Widespread occurrence of the amphibian chytrid panzootic lineage in Uruguay is constrained by climate.

The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) causes chytridiomycosis, a disease among the main causes of amphibian declines worldwide. However, Bd studies on Neotropical amphibians from temperate areas are scarce. We present a comprehensive survey of Bd in Uruguay, in temperate central eastern South America, carried out between 2006 and 2014. Skin swabs of 535 specimens of 21 native and exotic frogs were tested by PCR. We used individual-level data to examine the relationship between infection, climatic variables, and their effects on body condition and the number of prey items found in stomach contents. Infection was widespread in free-ranging anurans with an overall prevalence of 41.9%, detected in 15 native species, wild American bullfrogs Aquarana catesbeiana, and captive specimens of Ceratophrys ornata and Xenopus laevis. Three haplotypes of the Bd ITS region were identified in native amphibians, all belonging to the global panzootic lineage (BdGPL), of which only one was present in exotic hosts. Despite high infection frequencies in different anurans, we found no evidence of morbidity or mortality attributable to chytridiomycosis, and we observed no discernible impact on body condition or consumed prey. Climatic conditions at the time of our surveys suggested that the chance of infection is associated with monthly mean temperature, mean humidity, and total precipitation. Temperatures below 21°C combined with moderate humidity and pronounced rainfall may increase the likelihood of infection. Multiple haplotypes of BdGPL combined with high frequencies of infection suggest an enzootic pattern in native species, underscoring the need for continued monitoring.

Cytogenetics of four foam-nesting frog species of the Physalaemus gracilis group (Anura, Leptodactylidae).

Intending to increase the knowledge about cytogenetics of Physalaemus and the sparsely studied P. gracilis group, we analyzed the karyotypes of P. carrizorum, P. gracilis, P. lisei, and P. sp. aff. gracilis. We studied chromosome morphology, heterochromatin patterns, Ag-NORs location and mapped the repetitive DNA sequence PcP190. All species showed diploid karyotypes composed of 22 bi-armed chromosomes and similar C- bands and Ag-NOR patterns. C-bands were mainly centromeric and pericentromeric; non-centromeric C-bands were detected on the telomeres of pair 1 in P. lisei, although polymorphic, and interstitially on pair 10 of P. gracilis. This last character is useful to distinguish P. gracilis from its sibling species P. sp. aff. gracilis. The Ag-NOR sites were detected on the long arms of chromosome pair 8 but with a variable position among species. Clusters of PcP190 showed centromeric and pericentromeric positions coincident with conspicuous C-bands, on pairs 2 and 9 in P. gracilis and P. sp. aff. gracilis, pair 3 in P. carrizorum, and pair 7 in P. lisei. These results significantly increase the knowledge about Physalaemus cytogenetics and encourage further studies on the satellite PcP190 in other genera of Leiuperinae to better understand its taxonomic distribution and the evolutionary dynamics.

Aberrant colourations in wild snakes: case study in Neotropical taxa and a review of terminology

The criteria used by previous authors to define colour aberrancies of snakes, particularly albinism, are varied and terms have widely been used ambiguously. The aim of this work was to review genetically based aberrant colour morphs of wild Neotropical snakes and associated terminology. We compiled a total of 115 cases of conspicuous defective expressions of pigmentations in snakes, including melanin (black/brown colour), xanthins (yellow), and erythrins (red), which involved 47 species of Aniliidae, Boidae, Colubridae, Elapidae, Leptotyphlopidae, Typhlopidae, and Viperidae. Most of them were hypopigmented conditions, mainly amelanism, but also anerythrism, axanthism, hypomelanism, leucism, piebaldism, and albinism (total absence of pigments). Hyperpigmented aberrancies were mostly melanism and xanthism, plus a few instances of erythrism. No associations with diurnality and fossorial behaviour were observed, neither for blanched nor hyperpigmented aberrancies. A discussion of the terms most commonly used for wild snakes is provided, with an account of cases of aberrant colourations in other South American reptiles. Finally, we propose a simple classification framework of wild snake colour aberrancies based on predominant dorsal colour and eye pigmentation for the adoption of a standardized terminology, which may be applicable to other squamates and chelonians. We advocate the use of a more accurate terminology in the scientific literature that would avoid the use of confusing terms like “partial albinism”.

Correction: A review of the elusive bicolored iris Snouted Treefrogs (Anura: Hylidae:Scinax uruguayus group).

[This corrects the article DOI: 10.1371/journal.pone.0222131.].

A new frog of the Leptodactylus fuscus species group (Anura: Leptodactylidae), endemic from the South American Gran Chaco.

A new species of Leptodactylus frog (Anura: Leptodactylidae) from the South American Gran Chaco, morphologically similar and previously confused with the widespread Leptodactylus mystacinus, is described through the use of multiple sources of evidence (molecular, external morphology, coloration, osteology, bioacoustics, and behavior). The phylogenetic analysis with partial sequences of mitochondrial rDNA genes (12S and 16S) recovered the new species within the L. fuscus group, being highly divergent (>3% genetic distance in 16S). The new species was recovered as sister taxa of L. mystacinus, from which it is distinguished by tympanum coloration, cephalic index, dorsum and legs coloration, and some osteological differences in nasals and prevomers. This new frog is characterized by a moderate body size (SVL 46.80-66.21 mm), distinctive color pattern (reddish dorsal surfaces of body with noticeable black stripes in the dorsolateral folds), a circular and dark tympanum with dark tympanic annuli, and behavior of males that call on top of fallen logs and tree branches close to the ground.

A review of the elusive bicolored iris Snouted Treefrogs (Anura: Hylidae:Scinax uruguayus group).

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.

Early ontogeny and sequence heterochronies in Leiuperinae frogs (Anura: Leptodactylidae).

The study of early development in Neotropical Leiuperinae frogs (Anura, Leptodactylidae) has been addressed by several works in recent times. However, a comparative developmental approach under a phylogenetic context was not available. Herein we analyzed the morphological and ontogenetic diversity of embryos belonging to 22 species of the three largest genera in Leiuperinae. We find that in most cases, variations fit with the phylogeny at the inter- and intrageneric levels. Embryo kyphosis and whitish color are synapomorphies for the clade grouping Physalaemus and Engystomops. The presence of a third lower tooth row on the oral disc is plesiomorphic for Leiuperinae, only changing in derived clades. The configurations and developmental trajectories of the lower lip are exceptionally diverse. The developmental sequences optimized on the phylogenetic tree recover an early differentiated first lower tooth row a synapomorphy of Pseudopaludicola and Physalaemus, and an early differentiated second row as synapomorphy of Pleurodema. On the other hand, few features are highly conserved in the subfamily, such as the adhesive glands universally present in a type-C configuration. Our results also suggest that the morphology and ontogeny of embryos is in some cases associated to the environment where they develop. A large body size, poorly developed transient respiratory structures, large yolk provision and delayed development of the digestive tract occur convergently in embryos inhabiting cold, oxygenated environments. Embryos that develop in warmer water bodies in xeric environments show more complex and persistent transient respiratory structures and an early onset of hind limbs development. Our survey highlights that morphology and early development of anurans can be a valuable source of information for phylogenetic studies, and provide fundamental bases to explore and discuss how evolutionary changes can be shaped by environmental conditions.

Sensitivity of histology for the detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis.

Histology is often underappreciated for the detection of the amphibian pathogenic fungus Batrachochytrium dendrobatidis, the cause of the potentially lethal skin disease chytridiomycosis. We evaluated the sensitivity of histology to detect chytrids in 20 wild specimens of 2 frog species from Uruguay that were clinically normal, but confirmed by PCR to be infected by B. dendrobatidis. We detected maturing and sporulated sporangia in 15 of 20 (75%) frogs, which is more sensitive than previously reported for histology. The effort needed to identify chytrids in histologic skin sections of Physalaemus henselii and Pleurodema bibroni required examination of 3.2 and 8.7 mm of skin sections for each frog species, respectively.

Amphibian parasites of the Order Dermocystida (Ichthyosporea): current knowledge, taxonomic review and new records from Brazil.

Amphibian parasites of the Order Dermocystida (Ichthyosporea) are widespread pathogens known mainly from Europe and North America, which cause primarily a disease of skin and subcutaneous tissue in their hosts. The taxonomy of these organisms has been problematic given their conserved morphology, similar clinical disease and pathology. Currently recognized taxa belong to the three closely related genera, Amphibiocystidium, Amphibiothecum, and Rhinosporidium, whereas species of Dermocystidium and Sphaerothecum destruens include fish parasites. Here, we review the taxonomy of Dermocystida based on a molecular phylogenetic analysis, principally of amphibian parasites, including DNA sequences obtained from amphibian hosts collected in the central-eastern region of South America. A new taxonomic arrangement is proposed, which includes the designation of type material for Dermocystidium pusula, synonymization of Amphibiothecum with Dermocystidium, and the restriction of Amphibiocystidium to its type species A. ranae. We also review the taxonomic status of Dermosporidium hylarum until the present work included in the synonymy of the human and animal pathogen R. seeberi, and considered herein as a valid taxon, however. In addition, a new species of Sphaerothecum parasitic to amphibians is described, being the first record of this genus in the southern hemisphere and in an amphibian host.

Parasitism by larval tapeworms genus Spirometra in South American amphibians and reptiles: new records from Brazil and Uruguay, and a review of current knowledge in the region.

Spargana are plerocercoid larvae of cestode tapeworms of the genus Spirometra, Family Diphyllobothriidae, parasitic to frogs, reptiles, birds and mammals. This parasitic disease in humans can be transmitted through the use and consumption of amphibians and reptiles. The available knowledge about Spirometra in South America is scarce, and there are only a few reports on the occurrence of sparganum in amphibians and reptiles, many of them published in old papers not easily available to researchers. In this work we present a review on this topic, provide new records in two species of amphibians and 7 species of reptiles from Brazil and Uruguay respectively. We also summarize current knowledge of Spirometra in the continent, along with an updated of host taxonomy. We could gather from the literature a total of 15 studies about amphibian and reptile hosts, published between 1850 and 2016, corresponding to 43 case reports, mostly from Brazil (29) and Uruguay (8), Argentina (3), Peru (2), and Venezuela (1); the majority of them related to reptiles (five lizards and 26 snake species), and 14 corresponded to amphibians (9 anurans). Plerocercoid larvae were located in different organs of the hosts, such as subcutaneous tissue, coelomic cavity, peritoneum, and musculature. The importance of amphibians and reptiles in the transmission of the disease to humans in South America is discussed. Relevant issues to be studied in the near future are the taxonomic characterization of Spirometra in the region and the biological risk of reptile meat for aboriginal and other rural communities.

Ichthyophonus sp. (Ichthyophonae, Ichthyophonida) infection in a South American amphibian, the hylid frog Hypsiboas pulchellus.

We report infection by Ichthyophonus sp. in a South American amphibian, the hylid frog Hypsiboas pulchellus in Uruguay. This frog had a large subcutaneous mass over the urostyle and dorsal musculature comprised of parasitic cysts with mild granulomatous inflammation but otherwise appeared healthy.

Dermocystid-chytrid coinfection in the neotropical frog Hypsiboas pulchellus (Anura: Hylidae).

We present gross and histologic evidence of coinfection in amphibians by fungal-like parasites of the order Dermocystidia (Amphibiocystidium sp.) and the fungus Batrachochytrium dendrobatidis. The condition was observed in frogs Hypsiboas pulchellus (Hylidae) from Uruguay in 2009 to 2012. This report is the first of dermocystids in Neotropical amphibians since 1940.

A lost species or the loss of stripes? The case of Contomastix lizards from Cabo Polonio, Uruguay, with observations on C. lacertoides (Duméril & Bibron) and Cnemidophorus grandensis Cope (Squamata, Teiidae).

The main goal of this manuscript is the reevaluation of the taxonomic status of the teiid lizard Contomastix charrua, known only from Cabo Polonio, a small coastal rocky outcrop in southeastern Uruguay. This species was erected on the basis of the presence of a second pair of ceratobranchials and longer cornua in the hyoid bone, in addition to a reduced expression of the pattern of coloration as compared with C. lacertoides. Nevertheless, we found that both species have indistinguishable hyoid morphology, bearing C. lacertoides a noticeable second pair of ceratobranchials. Besides, we realized that the pattern of coloration in this species is more variable than previously considered. As a result of the present work, C. charrua is included in the synonymy of C. lacertoides. In addition, we provide some observations on the holotype of Cnemidophorus grandensis, a junior synonym of C. lacertoides.

Karyotypic Data on 28 Species of Scinax (Amphibia: Anura Hylidae) Diversity and Informative Variation

The hylid frog genus Scinax is the most species-rich within Hylinae, with more than 100 recognized species grouped in the S. catharinae and S. ruber clades. The karyotypes of 14 species of the S. catharinae clade and 14 of the S. ruber clade were analyzed, several of them for the first time. All studied species presented 2n  =  2x  =  24 biarmed chromosomes (FN  =  48) and no identifiable sex chromosomes. There are two alternate states associated with the size and morphology of pair 1, corresponding to the S. catharinae clade and to the S. ruber clade. The morphology of pairs 2 and 6 also differentiate the species of both major clades. Species of the S. ruber clade in general have Ag-NORs in pair 11, as is commonly observed among hylines with 2n  =  24. The Ag-NORs' position in the long arms of pair 11 is interstitial in S. fuscomarginatus, S. fuscovarius, S. nasicus, S. similis, S. squalirostris, and S. uruguayus, and terminal in S. acuminatus, S. curicica, S. duartei, S. granulatus, S. hayii, and S. perereca. The single exception among species of the S. ruber clade is S. alter, which has terminal Ag-NORs at the long arms of pair 3. Most species of the S. catharinae clade have Ag-NORs in pair 6, representing a putative synapomorphy of this clade, while the Ag-NORs in pair 11 that occur in S. canastrensis are most parsimoniously interpreted as a reversion. C-banding is predominantly centromeric, but in the S. catharinae clade there is a greater amount of heterochromatin than in the S. ruber clade. This study corroborates the occurrence of informative variation, some already considered in a previous cladistic analysis, and reports new characters, outlining the significance of cytogenetic data for the systematics of Scinax.

Chytridiomycosis in frogs from Uruguay.

Amphibian chytridiomycosis caused by Batrachochytrium dendrobatidis is reported in Uruguayan native amphibians for the first time. Histological evidence of infection was observed in tadpoles of Hypsiboas pulchellus, Odontophrynus maisuma, Physalaemus henselii, and Scinax squalirostris. The effects of chytridiomycosis on these species are still unknown. However, the disease is of potential concern for the conservation of the apparently declining species P. henselii and also for O. maisuma, given its restricted distribution in habitats which are being increasingly disturbed.