Geographic body size variation in ectotherms: effects of seasonality on an anuran from the southern temperate forest

Indexación: Web of Science; Scopus.Background: Body size variation has played a central role in biogeographical research, however, most studies have aimed to describe trends rather than search for underlying mechanisms. In order to provide a more comprehensive understanding of the causes of intra-specific body size variation in ectotherms, we evaluated eight hypotheses proposed in the literature to account for geographical body size variation using the Darwin's frog (Rhinoderma darwinii), an anuran species widely distributed in the temperate forests of South America. Each of the evaluated hypotheses predicted a specific relationship between body size and environmental variables. The level of support for each of these hypotheses was assessed using an information-theoretic approach and based on data from 1015 adult frogs obtained from 14 sites across the entire distributional range of the species. Results: There was strong evidence favouring a single model comprising temperature seasonality as the predictor variable. Larger body sizes were found in areas of greater seasonality, giving support to the "starvation resistance" hypothesis. Considering the known role of temperature on ectothermic metabolism, however, we formulated a new, non-exclusive hypothesis, termed "hibernation hypothesis": greater seasonality is expected to drive larger body size, since metabolic rate is reduced further and longer during colder, longer winters, leading to decreased energy depletion during hibernation, improved survival and increased longevity (and hence growth). Supporting this, a higher post-hibernation body condition in animals from areas of greater seasonality was found. Conclusions: Despite largely recognized effects of temperature on metabolic rate in ectotherms, its importance in determining body size in a gradient of seasonality has been largely overlooked so far. Based on our results, we present and discuss an alternative mechanism, the "hibernation hypothesis", underlying geographical body size variation, which can be helpful to improve our understanding of biogeographical patterns in ectotherms.https://frontiersinzoology.biomedcentral.com/articles/10.1186/s12983-015-0132-

Trophic ecology of the Endangered Darwin's frog inferred by stable isotopes

Indexación: Scopus.Acknowledgements. We thank Dr. Mauricio González-Chang for his contribution to invertebrate identification and Sally Wren for the revision of an earlier version of the manuscript. We are also extremely grateful to Tomás Elgueta Alvarez for providing Video S1. B.E.M.B. has a fellowship awarded by Universidad Andres Bello. This research project was approved by the Bioethics Committee at the Universi-dad Andres Bello, Chile (N°13/2015), and by permits N°5666/2013, N°230/2015, and N°212/2016 of the Chilean Agriculture and Livestock Service, and N°026/2013 and N°11/2015 IX of the Chilean National Forestry Corporation. This study was funded by the Dirección General de Investi-gación y Doctorados, Universidad Andres Bello, through grant N°DI-53-11/R and national funds through FONDE CYT N°11140902 and 1181758 (to C.S.A.).Darwin's frogs Rhinoderma spp. are the only known mouth-brooding frogs on Earth. The southern Darwin's frog, R. darwinii, is found in the temperate forests of southern South America, is listed as Endangered and could be the only extant representative of this genus. Based on stomach contents, invertebrate prey availability and stable isotope analysis, we determined for the first time trophic ecological parameters for this species. Our results showed that R. darwinii is a generalist sit-and-wait predator and a secondary consumer, with a trophic position of 2.9. Carbon and nitrogen isotope composition indicated that herbivore invertebrates are their main prey, detected in 68.1% of their assimilated food. The most consumed prey included mosquitoes, flies, crickets, grasshoppers and ants. Detritivore and carnivore invertebrates were also ingested, but in lower proportions. Our results contribute to a better understanding of the feeding habits of this fully terrestrial amphibian and provide the first insight into their role linking low forest trophic positions with intermediate predators. We provide valuable biological information for in situ and ex situ conservation which can be used when developing habitat protection, reintroduction and captive breeding programmes. As revealed here, stable isotope analysis is a valuable tool to study the trophic ecology of highly endangered and cryptic species. © The authors 2018.https://www.int-res.com/abstracts/esr/v36/p269-278

Cryptic disease-induced mortality may cause host extinction in an apparently stable host- parasite system

The decline of wildlife populations due to emerging infectious disease often shows a common pattern: the parasite invades a naive host population, producing epidemic disease and a population decline, sometimes with extirpation. Some susceptible host populations can survive the epidemic phase and persist with endemic parasitic infection. Understanding host–parasite dynamics leading to persistence of the system is imperative to adequately inform conservation practice. Here we combine field data, statistical and mathematical modelling to explore the dynamics of the apparently stable Rhinoderma darwinii–Batrachochytrium dendrobatidis (Bd) system. Our results indicate that Bd-induced population extirpation may occur even in the absence of epidemics and where parasite prevalence is relatively low. These empirical findings are consistent with previous theoretical predictions showing that highly pathogenic parasites are able to regulate host populations even at extremely low prevalence, highlighting that disease threats should be investigated as a cause of population declines even in the absence of an overt increase in mortality

Xenopus laevis and Emerging Amphibian Pathogens in Chile

Amphibians face an extinction crisis with no precedence. Two emerging infectious diseases, ranaviral disease caused by viruses within the genus Ranavirus and chytridiomycosis due to Batrachochytrium dendrobatidis (Bd), have been linked with amphibian mass mortalities and population declines in many regions of the globe. The African clawed frog (Xenopus laevis) has been indicated as a vector for the spread of these pathogens. Since the 1970s, this species has been invasive in central Chile. We collected X. laevis and dead native amphibians in Chile between 2011 and 2013. We conducted post-mortem examinations and molecular tests for Ranavirus and Bd. Eight of 187 individuals (4.3 %) tested positive for Ranavirus: seven X. laevis and a giant Chilean frog (Calyptocephallela gayi). All positive cases were from the original area of X. laevis invasion. Bd was found to be more prevalent (14.4 %) and widespread than Ranavirus, and all X. laevis Bd-positive animals presented low to moderate levels of infection. Sequencing of a partial Ranavirus gene revealed 100 % sequence identity with Frog Virus 3. This is the first report of Ranavirus in Chile, and these preliminary results are consistent with a role for X. laevis as an infection reservoir for both Ranavirus and Bd

Skin-associated lactic acid bacteria from North American bullfrogs as potential control agents of batrachochytrium dendrobatidis

The fungal pathogen Batrachochytrium dendrobatidis (Bd) is the causative agent of chytridiomycosis and has been a key driver in the catastrophic decline of amphibians globally. While many strategies have been proposed to mitigate Bd outbreaks, few have been successful. In recent years, the use of probiotic formulations that protect an amphibian host by killing or inhibiting Bd have shown promise as an effective chytridiomycosis control strategy. The North American bullfrog (Lithobates catesbeianus) is a common carrier of Bd and harbours a diverse skin microbiota that includes lactic acid bacteria (LAB), a microbial group containing species classified as safe and conferring host benefits. We investigated beneficial/probiotic properties: anti-Bd activity, and adhesion and colonisation characteristics (hydrophobicity, biofilm formation and exopolysaccharide-EPS production) in two confirmed LAB (cLAB-Enterococcus gallinarum CRL 1826, Lactococcus garvieae CRL 1828) and 60 presumptive LAB (pLAB) [together named as LABs] isolated from bullfrog skin.We challenged LABs against eight genetically diverse Bd isolates and found that 32% of the LABs inhibited at least one Bd isolate with varying rates of inhibition. Thus, we established a score of sensitivity from highest (BdGPL AVS7) to lowest (BdGPL C2A) for the studied Bd isolates. We further reveal key factors underlying host adhesion and colonisation of LABs. Specifically, 90.3% of LABs exhibited hydrophilic properties that may promote adhesion to the cutaneous mucus, with the remaining isolates (9.7%) being hydrophobic in nature with a surface polarity compatible with colonisation of acidic, basic or both substrate types. We also found that 59.7% of LABs showed EPS synthesis and 66.1% produced biofilm at different levels: 21% weak, 29% moderate, and 16.1% strong. Together all these properties enhance colonisation of the host surface (mucus or epithelial cells) and may confer protective benefits against Bd through competitive exclusion. Correspondence analysis indicated that biofilm synthesis was LABs specific with high aggregating bacteria correlating with strong biofilm producers, and EPS producers being correlated to negative biofilm producing LABs. We performed Random Amplified Polymorphic DNA (RAPD)-PCR analysis and demonstrated a higher degree of genetic diversity among rod-shaped pLAB than cocci. Based on the LAB genetic analysis and specific probiotic selection criteria that involve beneficial properties, we sequenced 16 pLAB which were identified as Pediococcus pentosaceus, Enterococcus thailandicus, Lactobacillus pentosus/L. plantarum, L. brevis, and L. curvatus. Compatibility assays performed with cLAB and the 16 species described above indicate that all tested LAB can be included in a mixed probiotic formula. Based on our analyses, we suggest that E. gallinarum CRL 1826, L. garvieae CRL 1828, and P. pentosaceus 15 and 18B represent optimal probiotic candidates for Bd control and mitigation. © 2019 Niederle et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited149FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP2016/25358-3This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 063 to SEP), Consejo de Investigaciones de la Universidad Nacional de Tucumán (PIUNT 26/D 414 and 26/D 645 to SEP, and PIUNT 528), Agencia Nacional de Promoción Científica y Tecnológica (PICT 2017-2244 to SEP, PICT 2015-2467 to CEA, and PICT2017-4324 to MENM), Ministerio de Economía y Competitividad de España (CGL2015-70070-R to JB), Fondo Nacional de Desarrollo Científico y Tecnológico (1181758 to CSA and 3180107 to AVS), Fundação de Amparo à Pesquisa do Estado de São Paulo (2016/25358-3 to LFT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscrip

Chytridiomycosis outbreak in a Chilean giant frog (Calyptocephalella gayi) captive breeding program: genomic characterization and pathological findings

Emerging infectious diseases in wildlife are increasingly associated with animal mortality and species declines, but their source and genetic characterization often remains elusive. Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has been associated with catastrophic and well-documented amphibian population declines and extinctions at the global scale. We used histology and whole-genome sequencing to describe the lesions caused by, and the genetic variability of, two Bd isolates obtained from a mass mortality event in a captive population of the threatened Chilean giant frog (Calyptocephalella gayi). This was the first time an association between Bd and high mortality had been detected in this charismatic and declining frog species. Pathological examinations revealed that 30 dead metamorphosed frogs presented agnathia or brachygnathia, a condition that is reported for the first time in association with chytridiomycosis. Phylogenomic analyses revealed that Bd isolates (PA1 and PA2) from captive C. gayi group with other Bd isolates (AVS2, AVS4, and AVS7) forming a single highly supported Chilean Bd clade within the global panzootic lineage of Bd (BdGPL). These findings are important to inform the strengthening of biosecurity measures to prevent the impacts of chytridiomycosis in captive breeding programs elsewhere

Synthesis of Batrachochytrium dendrobatidis infection in South America: amphibian species under risk and areas to focus research and disease mitigation

Amphibian chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd), has been recognized as the infectious disease causing the most catastrophic loss of biodiversity known to science, with South America being the most impacted region. We tested whether Bd prevalence is distributed among host taxonomy, ecoregion, conservation status and habitat preference in South America. Here we provide a synthesis on the extent of Bd infection across South America based on 21 648 molecular diagnostic assays, roles of certain species in the epidemiology of Bd and explore its association with the reported amphibian catastrophic declines in the region. We show that Bd is widespread, with a continental prevalence of 23.2%. Its occurrence in the region shows a phylogenetic signal and the probability of infection is determined by ecoregion, preferred habitat and extinction risk hosts' traits. The taxa exhibiting highest Bd occurrence were mostly aquatic amphibians, including Ranidae, Telmatobiidae, Hylodidae, Calyptocephalellidae and Pipidae. Surprisingly, families exhibiting unusually low Bd prevalence included species in which lethal chytridiomycosis and population declines have been described (genera Atelopus, Rhinoderma and Eleutherodactylus). Higher than expected prevalence of Bd occurred mainly in amphibians living in association with mountain environments in the Andes and Atlantic forests, reflecting highly favourable Bd habitats in these areas. Invasive amphibian species (e.g. Lithobates catesbeianus and Xenopus laevis) exhibited high Bd prevalence; thus we suggest using these as sentinels to understand their potential role as reservoirs, vectors or spreaders of Bd that can be subjected to management. Our results guide on the prioritization of conservation actions to prevent further biodiversity loss due to chytridiomycosis in the world's most amphibian diverse region

Genomic epidemiology of the emerging pathogen Batrachochytrium dendrobatidis from native and invasive amphibian species in Chile

Emerging fungal diseases represent a threat to food security, animal and human health worldwide. Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has been associated with catastrophic and well-documented amphibian population declines and extinctions. For the first time, Bd was cultured from native and non-native wild amphibians in Chile. Phylogenomic analyses revealed that Chilean isolates AVS2, AVS4 and AVS7 group within the global panzootic lineage of Bd (BdGPL) in a single highly supported clade that includes a genotype previously isolated from the United Kingdom. Our results extend the known distribution of BdGPL in South America and suggest a single and relatively recent introduction of BdGPL into the country, providing additional support to the role of anthropogenic activity in the global spread of this panzootic lineage

Response to comment on 'Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity'

Lambert et al. question our retrospective and holistic epidemiological assessment of the role of chytridiomycosis in amphibian declines. Their alternative assessment is narrow and provides an incomplete evaluation of evidence. Adopting this approach limits understanding of infectious disease impacts and hampers conservation efforts. We reaffirm that our study provides unambiguous evidence that chytridiomycosis has affected at least 501 amphibian species

High prevalence of chigger mite infection in a forest-specialist frog with evidence of parasite-related granulomatous myositis

Amphibians are hosts for a wide variety of micro- and macro-parasites. Chigger mites from the Hannemania genus are known to infect a wide variety of amphibian species across the Americas. In Chile, three species (H. pattoni, H. gonzaleacunae and H. ortizi) have been described infecting native anurans; however, neither impacts nor the microscopic lesions associated with these parasites have been described. Here, we document 70% prevalence of chigger mite infection in Eupsophus roseus and absence of infection in Rhinoderma darwinii in the Nahuelbuta Range, Chile. Additionally, we describe the macroscopic and microscopic lesions produced by H. ortizi in one of these species, documenting previously undescribed lesions (granulomatous myositis) within the host’s musculature. These findings highlight that further research to better understand the impacts of chigger mite infection on amphibians is urgently required in Chile and elsewhere