Development and Disease: How Susceptibility to an Emerging Pathogen Changes through Anuran Development

Abstract

Ranaviruses have caused die-offs of amphibians across the globe. In North America, these pathogens cause more amphibian mortality events than any other pathogen. Field observations suggest that ranavirus epizootics in amphibian communities are common during metamorphosis, presumably due to changes in immune function. However, few controlled studies have compared the relative susceptibility of amphibians to ranaviruses across life stages. Our objectives were to measure differences in mortality and infection prevalence following exposure to ranavirus at four developmental stages and determine whether the differences were consistent among seven anuran species. Based on previous studies, we hypothesized that susceptibility to ranavirus would be greatest at metamorphosis. Our results did not support this hypothesis, as four of the species were most susceptible to ranavirus during the larval or hatchling stages. The embryo stage had the lowest susceptibility among species probably due to the protective membranous layers of the egg. Our results indicate that generalizations should be made cautiously about patterns of susceptibility to ranaviruses among amphibian developmental stages and species. Further, if early developmental stages of amphibians are susceptible to ranaviruses, the impact of ranavirus epizootic events may be greater than realized due to the greater difficulty of detecting morbid hatchlings and larvae compared to metamorphs.

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

“…If all stages were equally susceptible, mortality in wood frog populations would occur in spring, which was not observed. Haislip et al ( 2011 ) also found that susceptibility to ranavirus differed among amphibian developmental stages, but metamorphosis was not always the most susceptible stage. Thus, the occurrence of metamorphosis is not a universal explanation for timing of ranavirus outbreaks in amphibian communities.…”

“…There are a growing number of experimental studies investigating the relative susceptibility of amphibian species to ranavirus infection and disease (Cullen et al 1995 ;Cullen and Owens 2002 ;Schock et al 2008 ;Hoverman et al 2010Hoverman et al , 2011Haislip et al 2011 ). Until the recent studies by Brenes et al ( 2014a , b ), comparative studies involving reptiles were generally lacking, and those involving fi sh are largely restricted to EHNV (Becker et al 2013 ;Langdon 1989 ; but see Brenes et al 2014b ).…”

“…Four were susceptible, one (the eastern mosquitofi sh, G. holbrooki ) was a potential carrier, and seven either did not become infected or recovered from infection (Becker et al 2013 ). Similarly, the outcome of exposure to an FV3-like ranavirus varied dramatically among 14 anurans and fi ve caudates from North America, from complete mortality to no infections detected at the end of the experiment (Hoverman et al 2010Haislip et al 2011 ). Challenges with three FV3-like ranaviruses isolated from a chelonian, fi sh, and anuran resulted in infection in only two of fi ve fi sh species (including the western mosquitofi sh) and two of three highly aquatic turtles (Florida softshell turtle, Apalone ferox , and Mississippi map turtle, Graptemys pseudogeographica kohni ; Brenes et al 2014b ).…”

“…Alternatively, individuals of certain species or life history stages that are carriers (i.e., remain infected and infectious for long periods without clearing or succumbing to the infection) may act as reservoirs for more susceptible species or stages (Haydon et al 2002 ). In general, only a small fraction of individuals survive for weeks or months with inapparent infections (Langdon 1989 ;Cullen and Owens 2002 ;Brunner et al 2004 ;Robert et al 2007 ;Haislip et al 2011 ;Hoverman et al 2011 ;Brenes 2013 ;Brenes et al 2014b ). For example, of the 43 ectothermic vertebrate species challenged with FV3-like ranaviruses by Hoverman et al ( 2011), Brenes ( 2013), and Brenes et al ( 2014b, there was about an 85 % correlation between infection and mortality after 28 days.…”

Comparative Pathology of Ranaviruses and Diagnostic Techniques

“…Moreover, Earl and Gray ( 2014 ) demonstrated that ranavirus-associated mortality of larvae or metamorphs was suffi cient to cause population declines in highly susceptible species. Researchers have demonstrated a strong correlation between infection prevalence and mortality in laboratory experiments with Frog Virus 3 (FV3)-like ranaviruses (see Haislip et al 2011 ;Hoverman et al 2011 ;Brenes et al 2014a ); thus, high infection prevalence during fi eld surveillance may be an indicator of an impending die-off .…”