Intraspecific Reservoirs: Complex Life History and the Persistence of a Lethal Ranavirus

Abstract

Virulent parasites cannot persist in small host populations unless the parasite also has a reservoir host. We hypothesize that, in hosts with complex life histories, one stage may act as an intraspecific reservoir for another. In amphibians, for example, larvae often occur at high densities, but these densities are ephemeral and fixed in space, whereas metamorphs are long-lived and vagile but may be very sparse. Parasite persistence is unlikely in either stage alone, but transmission between stages could maintain virulent parasites in seasonally fluctuating amphibian populations.We examined this hypothesis with a lethal ranavirus, Ambystoma tigrinum virus (ATV), that causes recurrent epidemics in larval tiger salamander populations, but which has no reservoir host and degrades quickly in the environment. Although exposure to ATV is generally lethal, larvae and metamorphs maintained sublethal, transmissible infections for Ͼ5 mo. Field data corroborate the persistence of ATV between epidemics in sublethally infected metamorphs. Three-quarters of dispersing metamorphs during one epidemic were infected, and apparently healthy metamorphs returning to breed harbored ATV infections. Our results suggest that larval epidemics amplify virus prevalence and sublethally infected metamorphs (re)introduce the virus into uninfected larval populations. Intraspecific reservoirs may explain the persistence of parasites in and declines of small, isolated amphibian populations.

Frog Virus 3-Like Infections in Aquatic Amphibian Communities

“…Since we have found extensive infection of ambystomatid salamanders with FV3 or an FV3-like virus in our pond communities, it is possible that virus movement between ponds is mediated by salamanders or other amphibians living in these pond communities. It has been suggested that, for Ambystoma tigrinum virus (ATV), a ranavirus related to FV3, infected Arizona tiger salamander adults can act as intraspecies reservoirs for ATV (Brunner et al, 2004). However, this does not explain the geographical heterogeneity of ranavirus infections in a continuous landscape.…”

“…It has been hypothesized that salamanders, which are chronically and sublethally infected with a ranavirus, can reintroduce the virus into their breeding pond upon their return the next breeding season and can therefore infect the next generation of larvae (Brunner et al, 2004). Brunner et al (2004) provided evidence of infection in returning salamanders (two of 30), but they provided no mechanism for the transfer of the virus between these adults and larvae.…”

“…Although the mechanism of FV3/FV3-like virus transmission remains unclear, both vertical (reproduction-dependent) and horizontal (nonreproduction-dependent) transmission may be possible. A horizontal transmission model has been proposed for another member of the Ranavirus genus, Ambystoma tigrinum virus (ATV), which can be passed to larval and recently metamorphosed Arizona tiger salamanders (Ambystoma tigrinum nebulosum) by exposure to free virus in water (Brunner et al, 2004). In addition, salamanders that were exposed to ATV as larvae could become ATV carriers as adults and pass the virus on to uninfected adults (Brunner et al, 2004).…”

“…A horizontal transmission model has been proposed for another member of the Ranavirus genus, Ambystoma tigrinum virus (ATV), which can be passed to larval and recently metamorphosed Arizona tiger salamanders (Ambystoma tigrinum nebulosum) by exposure to free virus in water (Brunner et al, 2004). In addition, salamanders that were exposed to ATV as larvae could become ATV carriers as adults and pass the virus on to uninfected adults (Brunner et al, 2004). A recent and similar study examined potential transmission mechanisms of ranaviruses between wood frogs inhabiting geographically isolated ponds (Harp and Petranka, 2006).…”

Antimicrobial Peptide Defenses in the Salamander, Ambystoma Tigrinum, Against Emerging Amphibian Pathogens

“…Our results closely agree with observations of diseases of A. tigrinum in the field. This species does not generally die of B. dendrobatidis even when heavily infected (Davidson et al, 2003b), but is readily killed by low concentrations of ATV (Jancovich et al, 1997;Brunner et al, 2004Brunner et al, , 2005.…”