Ché Weldon

Origin of the Amphibian Chytrid Fungus

Histologic evidence indicates southern Africa as the origin of the amphibian chytrid fungus.

Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage

Batrachochytrium dendrobatidis (Bd) is a globally ubiquitous fungal infection that has emerged to become a primary driver of amphibian biodiversity loss. Despite widespread effort to understand the emergence of this panzootic, the origins of the infection, its patterns of global spread, and principle mode of evolution remain largely unknown. Using comparative population genomics, we discovered three deeply diverged lineages of Bd associated with amphibians. Two of these lineages were found in multiple continents and are associated with known introductions by the amphibian trade. We found that isolates belonging to one clade, the global panzootic lineage (BdGPL) have emerged across at least five continents during the 20th century and are associated with the onset of epizootics in North America, Central America, the Caribbean, Australia, and Europe. The two newly identified divergent lineages, Cape lineage (BdCAPE) and Swiss lineage (BdCH), were found to differ in morphological traits when compared against one another and BdGPL, and we show that BdGPL is hypervirulent. BdGPL uniquely bears the hallmarks of genomic recombination, manifested as extensive intergenomic phylogenetic conflict and patchily distributed heterozygosity. We postulate that contact between previously genetically isolated allopatric populations of Bd may have allowed recombination to occur, resulting in the generation, spread, and invasion of the hypervirulent BdGPL leading to contemporary disease-driven losses in amphibian biodiversity.

Rapid Global Expansion of the Fungal Disease Chytridiomycosis into Declining and Healthy Amphibian Populations

The fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis, is enigmatic because it occurs globally in both declining and apparently healthy (non-declining) amphibian populations. This distribution has fueled debate concerning whether, in sites where it has recently been found, the pathogen was introduced or is endemic. In this study, we addressed the molecular population genetics of a global collection of fungal strains from both declining and healthy amphibian populations using DNA sequence variation from 17 nuclear loci and a large fragment from the mitochondrial genome. We found a low rate of DNA polymorphism, with only two sequence alleles detected at each locus, but a high diversity of diploid genotypes. Half of the loci displayed an excess of heterozygous genotypes, consistent with a primarily clonal mode of reproduction. Despite the absence of obvious sex, genotypic diversity was high (44 unique genotypes out of 59 strains). We provide evidence that the observed genotypic variation can be generated by loss of heterozygosity through mitotic recombination. One strain isolated from a bullfrog possessed as much allelic diversity as the entire global sample, suggesting the current epidemic can be traced back to the outbreak of a single clonal lineage. These data are consistent with the current chytridiomycosis epidemic resulting from a novel pathogen undergoing a rapid and recent range expansion. The widespread occurrence of the same lineage in both healthy and declining populations suggests that the outcome of the disease is contingent on environmental factors and host resistance.

The Challenge of Conserving Amphibian Megadiversity in Madagascar

Highly diverse and so far apparently untouched by emergent diseases, Malagasy frogs nevertheless are threatened by ongoing habitat destruction, making pro-active conservation actions especially important for preserving this unique, pre-decline, amphibian fauna.

Widespread presence of the pathogenic fungus Batrachochytrium dendrobatidis in wild amphibian communities in Madagascar

Amphibian chytridiomycosis, an emerging infectious disease caused by the fungus Batrachochytrium dendrobatidis (Bd), has been a significant driver of amphibian declines. While globally widespread, Bd had not yet been reported from within Madagascar. We document surveys conducted across the country between 2005 and 2014, showing Bds first record in 2010. Subsequently, Bd was detected in multiple areas, with prevalence reaching up to 100%. Detection of Bd appears to be associated with mid to high elevation sites and to have a seasonal pattern, with greater detectability during the dry season. Lineage-based PCR was performed on a subset of samples. While some did not amplify with any lineage probe, when a positive signal was observed, samples were most similar to the Global Panzootic Lineage (BdGPL). These results may suggest that Bd arrived recently, but do not exclude the existence of a previously undetected endemic Bd genotype. Representatives of all native anuran families have tested Bd-positive, and exposure trials confirm infection by Bd is possible. Bds presence could pose significant threats to Madagascars unique “megadiverse” amphibians.

Mitigating amphibian chytridiomycoses in nature

Amphibians across the planet face the threat of population decline and extirpation caused by the disease chytridiomycosis. Despite consensus that the fungal pathogens responsible for the disease are conservation issues, strategies to mitigate their impacts in the natural world are, at best, nascent. Reducing risk associated with the movement of amphibians, non-amphibian vectors and other sources of infection remains the first line of defence and a primary objective when mitigating the threat of disease in wildlife. Amphibian-associated chytridiomycete fungi and chytridiomycosis are already widespread, though, and we therefore focus on discussing options for mitigating the threats once disease emergence has occurred in wild amphibian populations. All strategies have shortcomings that need to be overcome before implementation, including stronger efforts towards understanding and addressing ethical and legal considerations. Even if these issues can be dealt with, all currently available approaches, or those under discussion, are unlikely to yield the desired conservation outcome of disease mitigation. The decision process for establishing mitigation strategies requires integrated thinking that assesses disease mitigation options critically and embeds them within more comprehensive strategies for the conservation of amphibian populations, communities and ecosystems. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

Quantification of the trade in Xenopus laevis from South Africa, with implications for biodiversity conservation

Abstract Harvesting wild amphibians for animal trade and consequent introductions of exotic species are considered threats to biodiversity. For this study, we evaluated the literature and unpublished data on Xenopus laevis exports from the Western Cape, South Africa, since the onset of the trade in the early 1930s. Exports for medical science have changed from the use of both captive‐bred and wild‐caught animals to the export of wild‐caught animals only. More than 10 000 frogs were exported annually during 1998–2004 to 132 facilities situated in 30 countries. Uncontrolled harvesting, feral populations, and the spread of parasites and disease associated with X. laevis trade, highlight the relevance of this trade to the conservation of amphibian biodiversity.

Population structure of the African Clawed Frog (Xenopus laevis) in maize‐growing areas with atrazine application versus non‐maize‐growing areas in South Africa

Abstract The herbicide atrazine has been suggested to cause gonadal deformities in frogs and could possibly impact on reproduction. Since the early 1960s, atrazine has been used in large amounts in maize production areas of South Africa. These areas overlap with populations of the African Clawed Frog (Xenopus laevis) that has a wide distribution in southern Africa and is found in most water‐bodies including those where atrazine residues are detected. The aim of this study was to compare various attributes of individual‐ and population‐level responses of X laevis from maize‐growing and non‐maize‐growing areas. Xenopus laevis were studied in three reference and five maize‐growing sites. Sex ratio, snout‐vent length, body‐mass and age profiles were found to be similar for populations in maize‐growing and non‐maize‐growing areas. Our mark‐recapture data indicated that all sites had robust populations. There were no significant relationships between exposure to atrazine and any of the parameters investigated in populations of X. laevis.

Seasonal pattern of chytridiomycosis in common river frog (Amietia angolensis) tadpoles in the South African Grassland Biome

Environmental parameters such as temperature and rainfall influence the biology of amphibians and are likely to similarly influence the growth and prevalence of associated pathogens. Amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), causes an infectious disease, chytridiomycosis, in amphibians worldwide. Field studies on post-metamorphic anurans from tropical Australia have correlated increased prevalence with cool winter temperatures, but similar studies are lacking from Africa. We monitored the seasonality of amphibian chytrid in the Highveld of South Africa through microscopic examination of common river frog (Amietia angolensis) tadpoles over 12 months. Within the study area Bd was found to be widespread, but largely limited to riverine systems. The seasonal infection pattern was inconsistent with the findings of past studies, which showed that prevalence usually peaks during the cooler months of the year. This study indicates that infection levels increased during spring in the Grassland Biome, when temperatures favoured optimum thermal growth of the fungus and when streams reached minimum flow levels.

Pre–emptive national monitoring plan for detecting the amphibian chytrid fungus in Madagascar

Unit for Environmental Science and Management, North-West University, Private Bag X6001, Potchefstroom 2520, South Africa CIBIO, Centro de Investigacao em Biodiversidade e Recursos Geneticos, Campus Agrario de Vairao, Rua Padre Armando Quintas, 4485-661 Vairao, Portugal Madagascar Fauna Group, BP 442, Morafeno, 501 Toamasina, Madagascar Department of Animal Biology, University of Antananarivo, BP 906, 101 Antananarivo, Madagascar International Training Centre, Durrell Wildlife Conservation Trust, Les Augres Manor, La Profonde Rue, Trinity, Jersey JE3 5BP, UK North of England Zoological Society, Chester Zoo, Upton-by-Chester CH2 1LH, UK Museo Regionale di Scienze Naturali, Via G. Giolitti, 36, 10123 Turin, Italy