Co-infection by alveolate parasites and frog virus 3-like ranavirus during an amphibian larval mortality event in Florida, USA

Abstract

A multispecies amphibian larval mortality event, primarily affecting American bullfrogs Lithobates catesbeianus, was investigated during April 2011 at the Mike Roess Gold Head Branch State Park, Clay County, Florida, USA. Freshly dead and moribund tadpoles had hemorrhagic lesions around the vent and on the ventral body surface, with some exhibiting a swollen abdomen. Bullfrogs (100%), southern leopard frogs L. sphenocephalus (33.3%), and gopher frogs L. capito (100%) were infected by alveolate parasites. The intensity of infection in bullfrog livers was high. Tadpoles were evaluated for frog virus 3 (FV3) by histology and PCR. For those southern leopard frog tadpoles (n = 2) whose livers had not been obscured by alveolate spore infection, neither a pathologic response nor intracytoplasmic inclusions typically associated with clinical infections of FV3-like ranavirus were noted. Sequencing of a portion (496 bp) of the viral major capsid protein gene confirmed FV3-like virus in bullfrogs (n = 1, plus n = 6 pooled) and southern leopard frogs (n = 1, plus n = 4 pooled). In July 2011, young-of-the-year bullfrog tadpoles (n = 7) were negative for alveolate parasites, but 1 gopher frog tadpole was positive. To our knowledge, this is the first confirmed mortality event for amphibians in Florida associated with FV3-like virus, but the extent to which the virus played a primary role is uncertain. Larval mortality was most likely caused by a combination of alveolate parasite infections, FV3-like ranavirus, and undetermined etiological factors.KEY WORDS: Alveolate parasite · Ranavirus · Frog virus 3 · Amphibian mortality · Bullfrog · Southern leopard frog · Gopher frog · Tadpole OPEN PEN ACCESS CCESSDis Aquat Org 105: [89][90][91][92][93][94][95][96][97][98][99] 2013 eases (Ouellet et al. 2005, Robert 2010, Lesbarrères et al. 2012. The risk of pathogen transfer from free-ranging to captive amphibians and vice versa is of particular concern. The World Organization for Animal Health (OIE) recently listed Bd and amphibian ranaviruses as reportable diseases (Schloegel et al. 2010). Iridoviruses of the genus Ranavirus infect poikilothermic vertebrates across 3 taxonomic classes: anuran and caudate amphibians, squamate and testudine reptiles, and bony fishes (Chinchar 2002, Chinchar et al. 2009). Frog virus 3 (FV3), the type species for the genus Ranavirus, is pathogenic to both larval and adult amphibians and has been responsible for frog population declines and dieoffs worldwide (Gray et al. 2009b, Lesbarrères et al. 2012.Another parasite that appears to be of high pathogenic significance but has yet to achieve reportable status is the alveolate protistan parasite responsible for larval amphibian die-offs throughout the USA (Green et al. 2003, Davis et al. 2007, Cook 2008). This parasite, the cause of an emerging disease in amphibians, has not yet been officially named. Herein we refer to the pathogen as an alveolate parasite, but it has been reported as Dermomycoides sp., a Perkinsus-like parasite, and Anuraperkin...

Xenopus-FV3 host-pathogen interactions and immune evasion

“…Consistent with this, tadpoles are usually more susceptible to ranavirus infection (Bayley et al, 2013; Landsberg et al, 2013; Reeve et al, 2013). In X. laevis , tadpoles are typically unable to control FV3 infection and most of them succumb.…”

Prominent Amphibian (Xenopus laevis) Tadpole Type III Interferon Response to the Frog Virus 3 Ranavirus

“…Ranaviruses are large, icosahedral, double-stranded DNA (dsDNA) viruses that manifest in systemic diseases, hemorrhaging, and necrotic cell death within multiple afflicted organs (18). Typically, amphibian tadpoles are more susceptible to, and succumb from, these infections, whereas mature adults are usually more resistant to these pathogens (14,(21)(22)(23)(24). Frog virus 3 (FV3) is the type species of the ranavirus genus, and thus FV3 infection of the amphibian Xenopus laevis presents a pertinent research platform for studying the interface between the ranavirus and the amphibian host immune response.…”

Disease dynamics of red-spotted newts and their anuran prey in a montane pond community

“…The affected larvae were negative for Bd according to PCR. Histologically there was no evidence of infection by Perkinsealike alveolates, which are protistan parasites that have been implicated in mortality of larval ranids at other sites in Georgia (Davis et al 2007) and Florida (Landsberg et al 2013). Histopathological findings were consistent with Rv and all 7 larvae were PCR-positive for Rv (Table 3).…”