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Archive | 2015

Distribution and Host Range of Ranaviruses

Amanda L. J. Duffus; Thomas B. Waltzek; Anke C. Stöhr; Matthew C. Allender; Michael Gotesman; Richard J. Whittington; Paul Hick; Megan K. Hines; Rachel E. Marschang

Ranaviruses are globally distributed pathogens in amphibian, fish, and reptile communities that appear to be emerging. Cases of ranavirus infection or disease have been confirmed in at least 105 amphibian species (18 families), 41 fish species (22 families), and 29 reptile species (12 families). Ranaviruses have been documented on all continents except Antarctica, and are frequently associated with mass die-offs. Host susceptibility differs among species, with some species harboring subclinical infections and likely serving as reservoirs for the virus, and other highly susceptible species amplifying the virus. Currently, there are six recognized species of ranavirus, and all are not equally pathogenic among hosts. Frog virus 3 (FV3) is the type species of the genus Ranavirus, and appears to be the most globally distributed species infecting ectothermic taxonomic across three vertebrate classes. International commerce involving subclinically infected ectothermic vertebrates undoubtedly has contributed to the global distribution and emergence of ranaviruses. Herein, we describe the global distributed species infecting ectothermic vertebrates across three taxonomic classes.


PLOS ONE | 2015

Phylogeny and Differentiation of Reptilian and Amphibian Ranaviruses Detected in Europe

Anke C. Stöhr; Alberto López-Bueno; Silvia Blahak; Maria F. Caeiro; Gonçalo M. Rosa; A.P. Alves de Matos; An Martel; Alí Alejo; Rachel E. Marschang

Ranaviruses in amphibians and fish are considered emerging pathogens and several isolates have been extensively characterized in different studies. Ranaviruses have also been detected in reptiles with increasing frequency, but the role of reptilian hosts is still unclear and only limited sequence data has been provided. In this study, we characterized a number of ranaviruses detected in wild and captive animals in Europe based on sequence data from six genomic regions (major capsid protein (MCP), DNA polymerase (DNApol), ribonucleoside diphosphate reductase alpha and beta subunit-like proteins (RNR-α and -β), viral homolog of the alpha subunit of eukaryotic initiation factor 2, eIF-2α (vIF-2α) genes and microsatellite region). A total of ten different isolates from reptiles (tortoises, lizards, and a snake) and four ranaviruses from amphibians (anurans, urodeles) were included in the study. Furthermore, the complete genome sequences of three reptilian isolates were determined and a new PCR for rapid classification of the different variants of the genomic arrangement was developed. All ranaviruses showed slight variations on the partial nucleotide sequences from the different genomic regions (92.6–100%). Some very similar isolates could be distinguished by the size of the band from the microsatellite region. Three of the lizard isolates had a truncated vIF-2α gene; the other ranaviruses had full-length genes. In the phylogenetic analyses of concatenated sequences from different genes (3223 nt/10287 aa), the reptilian ranaviruses were often more closely related to amphibian ranaviruses than to each other, and most clustered together with previously detected ranaviruses from the same geographic region of origin. Comparative analyses show that among the closely related amphibian-like ranaviruses (ALRVs) described to date, three recently split and independently evolving distinct genetic groups can be distinguished. These findings underline the wide host range of ranaviruses and the emergence of pathogen pollution via animal trade of ectothermic vertebrates.


Veterinary Research | 2013

Ranavirus infections associated with skin lesions in lizards

Anke C. Stöhr; Silvia Blahak; Kim O. Heckers; Jutta Wiechert; Helge Behncke; Karina Mathes; Pascale Günther; Peer Zwart; Inna Ball; Birgit Rüschoff; Rachel E. Marschang

Ranaviral disease in amphibians has been studied intensely during the last decade, as associated mass-mortality events are considered to be a global threat to wild animal populations. Several studies have also included other susceptible ectothermic vertebrates (fish and reptiles), but only very few cases of ranavirus infections in lizards have been previously detected. In this study, we focused on clinically suspicious lizards and tested these animals for the presence of ranaviruses. Virological screening of samples from lizards with increased mortality and skin lesions over a course of four years led to the detection of ranaviral infections in seven different groups. Affected species were: brown anoles (Anolis sagrei), Asian glass lizards (Dopasia gracilis), green anoles (Anolis carolinensis), green iguanas (Iguana iguana), and a central bearded dragon (Pogona vitticeps). Purulent to ulcerative-necrotizing dermatitis and hyperkeratosis were diagnosed in pathological examinations. All animals tested positive for the presence of ranavirus by PCR and a part of the major capsid protein (MCP) gene of each virus was sequenced. Three different ranaviruses were isolated in cell culture. The analyzed portions of the MCP gene from each of the five different viruses detected were distinct from one another and were 98.4-100% identical to the corresponding portion of the frog virus 3 (FV3) genome. This is the first description of ranavirus infections in these five lizard species. The similarity in the pathological lesions observed in these different cases indicates that ranaviral infection may be an important differential diagnosis for skin lesions in lizards.


Journal of Zoo and Wildlife Medicine | 2014

Partial characterization of new adenoviruses found in lizards.

Inna Ball; Helge Behncke; Volker Schmidt; Tibor Papp; Anke C. Stöhr; Rachel E. Marschang

Abstract: In the years 2011–2012, a consensus nested polymerase chain reaction was used for the detection of adenovirus (AdV) infection in reptiles. During this screening, three new AdVs were detected. One of these viruses was detected in three lizards from a group of green striped tree dragons (Japalura splendida). Another was detected in a green anole (Anolis carolinensis). A third virus was detected in a Jacksons chameleon (Chamaeleo jacksonii). Analysis of a portion of the DNA-dependent DNA polymerase genes of each of these viruses revealed that they all were different from one another and from all previously described reptilian AdVs. Phylogenetic analysis of the partial DNA polymerase gene sequence showed that all newly detected viruses clustered within the genus Atadenovirus. This is the first description of AdVs in these lizard species.


Veterinary Record | 2013

Mass-mortality in green striped tree dragons (Japalura splendida) associated with multiple viral infections

Helge Behncke; Anke C. Stöhr; Kim O. Heckers; Inna Ball; Rachel E. Marschang

In spring 2011, high mortality in association with skin lesions, systemic haemorrhages and necrosis occurred in a group of green striped tree dragons (Japalura splendida) which were imported from southwestern China via Florida to Germany. Infections with various endoparasites were diagnosed in coprological examinations. Different antiparasitic and antibiotic treatments over a period of three months did not reduce the mortality rate. The remaining animals were therefore euthanased and submitted for additional testing. Predominant findings in pathological examination were granulomatous and necrotising inflammation of the skin, vacuolar tubulonephrosis of the distal renal tubules, hyperaemia and liver necrosis. Eosinophilic intranuclear and basophilic intracytoplasmic inclusion bodies were detected in the liver. Virological testing (PCR and virus isolation methods) demonstrated the presence of ranavirus, adenovirus and invertebrate iridovirus.


Veterinary Journal | 2013

Long-term study of an infection with ranaviruses in a group of edible frogs (Pelophylax kl. esculentus) and partial characterization of two viruses based on four genomic regions

Anke C. Stöhr; Alexandra Hoffmann; Tibor Papp; Nadia Robert; Nicolas B. M. Pruvost; Heinz-Ulrich Reyer; Rachel E. Marschang

Several edible frogs (Pelophylax kl. esculentus) collected into a single group from various ponds in Europe died suddenly with reddening of the skin (legs, abdomen) and haemorrhages in the gastrointestinal tract. Ranavirus was detected in some of the dead frogs using PCR, and virus was also isolated in cell culture. Over the following 3 years, another two outbreaks occurred with low to high mortality in between asymptomatic periods. In the first 2 years, the same ranavirus was detected repeatedly, but a new ranavirus was isolated in association with the second mass-mortality event. The two different ranaviruses were characterized based on nucleotide sequences from four genomic regions, namely, major capsid protein, DNA polymerase, ribonucleoside diphosphate reductase alpha and beta subunit genes. The sequences showed slight variations to each other or GenBank entries and both clustered to the Rana esculenta virus (REV-like) clade in the phylogenetic analysis. Furthermore, a quiescent infection was demonstrated in two individuals. By comparing samples taken before and after transport and caging in groups it was possible to identify the pond of origin and a ranavirus was detected for the first time in wild amphibians in Germany.


Diseases of Aquatic Organisms | 2013

Ranavirus infection in a group of wild-caught Lake Urmia newts Neurergus crocatus imported from Iraq into Germany.

Anke C. Stöhr; Jürgen Fleck; Frank Mutschmann; Rachel E. Marschang

High mortality, in association with anorexia and skin ulcerations, occurred in a group of wild-caught Lake Urmia newts Neurergus crocatus, imported from Iraq in 2011. Predominant findings in the pathological examinations consisted of systemic hemorrhages and ulcerative dermatitis. Ranavirus DNA was detected via PCR in 2 of 3 dead animals, and a part of the major capsid protein (MCP) gene was sequenced. The analyzed portion of the MCP gene was 99% identical to the corresponding portion of the frog virus 3 genome. This is the first description of a ranavirus in Lake Urmia newts and in wild-caught amphibians from Iraq, as well as the first description of ranavirus infection in a urodele from the Middle East.


Journal of herpetological medicine and surgery | 2010

Detection of a tortoise herpesvirus type 1 in a Hermann's tortoise (Testudo hermanni boettgeri) in Germany.

Anke C. Stöhr; Rachel E. Marschang

ABSTRACT A Hermanns tortoise (Testudo hermanni boettgeri) from Germany was presented for medical examination showing signs of upper respiratory tract disease and hyperuricemia. The tortoise was kept with a Russian tortoise (Testudo horsfieldii) for 1 month before presentation. After 1 month of treatment, the respiratory symptoms disappeared. Herpesvirus (HV) was detected from an oral swab by polymerase chain reaction (PCR). The use of different PCRs and sequencing a portion of the DNA polymerase gene demonstrated that the virus was identical to other HV isolates from Russian tortoises (tortoise herpesvirus 1, ToHV1) but distinct from HV isolates from other tortoises, including previously described HVs from Hermanns tortoises (ToHV3). This is the first description of the detection of a ToHV1 in a Hermanns tortoise.


Scientific Reports | 2017

Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages

Gonçalo M. Rosa; Joana Sabino-Pinto; Telma G. Laurentino; An Martel; Frank Pasmans; Rui Rebelo; Richard A. Griffiths; Anke C. Stöhr; Rachel E. Marschang; Stephen J. Price; Trenton W. J. Garner; Jaime Bosch

Emerging diseases have been increasingly associated with population declines, with co-infections exhibiting many types of interactions. The chytrid fungus (Batrachochytrium dendrobatidis) and ranaviruses have extraordinarily broad host ranges, however co-infection dynamics have been largely overlooked. We investigated the pattern of co-occurrence of these two pathogens in an amphibian assemblage in Serra da Estrela (Portugal). The detection of chytridiomycosis in Portugal was linked to population declines of midwife-toads (Alytes obstetricans). The asynchronous and subsequent emergence of a second pathogen - ranavirus - caused episodes of lethal ranavirosis. Chytrid effects were limited to high altitudes and a single host, while ranavirus was highly pathogenic across multiple hosts, life-stages and altitudinal range. This new strain (Portuguese newt and toad ranavirus – member of the CMTV clade) caused annual mass die-offs, similar in host range and rapidity of declines to other locations in Iberia affected by CMTV-like ranaviruses. However, ranavirus was not always associated with disease, mortality and declines, contrasting with previous reports on Iberian CMTV-like ranavirosis. We found little evidence that pre-existing chytrid emergence was associated with ranavirus and the emergence of ranavirosis. Despite the lack of cumulative or amplified effects, ranavirus drove declines of host assemblages and changed host community composition and structure, posing a grave threat to all amphibian populations.


Journal of herpetological medicine and surgery | 2016

Repeated Detection of an Invertebrate Iridovirus in Amphibians

Anke C. Stöhr; Tibor Papp; Rachel E. Marschang

Abstract Invertebrate iridoviruses (IIVs) (family: Iridoviridae) are known pathogens for invertebrates, causing high mortality and reduced fertility in affected insects. Over the past two decades, IIVs have also been increasingly found in lizards in association with nonspecific clinical signs. It has been hypothesized that IIVs from insects can also infect reptiles. From 2010–11, IIVs were repeatedly detected via polymerase chain reaction testing and virus isolation methods in routine diagnostic samples from different amphibians: three blue poison dart frogs (Dendrobates tinctorius azureus), four edible frogs (Pelophylax kl. esculentus), a giant ditch frog (Leptodactylus fallax), an Amazon milk frog (Trachycephalus resinifictrix), mixed organs from agile frogs (Rana dalmatina), a black-spined toad (Bufo melanostictus), and one Lake Urmia newt (Neurergus crocatus). IIVs were found in skin swabs from apparently healthy animals, as well as in multiple organs of frogs that died of unknown causes. Prey insects (crickets) from one owner also tested positive for the presence of IIV. The obtained partial sequences from the major capsid protein (MCP) gene (222nt) from each of these were 100% identical to each other and 98% identical to IIV-6, the type species of the genus Iridovirus. Although the pathogenicity of IIV in amphibians remains unclear, these findings provide further evidence that IIVs may be able to infect vertebrates under some conditions and underline the importance of the genus Iridovirus in vertebrates.

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Inna Ball

University of Hohenheim

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Tibor Papp

Hungarian Academy of Sciences

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Joana Sabino-Pinto

Braunschweig University of Technology

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