Family Centrolenidae Research Articles

SORNE CONSIDERATIONS ON THE EX-SITU MANAGEMENT AND CARE OF GLASSFROG EGG MASSES AND TADPOLES (ANURA: CENTROLENIDAE)

A methodology is presented for the captive management of anuran larvae of the family Centrolenidae under controlled conditions. The importance to make and enhance this process as a useful tool to describe and compare centrolenid larvae is discussed.

A third species of glassfrog in the genus Chimerella (Anura, Centrolenidae) from central Peru, discovered by an integrative taxonomic approach

We studied the taxonomic status of glassfrogs collected in Departamento Huánuco, central Peru, which in the field were tentatively allocated to Chimerella, one of the twelve genera currently recognized in the family Centrolenidae. Detailed analyses of their morphology, bioacoustics, and molecular genetics supported their generic allocation and provided evidence for them representing a divergent and unnamed evolutionary lineage within Chimerella. We herein describe this lineage as a new species, being mainly distinguished from the two other known congeners, C. corleone and C. mariaelenae, by details of colouration in life and preservative, substantial differences in advertisement call, and differentiation in mitochondrial markers (12S rRNA, 16S rRNA, cytochrome b) and a nuclear-encoded marker (Rag-1). The new species is the southernmost distributed species in the genus and was found in a swampy habitat at the bank of the Río Patay Rondos, a tributary of the Río Monzon, in rainforest at the Andean-Amazon foothills at 798 m above sea level. Aspects of species delimitation within Chimerella and related future research are briefly addressed and discussed.

A multidisciplinary approach reveals a new species of glassfrog from Colombia (Anura: Centrolenidae: Nymphargus).

Anurans of the family Centrolenidae are a highly diverse clade of Neotropical treefrogs. In the last two decades, glassfrogs have become a model system for studies in ecology and evolutionary biology, in part because their taxonomy and phylogenetic relationships are considered relatively well established. However, there are still many gaps in our knowledge, for example, which morphological characters are important for species delimitation. Consequently, several species complexes in Centrolenidae remain unresolved. Using data on external and internal morphology of adult individuals, tadpoles, advertisement call traits and genetic sequences, we describe a new species of glassfrog (Nymphargus pijao sp. nov.) endemic to Colombia that has been previously missasigned to Nymphargus griffithsi. We include in this description data of three phenotypic characters related to pectoral musculature and testis size, which have been traditionally overlooked in studies about the taxonomy and systematics of glassfrogs. In addition, we present details of a low-cost method implemented in the field to rear tadpoles of the new species. This methodology can solve common problems during the management and care of glassfrogs egg masses and tadpoles, and hence, promotes their description for more species and a better knowledge of the anuran biodiversity in Neotropics.

Description of two Staurois tadpoles from Borneo, Staurois parvus and Staurois tuberilinguis (Anura: Ranidae).

The external morphology of two molecularly identified tadpoles of the genus Staurois, S. parvus and S. tuberilinguis is described. These tadpoles display a typical fossorial morphology characterized by a strongly depressed body, small subcutaneous eyes, a vermiform appearance with a long tail and reduced fins, a nearly pigmentless skin, a KRF of 1:1+1 on the upper labium and numerous keratodont rows on the lower one. The two species can be distinguished by several morphological differences, the most conspicuous are the eye condition (not bulging and covered by skin in S. tuberilinguis) and the presence of numerous white isolated acini on the body and tail in S. parvus. These differences support the specific status of S. parvus relatively to S. tuberilinguis despite low genetic divergence between these two taxa. The morphology of these tadpoles, as well as the buccopharyngeal anatomy of S. parvus, are compared to those of the tadpoles in the family Centrolenidae and the definition of the fossorial ecomorphological guild is updated.

Egg Clutch Survival under Prolonged Paternal Care in a Glass Frog, Hyalinobatrachium talamancae

Previous studies have reported egg attendance as the most common protective behavior among the Neotropical frog family Centrolenidae. However, research on the effect of parental care and other factors thought to affect offspring survival is still missing for a great number of species. Here, we performed field observations during day and night to associate male-only care, habitat characteristics, and environmental variables with egg clutch survival in the understudied glass frog, Hyalinobatrachium talamancae. We conducted 34 nest survival models for 39 egg clutches considering constant daily survival rates, temporal variation in the survival probability, and other biotic and abiotic variables thought to affect the survival of embryos. We found that egg attendance was strongly associated with egg clutch survival in H. talamancae. Our results showed similar degrees of parental investment during day and night, accounting for extensive caring periods over one or multiple clutches as paternal care did not hinder re-mating in this species. Egg clutches exhibited daily survival rates of 0.93±0.02, often reaching pre-hatching stages when attended by males. Our results may thus suggest that egg attendance is a major, if not predominant, determining factor of embryo survival in H. talamancae. This study contributes to the understanding of the natural history associated with paternal care in H. talamancae and provides insight into the evolution of prolonged male-only care in the family Centrolenidae.

First record of <i>Vitreorana ritae</i> (Anura, Centrolenidae) for southern Amazonia inferred from molecular, reproductive and acoustic evidence

Frogs of the family Centrolenidae are adapted to live at high altitudes, and so it is not surprising that their greatest diversity is in the Andes mountain range. Here we extend the known geographic distribution of Vitreorana ritae by more than 550 km towards southern Amazonia. The species was identified by morphological, acoustic and molecular characteristics (mitochondrial marker 16S rRNA). The records reported here are the first for the genus Vitreorana in the state of Mato Grosso, Brazil, as well as for the transition zone between the Amazonia and Cerrado biomes. These records are consistent with the hypothesis that the low number of species of centrolenids reported in the lowlands of the Amazon region may be the result of limited sampling. Even though V. ritae is distributed throughout the Amazon, most of its diagnostic morphological characteristics are conserved. Thus, the great rivers of the Amazon Basin do not seem to act as geographical barriers for this species; however, due to the limited sample size, further acoustic and molecular studies are needed to confirm this hypothesis.

Oviposition site preference and reproductive ecology of Teratohyla midas (Anura: Centrolenidae) in the Colombian Amazon

ABSTRACTThe family Centrolenidae (Glass frogs) includes 157 species of anurans with a Neotropical distribution. Although glass frogs have been the subject of several studies encompassing various aspects of their biology, natural history data on their reproductive ecology is still scarce. One of the important aspects of reproductive ecology is the oviposition site since it can impact the reproductive success of a species. Herein, we provide detailed information on the reproductive ecology of a population of Teratohyla midas from the Colombian Amazon foothills and test whether this species shows a preference on substrate and height of oviposition site. We monitored a population using capture-mark-recapture of individuals identified by a photograph of their unique pattern of dorsal yellow spots. Wild-ID Software was used to corroborate if the dorsal pattern was different between individuals. Additionally, we monitored the presence of egg clutches, amplexus and oviposition behaviour. We observed 110 males and 5 females of T. midas, seen at an average height of 3.1 m ± 2.9 (0–17.8 m) from the ground. Likewise, we recorded the amplexus behaviour of two pairs for approximately 150 min. Once the oviposition happened, the male retreated, and the female covered the egg clutches for approximately 60 min. We observed 25 egg clutches with 60% being deposited in leaves of Selaginella sp and found at an average height of 2.9 ± 1.7 m (1.1–7.0 m). Thus, the selection of oviposition site was not random but mostly specific to one type of substrate. Furthermore, there was an overlap of the re-sampled median height distributions of active individuals and clutches, which suggests that oviposition does not occur at a preferred height within the vertical distribution of individuals. The information presented here is the first detailed record of reproductive ecology for this species and we hope to provide a basis to improve our knowledge on the biology of this species and other glass frogs.

Diversity of glass frogs (Centrolenidae: Anura) in tropical rain forest areas in the center of the department of Choco, Colombia

The central area of the department of Choco (Colombia), is composed of a tropical rain forest. Has a large of variety of amphibians that provides an ecosystem service, being the Family Centrolenidae listed as an excellent indicator of the forest condition. The focus of this study was to determine the richness and distribution in the habitats of the family Centrolenidae in two vegetation coverings in a tropical rain forest of the department of Choco, using the Visual Encounter Survey (VES) method with an effort of 240 per hour. There were 53 individuals registered, distributed in five genera and six species, being the Hyalinobatrachium genus the best represented. The most abundant species was Teratohyla spinosa, being the most dominant for the secondary forest and Hyalinobatrachium collymbiphyllum for the primary forest. Espadarana callistomma and Teratohyla spinosa were the most plastic species in terms of habitat since they were recorded in both coverages. The centrolenids registered showed a preference for high (73.5%) and medium (26.4%) perches, in terms of the substrate leaf (83%) and the branch (17%). Regarding the state of conservation, the species are in the category of LC, DD, and NT; however, it is important to conserve their habitats since some centrolenids are tolerant to intervened ecosystems that have good vegetation and bodies of water with a permanent flow for their development.

Size, Endurance, or Parental Care Performance? Male–Male Competition, Female Choice, and Non-Random Mating Pattern in the Glassfrog Centrolene savagei

Previous work has shown that Centrolene savagei is unique among the more than 150 species in the family Centrolenidae in demonstrating large-male mating advantage. However, it is still unknown whether non-random mating in this species is mediated by intrasexual and/or intersexual selection. To disentangle the effect of these selective pressures on mating pattern in this species, we monitored the breeding behavior of individuals in a population located in the department of Quindío, Central Andes of Colombia. We conducted diurnal and nocturnal surveys each weekend between February and July of 2016 in which we documented morphological (i.e., body size) and behavioral (i.e., chorus tenure, parental-care behavior) characteristics of males to determine their relationship with mating success. We corroborated that in this population of C. savagei, larger males obtain a higher number of mates than do smaller males; male body size co-varies positively with chorus tenure and drives this mating pattern. Male body size was not related to higher fertilization efficiency of eggs laid by females, or a higher survival of embryos in clutches cared for by them. In sum, the higher mating success of larger males in the glassfrog C. savagei seems most strongly related to a mechanism of endurance rivalry competition (intrasexual selection) than female choice (intersexual selection) based on egg fertilization efficiency or parental care quality.

The Advertisement Call and Notes on the Reproductive Ecology of the Glassfrog “Centrolene”quindianum(Anura: Centrolenidae)

Abstract. Frogs of the family Centrolenidae have been a good model system in recent studies of evolutionary ecology, biogeography, and systematics; however, the taxonomic status of some species is still uncertain. Knowing aspects about the natural history of such species can offer diagnostic characters useful for species delimitation and hence, baseline data for understanding the biology of the family Centrolenidae. We describe the advertisement call and aspects of the breeding biology of “Centrolene” quindianum, a threatened species endemic to the Andes of Colombia whose taxonomic status and phylogenetic relationships require clarification. Between July–December 2015, we performed weekly fieldtrips to monitor the breeding activity of this species in a population located in department of Quindio, western slope of the Central Andes of Colombia. The advertisement call of “C.” quindianum consist of two types of calls. The most frequently emitted call is composed of two notes with amplitude modulation and a d...

Description of the previously unknown advertisement call and tadpole of the Colombian endemic glassfrog Centrolene savagei (Anura: Centrolenidae).

Glassfrogs (family Centrolenidae) are a charismatic group that currently contains about 149 species biogeographically restricted to the Neotropics (Frost 2013). The advertisement call and tadpole has been described for less than 25% glassfrog species, 32 and 35 species respectively (e.g. Márquez et al. 1996; Ospina-Sarria et al. 2011). Centrolene savagei (Ruiz-Carranza & Lynch 1991; Fig. 1) is a species of relatively small size frogs (mean snout-vent length, SVL, females: 23.6 mm, males: 21.1 mm) occurring in both the Western and Central Andes (Cordillera Occidental and Cordillera Central) of Colombia, between 1400–2410 m a.s.l. (Ruiz-Carranza & Lynch 1991; Rojas-Morales et al. 2011). Although there is some information regarding egg attendance and natural history of C. savagei (Vargas-Salinas et al. 2007), neither the advertisement call or the larval morphology have been described.

Centrolene daidaleum (Ruiz-Carranza & Lynch, 1991) (Anura, Centrolenidae): A glassfrog with primitive and derived combat behavior

Glassfrogs (family Centrolenidae) constitute a diverse Neotropical group of epiphyllous and arboreal anurans (Señaris & Ayarzagüena 2005; Guayasamin et al. 2009). They are commonly encountered on stream-side vegetation and many species may show high densities during their reproductive season, with numerous territorial males calling for mates in relative small areas (Señaris & Ayarzagüena 2005; Kubicki 2007; Delia et al. 2010). Territoriality of males in several glassfrog species occasionally implies combat behaviors. Combat behavior has been poorly documented in glassfrogs, mainly reported from anecdotal observations in just 11 species (McDiarmid & Adler 1974; Duellman & Savitzky 1976; Greer & Wells 1980; Jacobson 1985; Restrepo-Toro 1996; Bolívar et al. 1999; Savage 2002; Guayasamin & Barrio-Amorós 2005; Kubicki 2007; Delia et al. 2010).

Endemic Ecuadorian glassfrog Cochranella mache is Critically Endangered because of habitat loss

Amphibians are one of the most threatened ani- mal groups. In the Family Centrolenidae c. 50% of the spe- cies are declining and threatened with extinction. One of these is the glassfrog Cochranella mache, endemic to seasonal evergreen forests of the West Ecuadorian region and restricted to highly fragmented forest of , 100 km 2 in the Cordillera Mache-Chindul, north-western coastal Ec- uador, at 100-640 m. We surveyed this region to elucidate the distribution and conservation status of C. mache. We located it in three new localities and also found a museum specimen from a further new locality. We recommend that the species should be categorized as Critically Endangered because of the continuous and progressive destruction of its increasingly fragmented habitat. Recent surveys of glassfrog species sympatric with C. mache showed low relative abundances compared to surveys in the 1970s and 1980s. Because of the relationship between forest and local climate we suggest that gradual declines of lowland glassfrog pop- ulations may be caused by local climate changes produced by forest destruction. In situ conservation is required to halt and mitigate these impacts. Further research on the effects of habitat loss, fragmentation, and associated climate changes on Neotropical amphibians is required.

Description of a new species of Teratohyla Taylor (Amphibia: Athesphatanura: Centrolenidae) from north-western Ecuador

We describe a new species of Glassfrog of the family Centrolenidae. This new taxon, Terarohyla sornozai sp. nov., is diagnosed by having a protruding snout in lateral profile, uniform green dorsal colouration in life, concealed prepollex, extensive webbing between the outer fingers, fully webbed toes, and small body size. It inhabits the Non-Seasonal Evergreen Foothill and Lowland forests in the provinces of Esmeraldas, Imbabura, and Pichincha, north-western Ecuador.

The Tadpole of Vitreorana oyampiensis (Anura, Centrolenidae) in Central Amazonia, Brazil

The family Centrolenidae contains about 148 species (Frost 2009), 11 genera and two subfamilies, distributed from southern Mexico to Panama, through the Andes from Venezuela to Bolivia, with species in the Amazon and Orinoco river basins, the Guiana Shield region, and the Atlantic forests of southeastern Brazil and northeastern Argentina (Guayasamin et al. 2009). The subfamily Centroleninae contains nine genera (Centrolene, Chimerella, Cochranella, Espadarana, Nymphargus, Rulyrana, Sachatamia, Teratohyla, and Vitreorana; Guayasamin et al. 2009). In spite of the high diversity in this subfamily, only the larvae of 15 species are well known (Centrolene altitudinale, C. daidaleum, C. geckoideum, C. hesperium, C. venezuelense, Cochranella granulosa, Espadarana andinum, E. prosoblepon, Teratohyla midas, T. pulverata, T. spinosa, Vitreorana castroviejoi, V. eurygnatha, V. helenae, and V. uranoscopa - Starret 1960; Duellman 1978; Heyer 1985; Cadle & McDiarmid 1990; Mijares-Urrutia 1990; Rada de Matinez 1990; Rueda-Almonacid 1994; Hoffmann 2004; Señaris & Ayarzagüena 2005; Rada et al. 2007). Thirteen of them are associated with Amazonian forests or forested slopes of the Andes (Frost 2009). The tadpole of Vitreorana oyampiensis (=Cochranella oyampiensis) has not been formally described; it was mentioned briefly (diagrammatic drawings and larval color notes) in Hero´s tadpole identification key from Central Amazonia (Hero 1990). In this paper we describe the tadpoles of V. oyampiensis and also provide comments on the spawning sites, clutch size, breeding periods and development site of tadpoles.

Phylogenetic relationships of glassfrogs (Centrolenidae) based on mitochondrial and nuclear genes

Glassfrogs (family Centrolenidae) represent an exceptionally diverse group among Neotropical anurans, but their evolutionary relationships never have been assessed from a molecular perspective. Mitochondrial and nuclear markers were used to develop a novel hypothesis of centrolenid phylogeny. Ingroup sampling included 100 terminals, with 78 (53%) of the named species in the family, representing most of the phenotypic diversity described for the group. Thirty-five species representing taxa traditionally associated with glassfrogs were used as outgroups. Gene sampling consisted of complete or partial sequences of three mitochondrial ( 12S, 16S, ND1) and three nuclear markers ( c-myc exon 2, RAG1, POMC) for a total of ∼4362 bp. Phylogenies were estimated using maximum parsimony, maximum likelihood, and Bayesian analyses for individual genes and combined datasets. The separate analysis of mitochondrial and nuclear datasets allowed us to clarify the relationships within glassfrogs; also, we corroborate the sister-group relationship between Allophryne ruthveni and glassfrogs. The new phylogeny differs significantly from all previous morphology-based hypotheses of relationships, and shows that hypotheses based on few traits are likely to misrepresent evolutionary history. Traits previously hypothesized as unambiguous synapomorphies are shown to be homoplastic, and all genera in the current taxonomy ( Centrolene, Cochranella, Hyalinobatrachium, Nymphargus) are found to be poly- or paraphyletic. The new topology implies a South American origin of glassfrogs and reveals allopatric speciation as the most important speciation mechanism. The phylogeny profoundly affects the traditional interpretations of glassfrog taxonomy, character evolution, and biogeography—topics that now require more extensive evaluation in future studies.

Revision of the characters of Centrolenidae (Amphibia: Anura: Athesphatanura), with comments on its taxonomy and the description of new taxa of glassfrogs

Anurans of the family Centrolenidae are a diverse clade of arboreal frogs distributed across tropical America. Knowledge of their taxonomy, systematics, ecology, behavior, morphology, and other evolutionary aspects of their biology is deficient. Relationships among centrolenid species remain largely unresolved, with no satisfactory phylogenetic hypothesis, and none of the current genera has compelling evidence of monophyly. Further, understanding the phylogeny of glassfrogs is constrained by species-level taxonomic problems, including incorrect description of characters, incomplete analyses of intraspecific variation, and lack of appreciation of species diversity. Herein, we define and analyze the 23 characters that are useful, in combination, in diagnosing centrolenid species, and thereby provide a reference for the use of future workers. We propose revised classifications for the parietal and visceral peritoneal pigmentation, liver form and coloration of its associated hepatic peritoneum, nuptial excrescences, and hand ornamentation. We comment on the generic and species-level taxonomy of Centrolenidae, proposing the recognition of a new genus and describing a new species from Ecuador. We treat Hyla ocellifera Boulenger as a synonym of Centrolene prosoblepon (Boettger), Hyalinobatrachium cardiacalyptum McCranie & Wilson as a synonym of Hyalinobatrachium chirripoi (Taylor), and Hyalinobatrachium crybetes McCranie and Wilson as a synonym of Hyalinobatrachium colymbiphyllum (Taylor). We also present an annotated list of the species of glassfrogs from the Republic of Ecuador with some distributional remarks.

An enigmatic new species of Glassfrog (Amphibia: Anura: Centrolenidae) from the Amazonian Andean slopes of Ecuador

We describe a new species of frog of the family Centrolenidae, Cochranella amelie n. sp., from the central Amazonian Andean slopes, collected at the Oglan River, Province of Pastaza, Ecuador. This new species shows a very unusual combination of characters (lavender dorsum in preservative, absence of a humeral spine in adult males, transparent parietal peritoneum, white visceral peritonea, and bulbous liver). The relationships of this new species of Glassfrog are uncertain, and its assignment to Cochranella is preliminary.

Embryonic development and mortality in Hyalinobatrachium pulveratum (Anura: Centrolenidae) of south-western Costa Rica

The population biology and ecology of most members of the neotropical family Centrolenidae, or glass frogs, are unknown. Glass frogs deposit their eggs in a gelatinous mass on vegetation overhanging streams, the eggs hatch, and the tadpoles drop into the water, where they complete development (Savage 2002). This study will contribute to our limited understanding of centrolenid reproductive ecology by quantifying variation in clutch size, embryonic development and embryonic mortality in a population of Hyalinobatrachium pulveratum.

The morphology of dermal chromatophores in the infrared-reflecting glass-frog Centrolenella fleischmanni.

The morphology and organization of chromatophores in the neotropical glass-frog, Centrolenella fleischmanni (family Centrolenidae), were studied with both light and electron microscopes. Four types of pigment cells are described in the dorsal skin. The fine structure of two chromatophores corresponds to the typical amphibian xanthophore and iridophore; one is similar to the unusual melanophore found in phyllomedusine hylids; the fourth cell type is unlike any chromatophore previously described. Pigment granules in the unusual chromatophore are moderately electron-dense and have an irregular shape, suggesting a fluid composition. This pigment appears to be laid down in organelles similar in appearance to pterinosomes. The organization of pigment cells in this species differs from that of other green, leaf-sitting frogs in that there are few discrete groups resembling "dermal chromatophore units." It is suggested that the unusual new pigment cell contributes significantly to the overall green color of C. fleischmanni.