Dataset Information

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.

SUBMITTER: Mesquita AFC

PROVIDER: S-EPMC5709405 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Low resistance to chytridiomycosis in direct-developing amphibians.

Mesquita Andréa F C AFC Lambertini Carolina C Lyra Mariana M Malagoli Leo R LR James Timothy Y TY Toledo Luís Felipe LF Haddad Célio F B CFB Becker C Guilherme CG

Scientific reports 20171130 1

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 di ...[more]

PMID: 29192210

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Project description:Emerging infectious disease is a growing threat to global health, and recent discoveries reveal that the microbiota dwelling on and within hosts can play an important role in health and disease. To understand the capacity of skin bacteria to protect amphibian hosts from the fungal disease chytridiomycosis caused by Batrachochytrium dendrobatidis (Bd), we isolated 192 bacterial morphotypes from the skin of 28 host species of frogs (families Bufonidae, Centrolenidae, Hemiphractidae, Hylidae, Leptodactylidae, Strabomantidae, and Telmatobiidae) collected from the eastern slopes of the Peruvian Andes (540-3,865 m a.s.l.) in the Kosñipata Valley near Manu National Park, a site where we previously documented the collapse of montane frog communities following chytridiomycosis epizootics. We obtained isolates through agar culture from skin swabs of wild frogs, and identified bacterial isolates by comparing 16S rRNA sequences against the GenBank database using BLAST. We identified 178 bacterial strains of 38 genera, including 59 bacterial species not previously reported from any amphibian host. The most common bacterial isolates were species of Pseudomonas, Paenibacillus, Chryseobacterium, Comamonas, Sphingobacterium, and Stenotrophomonas. We assayed the anti-fungal abilities of 133 bacterial isolates from 26 frog species. To test whether cutaneous bacteria might inhibit growth of the fungal pathogen, we used a local Bd strain isolated from the mouthparts of stream-dwelling tadpoles (Hypsiboas gladiator, Hylidae). We quantified Bd-inhibition in vitro with co-culture assays. We found 20 bacterial isolates that inhibited Bd growth, including three isolates not previously known for such inhibitory abilities. Anti-Bd isolates occurred on aquatic and terrestrial breeding frogs across a wide range of elevations (560-3,695 m a.s.l.). The inhibitory ability of anti-Bd isolates varied considerably. The proportion of anti-Bd isolates was lowest at mid-elevations (6%), where amphibian declines have been steepest, and among hosts that are highly susceptible to chytridiomycosis (0-14%). Among non-susceptible species, two had the highest proportion of anti-Bd isolates (40 and 45%), but one common and non-susceptible species had a low proportion (13%). In conclusion, we show that anti-Bd bacteria are widely distributed elevationally and phylogenetically across frog species that have persisted in a region where chytridiomycosis emerged, caused a devastating epizootic and continues to infect amphibians.

Project description:Emerging infectious wildlife diseases have caused devastating declines, particularly when pathogens have been introduced in naïve host populations. The outcome of disease emergence in any host population will be dictated by a series of factors including pathogen virulence, host susceptibility, and prior opportunity for coevolution between hosts and pathogens. Historical coevolution can lead to increased resistance in hosts and/or reduced virulence in endemic pathogens that allows stable persistence of host and pathogen populations. Adaptive coevolution may also occur on relatively short time scales following introduction of a novel pathogen. Here, we performed a meta-analysis of multi-strain Batrachochytrium dendrobatidis (Bd) infection experiments to test whether: (1) amphibian hosts exhibit lower mortality rates when infected with strains belonging to endemic Bd lineages relative to the Global Panzootic Lineage (Bd-GPL), hypothetically owing to long co-evolutionary histories between endemic Bd lineages and their amphibian hosts; and (2) amphibians exhibit lower mortality rates when infected with local Bd-GPL strains compared with non-local Bd-GPL strains, hypothetically owing to recent selection for tolerance or resistance to local Bd-GPL strains. We found that in a majority of cases, amphibians in endemic Bd treatments experienced reduced mortality relative to those in Bd-GPL treatments. Hosts presumed to have historically coexisted with endemic Bd did not show reduced mortality to Bd-GPL compared with hosts that have not historically coexisted with endemic Bd. Finally, we detected no overall difference in amphibian mortality between local and non-local Bd-GPL treatments. Taken together, our results suggest that long-term historical coexistence is associated with less disease-induced mortality potentially due to hypovirulence in endemic Bd lineages, and that more recent coexistence between amphibians and Bd-GPL has not yet resulted in reduced host susceptibility or pathogen virulence. This corroborates previous findings that Bd-GPL introduced via the global amphibian trade has a high capacity for causing disease-induced mortality.

Dataset Information

Low resistance to chytridiomycosis in direct-developing amphibians.

Publications

Low resistance to chytridiomycosis in direct-developing amphibians.

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