Factors influencing detection and co-detection of Ranavirus and Batrachochytrium dendrobatidis in Midwestern North American anuran populations

Abstract

Amphibian populations are in decline worldwide as they face a barrage of challenges, including infectious diseases caused by ranaviruses and the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). Here we describe seasonal dynamics of Bd and ranavirus detection in free-ranging post-metamorphic wood frogs Lithobates sylvaticus, boreal chorus frogs Pseudacris maculata/triseriata, and gray treefrogs Hyla versicolor/chrysoscelis, sampled over a 3 season gradient in Minnesota (USA) wetlands. We detected Bd in 36% (n = 259) of individuals sampled in 3 wetlands in 2014, and 33% (n = 255) of individuals sampled in 8 wetlands in 2015. We also detected ranavirus in 60% and 18% of individuals sampled in 2014 and 2015, respectively. Ranavirus and Bd were detected concurrently in 26% and 2% of animals sampled in 2014 and 2015, respectively. We report clinical signs and associated infection status of sampled frogs; of the clinical signs observed, skin discoloration was significantly associated with ranavirus infection. Using generalized estimating equations, we found that species, season, wetland, and a species × season interaction term were significant predictors of Bd detection, whereas test year approached significance as a predictor of ranavirus detection. The odds of detecting both pathogens concurrently was significantly influenced by species, season, a species × season interaction term, year, and environmental ammonia. We propose an amphibian health monitoring scheme that couples population size surveys with seasonal molecular surveys of pathogen presence. This information is crucial to monitoring the health of remaining strongholds of healthy amphibian populations, as they face an uncertain future of further anthropogenic change.

Frog Skin Innate Immune Defences: Sensing and Surviving Pathogens

“…Only recently, however, has there been a shift in focus towards understanding whether frog skin derived AMPs are antimicrobial to frog pathogens. Emerging infectious diseases continue to decimate worldwide amphibian populations and, pathogens, such as ranaviruses and Bd , are implicated as proximal causes in frog declines (139). It is critical to gain a further understanding of how to mitigate these diseases in order to conserve dwindling frog populations.…”

Host–multiparasite interactions in amphibians: a review

“…Batrachochytrium dendrobatidis and ranaviruses, the most devastating parasites of amphibians [ 64 , 97 , 149 , 150 ], can co-occur [ 7 , 151 – 153 ] and cause repeated severe mass die-offs [ 154 ]. Although several studies have reported the co-infection of amphibians with Bd and Ranavirus under natural conditions [ 155 – 160 ] and captive populations [ 161 – 164 ], little information exists on within-host interactions between these agents.…”

“…as well [ 164 ]. Finally, elevated physiological stress periods, such as during breeding or when animals pass through sensitive developmental windows, may make amphibians temporally more vulnerable to co-infection [ 160 , 164 ].…”

“…In southern Peru at altitudes between 900 and 2400 m a.s.l., Warne et al [ 164 ] observed a rapid decline in Bd prevalence in adult Pristimantis spp. above 2100 m, while the prevalence of Ranavirus was the lowest below 1200 m, and co-infected adults were only present at elevations ranging between 1200 and 2100 m. Wetland pollution (e.g., ammonia) can be responsible for increased odds of the concurrent occurrence of Bd and Ranavirus , perhaps by overwhelming the immune system of amphibians [ 160 ]. Additionally, in adults of A. terrestris , Love et al [ 61 ] detected higher odds of co-infection with Bd and Ranavirus in metal-contaminated wetlands than reference wetlands.…”

“…Seasonality may also influence the probability of co-infection by affecting the prevalence of both Bd and Ranavirus : the prevalence of Bd is usually the highest during cool and moderately warm months [ 159 , 165 ]; in contrast, Ranavirus peaks were present in the warmest period(s) of the year [ 171 , 172 ]. Talbott and colleagues [ 160 ] found that Bd and Ranavirus co-infection probability was significantly higher during spring than summer or fall. On the other hand, Olori et al [ 159 ] observed large inter-annual variation in prevalence, but they did not detect significant differences across the months of each year.…”