Evidence of a salt refuge: chytrid infection loads are suppressed in hosts exposed to salt

Abstract

With the incidence of emerging infectious diseases on the rise, it is becoming increasingly important to identify refuge areas that protect hosts from pathogens and therefore prevent population declines. For the chytrid fungus Batrachochytrium dendrobatidis, temperature and humidity refuge areas for amphibian hosts exist but are difficult to manipulate. Other environmental features that may affect the outcome of infection include water quality, drying regimes, abundance of alternate hosts and isolation from other hosts. We identified relationships between water bodies with these features and infection levels in the free-living hosts inhabiting them. Where significant relationships were identified, we used a series of controlled experiments to test for causation. Infection loads were negatively correlated with the salt concentration of the aquatic habitat and the degree of water level fluctuation and positively correlated with fish abundance. However, only the relationship with salt was confirmed experimentally. Free-living hosts inhabiting water bodies with mean salinities of up to 3.5 ppt had lower infection loads than those exposed to less salt. The experiment confirmed that exposure to sodium chloride concentrations >2 ppt significantly reduced host infection loads compared to no exposure (0 ppt). These results suggest that the exposure of amphibians to salt concentrations found naturally in lentic habitats may be responsible for the persistence of some susceptible species in the presence of B. dendrobatidis. By manipulating the salinity of water bodies, it may be possible to create refuges for declining amphibians, thus allowing them to be reintroduced to their former ranges.

Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: Implications for translocations

“…Non‐salted water bodies (“low salinity” treatments) were found to fluctuate between 0 and 1 ppt. These ranges of salt levels in water bodies occupied by L. aurea are observed regularly in the field in natural L. aurea ponds and are within the known physiological limits of the species (Mahony et al., ; Stockwell, Clulow, et al., ). Salinity values were recorded periodically across the study period using a water quality meter (YSI professional plus water meter, Xylem, USA) to measure salt levels, and additional water or salt was added where necessary to maintain the targeted salt concentrations.…”

“…There is evidence that environmental factors mitigate the biological activity of Batrachochytrium dendrobatidis ( Bd ), the aetiological agent in chytridiomycosis, and as a result the disease dynamics in host populations. The viability and disease impact of the aquatically transmitted Bd may be inhibited and limited by elevated temperature (Forrest & Schlaepfer, ; Johnson, Berger, Phillips, & Speare, ; Piotrowski, Annis, & Longcore, ; Savage, Sredl, & Zamudio, ; Stevenson et al., ) and salinity (Heard, Scroggie, Clemann, & Ramsey, ; Stockwell, Clulow, & Mahony, , ; Stockwell, Storrie, Pollard, Clulow, & Mahony, ). As well, there is evidence that post‐metamorphic stages of some susceptible host species may be cleared of the disease in wild populations (Brannelly et al., ; Briggs et al., , ; Kriger & Hero, ; Murray, Skerratt, Speare, & McCallum, ).…”

“…Over time, some of those persisting populations are going extinct, while few, if any remaining ones can be regarded as secure (Mahony et al., ; White & Pyke, ). Coexistence of pathogen and host in remnant populations arguably leads to ongoing demographic instability in those populations (Bower et al., ), and understanding this is complicated by a temporal (seasonal) component to disease expression and impact (Stockwell et al., ), as well as spatial heterogeneity of environmental variables such as salinity that may affect survival and demographic parameters (Stockwell, Clulow, et al., ). Considering that this species has been subject to numerous translocation and reintroduction attempts (Germano et al., ; James, Stockwell, Clulow, Clulow, & Mahony, ; McFadden et al., ), many of which have failed due to the ongoing presence of Bd in the wild (Stockwell et al., ), it is an ideal species to explore the concept of environmental manipulation to mitigate the threat of disease.…”

“…We carried out an experiment using open mesocosms located within 5 km of a persisting, but unstable, population of L. aurea (from which captive‐bred animals were derived to perform the current study) to test whether altering environmental salinity could influence disease dynamics (pathogen transmission and host survivorship) and improve translocation success. The source population is close to the mouth of the Hunter River, NSW Australia (32°51′49S, 151°44′29E) and thus subject to maritime influences on water body salinities and climate, both of which may be factors in the persistence of the species (Hamer, Lane, & Mahony, ; Lane, Hamer, & Mahony, ; Stockwell, Clulow, et al., ). Specifically, we aimed to determine whether salinity reduced Bd transmission or provided a curative effect (or both) in real‐world environments and thus increased survival, which might explain persistence of L. aurea in coastal environments.…”

A review of the species, community, and ecosystem impacts of road salt salinisation in fresh waters

“…Karraker and Ruthig (2009) found no interactive effects between high salt and ubiquitous water moulds that infected amphibian clutches. Stockwell, Clulow, and Mahony (2015) actually found that NaCl concentrations >1,213 mg Cl − /L reduced host infection loads of chytrid fungus (Batrachochytrium dendrobatidis) in the eastern dwarf tree frog (Litoria fallax). However, in a recent study, Milotic, Milotic, and Koprivnikar (2017) found that wood frogs exposed to road salt concentrations >360 mg Cl − /L had more helminth parasite cysts and exhibited reduced anti-parasite behaviour compared to concentrations <100 mg Cl − /L.…”