Low resistance to chytridiomycosis in direct-developing amphibians

Abstract

Host-generalist pathogens sporadically infect naive hosts, potentially triggering epizootics. The waterborne fungus Batrachochytrium dendrobatidis (Bd) is linked to declines of hundreds of amphibian species with aquatic larvae. Although several population declines and extinctions attributed to Bd have been reported among cryptic species undergoing direct development away from water, epidemiological studies focused on these terrestrial frogs are lacking. Our field data support that terrestrial direct-developing hosts are less exposed to Bd during their ontogeny than species with aquatic larvae, and thus they might lack adaptive responses against waterborne chytrids. Using controlled laboratory experiments, we exposed wild-caught amphibian species with terrestrial and aquatic life histories to Bd and found that direct developers showed more rapid increases in infection loads and experienced higher mortality rates than species with aquatic larvae. Our findings provide novel information about host responses to generalist pathogens and specifically show that our focal direct developing species have low resistance to Bd infections. Finally, our results underscore that we should not ignore Bd as a potential threat to direct developing species simply because they are less exposed to Bd in nature; instead future amphibian conservation plans should include efforts to safeguard hundreds of direct-developing amphibian species globally.

Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian

“…Our experimental results are compatible with recent fieldbased studies linking Bd emergence, pathogen spillover and population declines of direct-developing amphibian species, such as our focal pumpkin toadlet [17,35]. Epizootics and long-term endemicity of Bd on several continents [17,[36][37][38] allowed significant evolution of host tolerance and resistance among amphibian species undergoing aquatic larval development [24]. In Brazil's Atlantic forest, for instance, Bd prevalence in amphibians with aquatic larvae could reach up to approximately 80% in natural forest habitats without causing apparent die-offs in tolerant species [35].…”

“…In Brazil's Atlantic forest, for instance, Bd prevalence in amphibians with aquatic larvae could reach up to approximately 80% in natural forest habitats without causing apparent die-offs in tolerant species [35]. The present study provides additional support that aquatic-breeding frogs could act as Bd reservoirs and sources of spillover [7] for susceptible terrestrial-breeding amphibians [24,39]. Field studies (and our results) support higher Bd prevalence among aquatic-breeding frogs, although terrestrial-breeding species often carry much higher average infection loads in the wild [16,40].…”

“…The likelihood of capturing an infected terrestrialbreeding frog in nature is also lower on average, because chytridiomycosis might quickly lead to host mortality in these species [40]. A rapid disease progression in a small fraction of the population thus precludes terrestrial-breeding amphibians from evolving acquired resistance and/or tolerance to Bd [24]. For instance, a previous study carried out at our field site showed that some individuals of terrestrialbreeding Ischnocnema guentheri carried very high natural infection loads (greater than 10 000 zoospores) [16].…”

“…We selected four aquatic-breeding amphibian species with varying life histories (stream and pond breeders; tree frogs and frogs), and one focal terrestrial-breeding species: the pumpkin toadlet Brachycephalus pitanga. Terrestrial-breeding amphibians tend to be less exposed to waterborne Bd throughout their ontogeny [23] and thus show lower acquired immunity and resistance to the pathogen than aquatic-breeding species [24]. To maximize ecological realism, we conducted an experiment using wild-collected hosts harbouring natural symbiotic microbiomes and Bd infection loads.…”

Island of opportunity: can New Guinea protect amphibians from a globally emerging pathogen?

“…Microhylid frogs in Australia are represented by just two genera, restricted to the northern fringe of the continent, and they lack the phylogenetic, morphological, and ecological diversity exhibited by this group in New Guinea. Frogs with direct developing embryos -a reproductive mode exhibited by all New Guinean microhylids -experience more rapid increases in chytrid infection loads and higher mortality rates than species with aquatic larvae (tadpoles), such as pelodryadid frogs (Mesquita et al 2017). Although declines related to chytrid infection have not been reported for the small number of Australian microhylids and at least some species appear resistant (Hauselberger and Alford 2012), declines could possibly be similar to those of most other major frog lineages around the globe that have been exposed to chytrid for which there are data.…”