Out of Bound: A New Threatened Harlequin Toad (Bufonidae, Atelopus) from the Outer Borders of the Guiana Shield in Central Amazonia Described through Integrative Taxonomy

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Abstract

We used integrative taxonomy to describe a new species of Atelopus from the lowlands of Central Amazonia in the region of Manaus, Amazonas, Brazil. The new species is geographically isolated from the southernmost species of Atelopus of the Guiana Shield. Atelopus manauensis species nova (sp. nov.) is characterized by the combination of the following characteristics: male snout-vent length range (SVL = 19.1–26.4 mm; n = 11); dorsal and lateral skin smooth; ventral surface entirely white or white with cream-colored gular region; fingers and toes lacking subarticular tubercles and fringes. The advertisement call of the new species has a call duration of 689–840 ms, contains 15–26 pulses, is emitted at an average pulse rate of 25.5 pulses per second, and has a dominant frequency ranging 3088–3610 Hz. The genetic divergence between the new species and its morphologically most similar congeners (A. spumarius and A. pulcher) is greater than 4%. Atelopus manauensis sp. nov. is closely related to species of the A. hoogmoedi complex inhabiting the Guiana Shield. The new species has a small geographic distribution (approximately 4500 km2) in a landscape that is strongly threatened by the growth of Manaus, the largest city in Brazilian Amazonia. The new species is considered critically endangered and in need of urgent conservation measures.

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The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice.

JÖRN KÖHLER, MARTIN JANSEN, ARIEL RODRÍGUEZ … (2017)

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.

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Underestimation of Species Richness in Neotropical Frogs Revealed by mtDNA Analyses

Antoine Fouquet, André Gilles, Miguel Vences … (2007)

Background Amphibians are rapidly vanishing. At the same time, it is most likely that the number of amphibian species is highly underestimated. Recent DNA barcoding work has attempted to define a threshold between intra- and inter-specific genetic distances to help identify candidate species. In groups with high extinction rates and poorly known species boundaries, like amphibians, such tools may provide a way to rapidly evaluate species richness. Methodology Here we analyse published and new 16S rDNA sequences from 60 frog species of Amazonia-Guianas to obtain a minimum estimate of the number of undescribed species in this region. We combined isolation by distance, phylogenetic analyses, and comparison of molecular distances to evaluate threshold values for the identification of candidate species among these frogs. Principal Findings In most cases, geographically distant populations belong to genetically highly distinct lineages that could be considered as candidate new species. This was not universal among the taxa studied and thus widespread species of Neotropical frogs really do exist, contrary to previous assumptions. Moreover, the many instances of paraphyly and the wide overlap between distributions of inter- and intra-specific distances reinforce the hypothesis that many cryptic species remain to be described. In our data set, pairwise genetic distances below 0.02 are strongly correlated with geographical distances. This correlation remains statistically significant until genetic distance is 0.05, with no such relation thereafter. This suggests that for higher distances allopatric and sympatric cryptic species prevail. Based on our analyses, we propose a more inclusive pairwise genetic distance of 0.03 between taxa to target lineages that could correspond to candidate species. Conclusions Using this approach, we identify 129 candidate species, two-fold greater than the 60 species included in the current study. This leads to estimates of around 170 to 460 frog taxa unrecognized in Amazonia-Guianas. Significance As a consequence the global amphibian decline detected especially in the Neotropics may be worse than realised.