Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages

Emerging diseases have been increasingly associated with population declines, with co-infections

exhibiting many types of interactions. The chytrid fungus (Batrachochytrium dendrobatidis) and

ranaviruses have extraordinarily broad host ranges, however co-infection dynamics have been largely

overlooked. We investigated the pattern of co-occurrence of these two pathogens in an amphibian

assemblage in Serra da Estrela (Portugal). The detection of chytridiomycosis in Portugal was linked

to population declines of midwife-toads (Alytes obstetricans). The asynchronous and subsequent

emergence of a second pathogen - ranavirus - caused episodes of lethal ranavirosis. Chytrid effects

were limited to high altitudes and a single host, while ranavirus was highly pathogenic across multiple

hosts, life-stages and altitudinal range. This new strain (Portuguese newt and toad ranavirus – member

of the CMTV clade) caused annual mass die-offs, similar in host range and rapidity of declines to other

locations in Iberia affected by CMTV-like ranaviruses. However, ranavirus was not always associated

with disease, mortality and declines, contrasting with previous reports on Iberian CMTV-like ranavirosis.

We found little evidence that pre-existing chytrid emergence was associated with ranavirus and the

emergence of ranavirosis. Despite the lack of cumulative or amplified effects, ranavirus drove declines

of host assemblages and changed host community composition and structure, posing a grave threat to

all amphibian populations.