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

Abstract

Wildlife disease dynamics are strongly influenced by the structure of host communities and their symbiotic microbiota. Conspicuous amphibian declines associated with the waterborne fungal pathogen Batrachochytrium dendrobatidis (Bd) have been observed in aquatic-breeding frogs globally. However, less attention has been given to cryptic terrestrial-breeding amphibians that have also been declining in tropical regions. By experimentally manipulating multiple tropical amphibian assemblages harbouring natural microbial communities, we tested whether Bd spillover from naturally infected aquatic-breeding frogs could lead to Bd amplification and mortality in our focal terrestrial-breeding host: the pumpkin toadlet Brachycephalus pitanga . We also tested whether the strength of spillover could vary depending on skin bacterial transmission within host assemblages. Terrestrial-breeding toadlets acquired lethal spillover infections from neighbouring aquatic hosts and experienced dramatic but generally non-protective shifts in skin bacterial composition primarily attributable to their Bd infections. By contrast, aquatic-breeding amphibians maintained mild Bd infections and higher survival, with shifts in bacterial microbiomes that were unrelated to Bd infections. Our results indicate that Bd spillover from even mildly infected aquatic-breeding hosts may lead to dysbiosis and mortality in terrestrial-breeding species, underscoring the need to further investigate recent population declines of terrestrial-breeding amphibians in the tropics.

Diversity-Stability Dynamics of the Amphibian Skin Microbiome and Susceptibility to a Lethal Viral Pathogen

“…As such, there exists some model section uncertainty regarding the effect of microbiome diversity on resistance to ranavirus infection. Several studies have provided evidence consistent with a correlation between overall microbiome diversity and susceptibility to infectious disease and costs associated with host responses to pathogen exposure (e.g., Cariveau et al, 2014;Kueneman et al, 2016), though these effects are not always consistent (e.g., Becker et al, 2019;Ma et al, 2019). Disruption of the normal microbiome by administration of antibiotics to laboratory mice can permit successful infection of Clostridium difficile (Theriot et al, 2014), loss of microbiome diversity in amphibians can increase susceptibility to the fungal pathogen Bd (Kueneman et al, 2016), and disruption of the microbiome in early life can increase downstream susceptibility to parasites (Knutie et al, 2017).…”

“…Anti-fungal metabolite production by bacteria increases dramatically when the bacteria are co-cultured (Loudon et al, 2014a), suggesting that microbiome-mediated host protection is likely a function of synergistic interactions among community members. Greater microbiome diversity may therefore offer increased protection from pathogens (e.g., Piovia-Scott et al, 2017;Antwis and Harrison, 2018;Greenspan et al, 2019; but see Becker et al, 2019), but the ecological processes structuring and maintaining microbial diversity on amphibian skin remain relatively understudied, especially at the level of the individual (Loudon et al, 2014b(Loudon et al, , 2016Longo and Zamudio, 2017;Hughey et al, 2019). For example, the diversitystability hypothesis predicts that more diverse communities should be more resistant to disturbance, and several empirical studies support this hypothesis in plant community assemblages (McCann, 2000;Costello et al, 2012), but it is unclear whether this theory is also relevant at the scale of host-associated microbial communities (Costello et al, 2012, but see Koskella et al, 2017).…”

Skin microbiome correlates with bioclimate and Batrachochytrium dendrobatidis infection intensity in Brazil’s Atlantic Forest treefrogs

“…Both environmental and host-specific factors are predictors of amphibian skin microbiome structure 18 , 19 . Among the environmental factors influencing the cutaneous bacterial communities of amphibians, life stage transitions 18 , 20 , 21 , diet composition 22 , disease 23 , elevation 24 , microbial interactions 25 , 26 , season 17 , 27 , temperature 14 , water pH 28 , contaminants 28 , captivity 29 , 30 , habitat fragmentation 31 , 32 , trophic network interactions 33 , host assemblages 34 , and precipitation have been identified 35 . Host associated factors are less studied but clearly also play a role because multiple studies have demonstrated that the skin microbiomes of co-occurring species are significantly different 18 , 29 , 36 , 37 .…”

The fast–slow continuum of longevity among yellow-bellied toad populations (Bombina variegata): intrinsic and extrinsic drivers of variation

“…Predation contributes considerably to mortality in amphibians (Lima & Dill, 1990; Grant, Ransom & Liebgold, 2018), but unpalatability determined by chemical defences (skin toxins) increases survival (Darst, Cummings & Cannatella, 2006; Hettyey et al, 2019). Pathogens, i.e., chytrid fungi, Ranavirus, and parasites, may reduce viability of hosts or cause their death (Spitzen-van der Sluijs et al, 2017; Campbell et al, 2018; Becker et al, 2019; Sinsch et al, 2019). Consequently, disentangling the multifactorial sources of variation in annual survival and longevity requires determining the specific influence of as many involved factors as possible.…”