and among conspecific populations, and require careful evaluation and analysis. We provide guidelines for the taxonomic interpretation of advertisement call differences in sympatric and allopatric situations, and emphasize the need for an integrative use of multiple datasets (bio-acoustics, morphology, genetics), particularly for allopatric scenarios. We show that small-sized frogs often emit calls with frequency components in the ultrasound spectrum, although it is unlikely that these high frequencies are of biological relevance for the majority of them, and we illustrate that detection of upper harmonics depends also on recording distance because higher frequencies are attenuated more strongly. Bioacoustics remains a prime approach in integrative taxonomy of anurans if uncertainty due to possible intraspecific variation and technical artifacts is adequately considered and acknowledged.
Intraspecific communication in frogs plays an important role in the recognition of conspecifics in general and of potential rivals or mates in particular and therefore with relevant consequences for ...pre-zygotic reproductive isolation. We investigate intraspecific communication in Hylodes japi, an endemic Brazilian torrent frog with territorial males and an elaborate courtship behavior. We describe its repertoire of acoustic signals as well as one of the most complex repertoires of visual displays known in anurans, including five new visual displays. Previously unknown in frogs, we also describe a bimodal inter-sexual communication system where the female stimulates the male to emit a courtship call. As another novelty for frogs, we show that in addition to choosing which limb to signal with, males choose which of their two vocal sacs will be used for visual signaling. We explain how and why this is accomplished. Control of inflation also provides additional evidence that vocal sac movement and color must be important for visual communication, even while producing sound. Through the current knowledge on visual signaling in Neotropical torrent frogs (i.e. hylodids), we discuss and highlight the behavioral diversity in the family Hylodidae. Our findings indicate that communication in species of Hylodes is undoubtedly more sophisticated than we expected and that visual communication in anurans is more widespread than previously thought. This is especially true in tropical regions, most likely due to the higher number of species and phylogenetic groups and/or to ecological factors, such as higher microhabitat diversity.
Introduced species have the potential to become invasive and jeopardize entire ecosystems. The success of species establishing viable populations outside their original extent depends primarily on ...favorable climatic conditions in the invasive ranges. Species distribution modeling (SDM) can thus be used to estimate potential habitat suitability for populations of invasive species. Here we review the status of six amphibian species with invasive populations in Brazil (four domestic species and two imported species). We (i) modeled the current habitat suitability and future potential distribution of these six focal species, (ii) reported on the disease status of Eleutherodactylus johnstonei and Phyllodytes luteolus, and (iii) quantified the acoustic overlap of P. luteolus and Leptodactylus labyrinthicus with three co-occurring native species. Our models indicated that all six invasive species could potentially expand their ranges in Brazil within the next few decades. In addition, our SDMs predicted important expansions in available habitat for 2 out of 6 invasive species under future (2100) climatic conditions. We detected high acoustic niche overlap between invasive and native amphibian species, underscoring that acoustic interference might reduce mating success in local frogs. Despite the American bullfrog Lithobates catesbeianus being recognized as a potential reservoir for the frog-killing fungus Batrachochytrium dendrobatidis (Bd) in Brazil, we did not detect Bd in the recently introduced population of E. johnstonei and P. luteolus in the State of São Paulo. We emphasize that the number of invasive amphibian species in Brazil is increasing exponentially, highlighting the urgent need to monitor and control these populations and decrease potential impacts on the locally biodiverse wildlife.
Taxonomists always have had intense discussions about how species should be delimited and recently many studies have used integrative approaches by combining molecular, morphological, and bioacoustic ...data. Although these studies are paramount for understanding species diversity, few of them actually formalize species delimitations to the final step of nomenclatural acts. Historically, the Neotropical frog genus Adenomera has been considered as a difficult taxonomic group because it comprises many morphologically similar species exhibiting high levels of intraspecific polymorphism. A recent work using molecular data shed light on the phylogenetic relationships within the genus and identified several lineages that may correspond to undescribed species but did not delimit species boundaries. In the Atlantic Forest, a clade formed by A. marmorata and two putative species (Adenomera sp. J and Adenomera sp. K) were identified. In this paper, we combine morphological, acoustic, and molecular data in order to evaluate species limits within this Atlantic Forest Adenomera clade. We provide a redescription of A. marmorata and restrict its type locality to the Tijuca Massif, in the Municipality of Rio de Janeiro, Brazil. Our results do not support A. marmorata and the two candidate species as diagnosable distinct species. Therefore A. marmorata corresponds to a species with pronounced morphological and acoustic variation in the genus and a complex phylogeographic structure.
The genus Scinax currently includes more than 120 species, recovered in two major clades, the S. catharinae and the S. ruber clades. The latter comprises 75 species, most of which remain unassigned ...to any species groups, while 12 are included in the S. rostratus and S. uruguayus groups. In this paper we present a taxonomic review of the two species currently included in the S. uruguayus group, discussing some putative phenotypic synapomorphies of this group. Although S. pinima and S. uruguayus have been considered as distinct species, this has been based on scant evidence, and several authors doubted of their distinctiveness. Our study of available specimens of S. pinima and S. uruguayus corroborates that both are valid and diagnosable species based on phenotypic evidence. Furthermore, our results show that S. pinima previously known only from its type locality, has a much widespread distribution than previously thought (including the Brazilian states of Paraná, Santa Catarina, and Rio Grande do Sul), which, added to the biological information presented here allows to suggest the removal of this species from the "Data Deficient" IUCN Red List category to "Least Concern". Also, we describe a new species formerly reported as S. aff. pinima and S. uruguayus from NE Argentina and some localities from the Brazilian State of Rio Grande do Sul. All species are diagnosed and characterized using adult and larval morphology, osteology, vocalizations, cytogenetics, and natural history.
Frogs are immediately associated to their conspicuous vocalizations emitted during the breeding season. Therefore, many scientists were inspired to study their acoustic communication. Nowadays, many ...types of calls are described and we felt the need of reviewing the terminology currently and historically applied. As a result, we proposed the classification of anuran vocalization into three major categories: reproductive, aggressive, and defensive calls. These categories are subdivided according to the social context of emission mostly reflecting also acoustic differences among call types. Some call types are here proposed to be synonymies of the mostly used and inclusive terms. We also suggest terminologies for basic bioacoustical analyses, mostly applied in call descriptions. Furthermore, we present cases of complex calls, including call gradation. Finally, based on novel data (such as an unusual case of juvenile vocalizations), we discuss situations in which it is difficult to classify call types, reflecting the need of experimental studies.
Anurans are a highly diverse group in the Atlantic Forest hotspot (AF), yet distribution patterns and species richness gradients are not randomly distributed throughout the biome. Thus, we explore ...how anuran species are distributed in this complex and biodiverse hotspot, and hypothesize that this group can be distinguished by different cohesive regions. We used range maps of 497 species to obtain a presence/absence data grid, resolved to 50×50 km grain size, which was submitted to k-means clustering with v-fold cross-validation to determine the biogeographic regions. We also explored the extent to which current environmental variables, topography, and floristic structure of the AF are expected to identify the cluster patterns recognized by the k-means clustering. The biogeographic patterns found for amphibians are broadly congruent with ecoregions identified in the AF, but their edges, and sometimes the whole extent of some clusters, present much less resolved pattern compared to previous classification. We also identified that climate, topography, and vegetation structure of the AF explained a high percentage of variance of the cluster patterns identified, but the magnitude of the regression coefficients shifted regarding their importance in explaining the variance for each cluster. Specifically, we propose that the anuran fauna of the AF can be split into four biogeographic regions: a) less diverse and widely-ranged species that predominantly occur in the inland semideciduous forests; b) northern small-ranged species that presumably evolved within the Pleistocene forest refugia; c) highly diverse and small-ranged species from the southeastern Brazilian mountain chain and its adjacent semideciduous forest; and d) southern species from the Araucaria forest. Finally, the high congruence among the cluster patterns and previous eco-regions identified for the AF suggests that preserving the underlying habitat structure helps to preserve the historical and ecological signals that underlie the geographic distribution of AF anurans.
Ecologists studying emerging wildlife diseases need to confront the realism of imperfect pathogen detection across heterogeneous habitats to aid in conservation decisions. For example, spatial risk ...assessments of amphibian disease caused by Batrachochytrium dendrobatidis (Bd) has largely ignored imperfect pathogen detection across sampling sites. Because changes in pathogenicity and host susceptibility could trigger recurrent population declines, it is imperative to understand how pathogen prevalence and occupancy vary across environmental gradients. Here, we assessed how Bd occurrence, prevalence, and infection intensity in a diverse Neotropical landscape vary across streams in relation to abiotic and biotic predictors using a hierarchical Bayesian model that accounts for imperfect Bd detection caused by qPCR error. Our model indicated that the number of streams harboring Bd-infected frogs is higher than observed, with Bd likely being present at ~ 43% more streams than it was detected. We found that terrestrial-breeders captured along streams had higher Bd prevalence, but lower infection intensity, than aquatic-breeding species. We found a positive relationship between Bd occupancy probability and stream density, and a negative relationship between Bd occupancy probability and amphibian local richness. Forest cover was a weak predictor of Bd occurrence and infection intensity. Finally, we provide estimates for the minimum number of amphibian captures needed to determine the presence of Bd at a given site where Bd occurs, thus, providing guidence for costeffective disease risk monitoring programs.
Many tropical organisms show large genetic differences among populations, yet the prevalent drivers of the underlying divergence processes are incompletely understood. We explored the effect of ...several habitat and natural history features (body size, macrohabitat, microhabitat, reproduction site, climatic heterogeneity, and topography) on population genetic divergence in tropical amphibians, based on a data set of 2680 DNA sequences of the mitochondrial cytochrome b gene in 39 widely distributed frog species from Brazil, Central America, Cuba, and Madagascar. Generalized linear models were implemented in an information-theoretic framework to evaluate the effects of the six predictors on genetic divergence among populations, measured as spatially corrected pairwise distances. Results indicate that topographic complexity and macrohabitat preferences have a strong effect on population divergence with species specialized to forest habitat and/or from topographically complex regions showing higher phylogeographic structure. This relationship changed after accounting for phylogenetic relatedness among taxa rendering macrohabitat preferences as the most important feature shaping genetic divergence. The remaining predictors showed negligible effects on the observed genetic divergence. A similar analysis performed using the population-scaled mutation rate (Θ) as response variable showed little effect of the predictors. Our results demonstrate greater evolutionary independence among populations of anurans from forested regions versus species from open habitats. This pattern may result from lower vagility and stringency in reproductive requirements of rainforest species. Conversely, open landscapes may offer ephemeral and unstable breeding sites suitable for vagile generalist species, resulting in reduced intraspecific divergence. Our results predict that, for a given period of time, there should be a higher chance of speciation in tropical anurans living in forests than in species adapted to open habitats.
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