Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus

Abstract

Transmission is central to pathogen fitness and strongly influences the impact of pathogens on host populations. Particularly important to transmission dynamics is the distinction between direct transmission requiring close physical contact (e.g. bumping, fighting, or coughing) and indirect transmission from environmental sources such as contaminated substrates. We present data from 4 experiments addressing the form, routes, and timing of transmission of Ambystoma tigrinum virus (ATV) among tiger salamanders Ambystoma tigrinum nebulosum. Our data suggest that ATV is efficiently transmitted by direct interactions between live animals (bumping, biting and cannibalism) as well as by necrophagy and indirectly via water and fomites. Determining which form of transmission is most important in nature is essential for understanding transmission at the population level. Our experiments also revealed an important temporal aspect of infectiousness: larval salamanders become infectious soon after exposure to ATV and their propensity to infect others increases with time. These results begin to clarify the mechanisms and dynamics of ATV transmission and lead to key questions that need to be addressed in future research.

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

“…Two studies found that wood frog and Italian agile frog ( Rana latastei ) tadpoles had greater mortality rates when allowed to scavenge dead FV3-infected conspecifi cs (Pearman et al 2004 ;Harp and Petranka 2006 ). Similarly, Brunner et al ( 2007 ) found that ATV-infected tiger salamander larvae were most infectious near or after death when they could be easily consumed.…”

“…The skin may not be a common site of infection in metamorphosed amphibians because they secrete antimicrobial peptides on their skin, which can inactivate several types of pathogens, including FV3 and ATV (Chinchar et al , 2004Sheafor et al 2008 ; Rollins-Smith 2009 ). Brunner et al ( 2007 ), however, demonstrated that a 1 s skinto-skin contact out of water was suffi cient for transmission of ATV from infected, symptomatic tiger salamander larvae to uninfected larvae, so entry through the epithelium is possible at least during the larval stage.…”

“…Ranaviruses can be transmitted by contact with infected individuals, through the water or on fomites (e.g., pond substrates), and by consuming part or all of infected animals (Langdon et al 1988 ;Reddacliff and Whittington 1996 ;Jancovich et al 1997 ;Plumb and Zilberg 1999b ;Woodland et al 2002b ;Pearman et al 2004 ;Harp and Petranka 2006 ;Brunner et al 2007 ;Cunningham et al 2007a ;Robert et al 2011 ;Brenes et al 2014a ). Viral mRNA is detectable in the intestines of larval and adult African clawed frogs ( Xenopus laevis ) as early as 3 h after exposure to virus in water and then spreads to other tissues, suggesting that the intestines are a primary point of entry of waterborne virus in amphibians (Robert et al 2011 ).…”

“…Only when there are many dead animals (and perhaps the scavengers are sated) does the event become obvious. Moreover, an accumulation of infectious carcasses may facilitate transmission (Pearman et al 2004 ;Harp and Petranka 2006 ;Brunner et al 2007 ), increasing the speed of the epidemic. There is some support of this hypothesis in amphibians.…”

Ecophysiology meets conservation: understanding the role of disease in amphibian population declines

“…wood frogs (Rana sylvatica) breed in temporary ponds while American bullfrogs (Rana catesbeiana) breed in permanent ponds). Although contaminated water and sediment are effective media for virus transmission within natural ponds, the virus is inactivated following pond drying [71]. Thus, species that breed in temporary ponds that dry each year may be exposed to ranaviruses less frequently, because viability of the virus among seasons outside the host is unlikely [72].…”