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Abstract

Glassfrogs (family: Centrolenidae) represent a fantastic radiation (~150 described species) of Neotropical anurans that originated in South America and dispersed into Central America. In this study, we review the systematics of Ecuadorian glassfrogs, providing species accounts of all 60 species, including three new species described herein. For all Ecuadorian species, we provide new information on the evolution, morphology, biology, conservation, and distribution. We present a new molecular phylogeny for Centrolenidae and address cryptic diversity within the family. We employ a candidate species system and designate 24 putative new species that require further study to determine their species status. We find that, in some cases, currently recognized species lack justification; specifically, we place Centrolene gemmata and Centrolene scirtetes under the synonymy of Centrolene lynchi; C. guanacarum and C. bacata under the synonymy of Centrolene sanchezi; Cochranella phryxa under the synonymy of Cochranella resplendens; and Hyalinobatrachium ruedai under the synonymy of Hyalinobatrachium munozorum. We also find that diversification patterns are mostly congruent with allopatric speciation, facilitated by barriers to gene flow (e.g., valleys, mountains, linearity of the Andes), and that niche conservatism is a dominant feature in the family. Conservation threats are diverse, but habitat destruction and climate change are of particular concern. The most imperiled glassfrogs in Ecuador are Centrolene buckleyi, C. charapita, C. geckoidea, C. medemi, C. pipilata, Cochranella mache, Nymphargus balionotus, N. manduriacu, N. megacheirus, and N. sucre, all of which are considered Critically Endangered. Lastly, we identify priority areas for glassfrog conservation in Ecuador.
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... When the advertisement calls of a species has been described from several populations, we separate them by country if applicable. We followed the taxonomic classification proposed by Guayasamin et al. (2020). ...
... Call descriptions in this group have increased since 2005, increasing from 15 to 105 in the last years. This increase in numbers has largely been due to taxonomic revision of glass frogs, for example, Señaris and Ayarzaguena (2005) in Venezuela and more recently Guayasamin et al. (2020) in Ecuador. In both papers, the advertisement calls are described for 12 and 14 species, respectively. ...
... Research in glass frogs has shifted focus from mostly species descriptions to attention on aspects of their natural history and evolutionary ecology, but it is in the most recent two decades that documenting attributes of life history and evolution has been most prevalent (e.g. Catenazzi et al. 2009;Hutter et al. 2013;Ríos-Soto et al. 2017;Rada et al. 2019;Delia et al. 2019Delia et al. , 2020Guayasamin et al. 2020;Navarro-Salcedo et al. 2022). Related to acoustic attributes as a communication strategy, this study may constitutes an important contribution, given the description of the advertisement calls for several species, one of them with a taxonomic status still to be defined. ...
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In anurans, vocalisations are the main behavioural modality of communication. Hence, the description of acoustic signals in anur-ans is important for understanding many aspects of their biology. We describe for the first time the advertisement calls for eight glass frog species (Centrolene antioquiensis, "Centrolene" robledoi, Nymphargus caucanus, N. chami, N. ignotus, N. rosada, N. spilotus, Sachatamia orejuela) and provide additional data on the recently described advertisement calls of Espadarana audax. In addition, we review the current knowledge of advertisement calls for all glass frog species (Centrolenidae). Based on the predominant temporal and the spectral structure, we identified three major types of calls in the family: 1) calls consisting of unpulsed short notes with amplitude modulation, similar to a 'Tic', 2) calls consisting of one long note (whistled) without amplitude modulation, similar to a 'Tii' and 3) calls consisting of pulsed or pulsatile notes, similar to a 'Trii'. We mapped these acoustic characters in the context of the evolutionary history of Centrolenidae. Descriptions presented here offer evidence to recognise most centrolenid calls using measurable characters in the field or laboratory. As such, we hope to stimulate future studies based on bioacoustical analysis in this widespread and highly diverse Neotropical clade.
... The diversity of glassfrogs (Family Centrolenidae) is concentrated in the northern Andes, which hosts more than half (83 taxa) of the species in the family (Guayasamin et al., 2020). The linearity of the Andes, combined with its topographical and climatic complexity, has facilitated numerous diversification events-dominated by allopatric speciation, niche conservatism, and few ecological shifts (Hutter, Guayasamin & Wiens, 2013;Castroviejo-Fisher et al., 2014;Guayasamin et al., 2020). ...
... The diversity of glassfrogs (Family Centrolenidae) is concentrated in the northern Andes, which hosts more than half (83 taxa) of the species in the family (Guayasamin et al., 2020). The linearity of the Andes, combined with its topographical and climatic complexity, has facilitated numerous diversification events-dominated by allopatric speciation, niche conservatism, and few ecological shifts (Hutter, Guayasamin & Wiens, 2013;Castroviejo-Fisher et al., 2014;Guayasamin et al., 2020). As a consequence, glassfrogs tend to occupy narrow distribution ranges in this biogeographic region, often restricted by elevation and river valleys (Guayasamin et al., 2020). ...
... The linearity of the Andes, combined with its topographical and climatic complexity, has facilitated numerous diversification events-dominated by allopatric speciation, niche conservatism, and few ecological shifts (Hutter, Guayasamin & Wiens, 2013;Castroviejo-Fisher et al., 2014;Guayasamin et al., 2020). As a consequence, glassfrogs tend to occupy narrow distribution ranges in this biogeographic region, often restricted by elevation and river valleys (Guayasamin et al., 2020). ...
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Background The Tropical Andes is the world’s most biodiverse hotspot. This region contains >1,000 amphibian species, more than half of which are endemic. Herein we describe two new glassfrog species (Centrolenidae: Hyalinobatrachium ) that we discovered within relatively unexplored and isolated localities of the Ecuadorian Andes. Methods We employed morphological, acoustic, and molecular methods to test the hypothesis that Hyalinobatrachium mashpi sp. nov and H. nouns sp. nov. are species new to science. Following standard methods, we generated mitochondrial sequences (16S) of 37 individuals in the genus Hyalinobatrachium . We inferred the phylogenetic relationships of the two new species in comparison to all other glassfrogs using Maximum Likelihood. In addition to describing the call of H. mashpi sp. nov., we performed a discriminant analysis of principal components (DAPC) with the advertisement call characteristics of several congeners. Results Based on an integrative taxonomy approach, we describe two new species. Morphological traits and the inferred phylogeny unambiguously place the new taxa in the genus Hyalinobatrachium . Both species are distinguished from other glassfrogs mainly by their dorsal coloration ( i.e ., dorsum lime green with small light yellow spots, head usually with interorbital bar) and transparent pericardium ( i.e ., the heart is visible through the ventral skin). The new species exhibit a high morphological similarity ( i.e ., cryptic) and occur within relatively close geographical proximity (closest aerial distance = 18.9 km); however, their uncorrected p distance for the mitochondrial gene 16S is 4.6–4.7%, a value that greatly exceeds the genetic distance between closely related species of centrolenid frogs. The DAPC revealed that the advertisement call of H. mashpi sp. nov. is acoustically distinct. Discussion Our findings are congruent with several previous studies that report a high degree of endemism in the Toisán mountain range, which appears to be isolated from the main Andean cordillera for some amphibian groups. We recommend that both H. mashpi sp. nov. and H. nouns sp. nov. be listed as Endangered, following IUCN criteria. These new species provide another example of cryptic diversity in the Andes—further evidence that the region fosters much more biodiversity than we have the resources to catalog. Threatened by mining and other exploitative industries, these glassfrogs and many other yet-to-be-discovered Andean species highlight the dire need for effective conservation measures—especially in northwestern Ecuador.
... Nymphargus Cisneros-Heredia & McDiarmid, 2007 currently includes 42 described species of glassfrogs (family Centrolenidae), and 21 of them occur in Ecuador (Guayasamin et al., 2020;Frost, 2021). Despite increasing efforts to better understand the diversity, natural history, ecology and distribution of glassfrogs in the tropical Andes, several species of Nymphargus remain known only from their type localities or few collected specimens (e.g., Nymphargus buenaventura (Cisneros-Heredia & Yánez-Muñoz, 2007;Yánez-Muñoz et al., 2014), N. laurae (Cisneros-Heredia & McDiarmid, 2007), N. lindae Guayasamin in Guayasamin et al. (2020), N. manduriacu Guayasamin et al. (2019)). ...
... Nymphargus Cisneros-Heredia & McDiarmid, 2007 currently includes 42 described species of glassfrogs (family Centrolenidae), and 21 of them occur in Ecuador (Guayasamin et al., 2020;Frost, 2021). Despite increasing efforts to better understand the diversity, natural history, ecology and distribution of glassfrogs in the tropical Andes, several species of Nymphargus remain known only from their type localities or few collected specimens (e.g., Nymphargus buenaventura (Cisneros-Heredia & Yánez-Muñoz, 2007;Yánez-Muñoz et al., 2014), N. laurae (Cisneros-Heredia & McDiarmid, 2007), N. lindae Guayasamin in Guayasamin et al. (2020), N. manduriacu Guayasamin et al. (2019)). ...
... Terminology, characters and measurements follow formats and definitions described by Cisneros-Heredia & McDiarmid (2007), Watters et al. (2016) and Guayasamin et al. (2020). Examined frogs were photographed in life, anaesthetised with lidocaine 2%; specimens and tissues were fixed in 96% ethanol and preserved separately in 75% ethanol. ...
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We report the rediscovery of Laura’s Glassfrog, Nymphargus laurae Cisneros-Heredia & McDiarmid, 2007, based on two specimens collected at the Colonso-Chalupas Biological Reserve, province of Napo, Ecuador. The species was described and known from a single male specimen collected in 1955 at Loreto, north-eastern Andean foothills of Ecuador. Limited information was available about the colouration, systematics, ecology, and biogeography of N. laurae . We provide new data on the external morphology, colouration, distribution and comment on its conservation status and extinction risk. We discuss the phylogenetic relationships of N. laurae , which forms a clade together with N. siren and N. humboldti . The importance of research in unexplored areas must be a national priority to document the biodiversity associated, especially in protected areas.
... Unfortunately, all such sites are under strong anthropogenic pressure, including mining concessions and the expansion of agricultural boundaries, among others (Cuesta et al., 2017;Roy et al., 2018;Guayasamin et al., 2019;Ortega et al., 2021). These privileged areas have proven to keep an extremely high cryptic diversity of small vertebrates and contain the last remnant populations of numerous threatened species (Cisneros-Heredia and Yanez-Muñoz, 2010;Reyes-Puig et al., 2010, 2019a, 2019bYánez-Muñoz et al., 2010bGuayasamin et al., 2018Guayasamin et al., , 2019Guayasamin et al., , 2020Sánchez-Nivicela et al., 2018;Barrio-Amorós et al., 2020). ...
... This clade is composed by the new species Noblella sp. nov., Noblella coloma N. worleyae Reyes-Puig, Maynard, Trageser, Vieira, Hamilton, Lynch, Culebras, Kohn, Brito andGuayasamin, 2020. Uncorrected p genetic distances are as follow: N. coloma (QCAZ 40579) and the new species (ZSFQ 050) = 5.1%; N. coloma (QCAZ 40579) and N. worleyae (ZSFQ 550-551) = 8.3%; N. worleyae (ZSFQ 550-551) and the new species (ZSFQ 050) = 1.2%. ...
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We describe a new species of terrestrial-breeding frog of the genus Noblella from the northwestern slopes of the Andes of Ecuador, in the province of Pichincha, Ecuador, and report a new locality for the recently described N. worleyae. We include a detailed description of the osteology of both species and discuss their phylogenetic relationships. The new species is differentiated from other species of Noblella by having discs of fingers rounded, without papillae; distal phalanges only slightly T-shaped; toes slightly expanded and rounded distally, without papillae; dorsum uniform brown with irregular suprainguinal dark brown marks; venter yellowish cream, ventral surfaces of legs and thighs reddish to brownish cream; and dark brown throat. The new locality for N. worleyae is located in Los Cedros Reserve, an area highly threatened by mining. We highlight the importance of protecting endemic species of small vertebrates in northwestern Ecuador.
... Allopatric speciation: when populations of the same species become isolated because of geographical barriers, such as rivers or mountain ranges; note that the resulting sister species occupy the same environment. Modified from Guayasamin et al. (2020). ...
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This Report provides a comprehensive, objective, open, transparent, systematic, and rigorous scientific assessment of the state of the Amazon’s ecosystems, current trends, and their implications for the long-term well-being of the region, as well as opportunities and policy relevant options for conservation and sustainable development.
... The notion that landscape complexity has shaped species richness is pervasive in the literature of Andean taxa diversification (Chazot et al., 2018;Esquerré et al., 2019;Guayasamin et al., 2020;Hazzi et al., 2018;Luebert & Weigend, 2014). Although Andean landscapes can favor lineage divergence via allopatric speciation (i.e., mediated by physical barriers to dispersal), they also favor ecological speciation by inducing selective pressures on lineages distributed along environmental gradients (e.g., climatic gradients; Cadena et al., 2011;Caro et al., 2013). ...
Article
Allopatric speciation has been posed as the main mechanism affecting amphibian diversification. In contrast, the role of alternative mechanisms such as ecological speciation has received less attention, and empirical evidence of this mechanism in shaping species richness gradients remains elusive in the tropics. Highly heterogeneous landscapes can favor both allopatric and ecological speciation either by producing physical barriers to dispersal or by inducing selective pressures on lineages distributed along environmental gradients (e.g., climatic gradients). Based on explicit predictions under the ecological speciation hypothesis, we tested whether the phylogeographic, acoustic, morphological, and climatic features differ across the range of Pristimantis viejas, a frog species distributed along a wide altitudinal gradient in the northern Andes of Colombia. In agreement with our predictions, we found two highly differentiated lineages within P. viejas, showing striking differences in molecular diversity, acoustic, and climatic distribution. Importantly, we found that variation of such characteristics is highly congruent with variation in elevational ranges of these two lineages (P. viejas distributed in the lowlands and a cryptic sister lineage distributed in the highlands), and our evidence suggest that the divergence of these lineages was influenced by temperature-related variables. These results support a temperature-driven speciation process which may influence the amphibian diversity patterns in tropical mountains. Last, we describe and name the new cryptic lineage distributed in the highlands. We highlight that an integrative framework in phylogeographic studies should not only focuses on the identification of hidden lineages and their associated processes but also, when multiple lines of evidence are available, it should conduct to their formal description as species are the units for multiple biodiversity disciplines.
... Muchas de las especies pertenecientes a las familias Bufonidae, Centrolenidae e Hylidae utilizan los riachuelos para su reproducción y generalmente se mantienen limitados a lugares donde éstos se encuentren (Duellman 1978). Las nuevas localidades en donde se reportan estas especies son un indicativo de los vacíos de información en la Cordillera del Toisán; esto aplica para algunas especies de distribución muy limitada, como Centrolene heloderma, Hyloscirtus criptico y Osornophryne occidentalis (véase Duellman 1981; Cisneros-Heredia y Gluesenkamp 2010; Coloma et al. 2012;Arteaga et al. 2013;Guayasamin et al. 2020). ...
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En el presente trabajo, tuvimos como objetivo registrar la diversidad y distribución altitudinal de los anfibios de la cordillera de Toisán, en el noroccidente de Ecuador. Para ello, realizamos cuatro transectos de 400x4 metros (m), desde los 2536 hasta los 2911 metros sobre el nivel del mar (msnm). Nuestro muestreo abarcó los distintos microhábitats donde los anfibios suelen ser comunes (i.e., hojarasca, bromelias, bajo troncos). Las especies registradas fueron colectadas para su revisión en el Museo de la Universidad Tecnológica Indoamérica, Quito, Ecuador. Para estimar la diversidad de la zona y en los distintos puntos altitudinales, utilizamos el índice de Shannon y el algoritmo de vecinos cercanos (K-NN). En total, registramos 14 especies, englobadas en cinco géneros y cuatro familias, siendo el género Pristimantis el de mayor riqueza. El transecto Toisán 1 fue el de mayor diversidad, probablemente debido a que no mostraba pendientes pronunciadas y se encontraba a menor altitud. En conclusión, nuestro estudio indica que varias de las especies estudiadas tienen rangos de distribución altitudinal muy restringidos. Existen también, al menos, cuatro especies de Pristimantis que son potencialmente nuevas. Finalmente, encontramos una especie (Hyloscirtus criptico) considerada como amenazada por la UICN.
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Nymphargus rosada (Ruiz-Carranza y Lynch1997) fue descrita como Cochranella rosada a partir de 23 personas colectadas en el municipio de Samaná, departamento de Caldas entre los 1430-1500 msnm, Colombia (Ruiz-Ca-rranza y Lynch 1997).
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Aquaculture, the farming of fish for human consumption and/or trade, is a growing industry throughout the world. The effects of farming on local ecosystems and wildlife are understudied, particularly in regions where farms are often limited to subsistence practices with little to no government regulation. The influence of Rainbow Trout (Oncorhynchus mykiss) farms on glassfrog community composition was assessed in the Mindo and Alambi regions of Ecuador. Call surveys were conducted during the dominant glassfrog reproductive season (March-May 2017) across 13 sites, six of which were in the immediate proximity of trout farms. Nonmetric multidimensional scaling ordination analyses and multiple response permutation procedures indicate that glassfrog communities differed between trout farm and non-trout farm sites (MRPP; A = 0.11, P = 0.04). Differences in glassfrog community composition were significantly or marginally correlated with percent canopy openness, dissolved oxygen (mg/L), conductivity (µS), and total dissolved solids (mg/L), environmental characteristics altered by the aquaculture practice. As the prevalence of trout farms increases across this region, it is likely that the glassfrog community composition will be altered, potentially resulting in a pattern of decreased species richness. It is also likely that habitat changes associated with trout farming practices including deforestation, water chemistry changes, and predation pressures by escaped trout will influence glassfrog species persistence. Mitigation strategies including improved barriers to decrease trout escape, the incorporation of settling ponds to decrease stream contamination, and the preservation of habitat in areas of high amphibian species richness are warranted.
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We have recorded for the first time the glass frog "Cochranella granulosa" for Ecuador, extending its distribution southward by approximately 950 km. Our finding increases the number of Ecuadorian glass frog species to 62.
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We assess the taxonomic status of Hyalinobatrachium petersi and Cochranella ametarsia based on the examination of type material and recently collected specimens. We conclude that the material assigned to them is morphologically undistinguishable from two previously described species (Cochranella pulverata and Cochranella oyampiensis, respectively) and, therefore, are junior synonyms.
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We describe a new species of Hyalinobatrachium from the Amazonian slopes of the Andes in Peru and Bolivia on the basis of morphological, bioacoustic and genetic characteristics. Hyalinobatrachium carlesvilai sp. nov. can be distinguished from other species of Hyalinobatrachium by the combination of the following characters: (1) truncate snout in dorsal and lateral view; (2) white pericardium; (3) enameled dorsal, tarsal and cloacal folds; (4) hand webbing formula III 2 – – 1 + IV; (5) iris cream; (6) advertisement call consisting of a single, frequency-modulated note with a pulsed section followed by a tonal section. The new species had been previously identified as Hyalinobatrachium munozorum and H. bergeri. The advertisement call of the new species was previously assigned to H. bergeri. Here we describe the previously unknown call of Hyalinobatrachium bergeri. Additionally, we study the taxonomic status of H. lemur and H. pellucidum and place the former as synonym of the later. We extend the distribution of H. pellucidum to Departamento Cusco in southern Peru.
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A new species of Glassfrog is described from the lowlands of northwestern Ecuador. The species is placed in the genus Centrolene and differs from the genera, Cochranella and Hyalinobatrachium, by having humeral spines in males. It differs from congenerics by having a uniformly green dorsal coloration, conspicuous humeral spine, and white iris with clearly defined black reticulations. Detailed cranial and postcranial osteological descriptions are provided, and some of osteological features that seem to be peculiar to centrolenids are discussed. A new suite of traits to characterize Glassfrogs and simplify comparisons among species is proposed.