Salinity stress increases the severity of ranavirus epidemics in amphibian populations

Abstract

The stress-induced susceptibility hypothesis, which predicts chronic stress weakens immune defences, was proposed to explain increasing infectious disease-related mass mortality and population declines. Previous work characterized wetland salinization as a chronic stressor to larval amphibian populations. Thus, we combined field observations with experimental exposures quantifying epidemiological parameters to test the role of salinity stress in the occurrence of ranavirus-associated mass mortality events. Despite ubiquitous pathogen presence (94%), populations exposed to salt runoff had slightly more frequent ranavirus related mass mortality events, more lethal infections, and 117-times greater pathogen environmental DNA. Experimental exposure to chronic elevated salinity (0.8–1.6 g l −1 Cl − ) reduced tolerance to infection, causing greater mortality at lower doses. We found a strong negative relationship between splenocyte proliferation and corticosterone in ranavirus-infected larvae at a moderate elevation of salinity, supporting glucocorticoid-medicated immunosuppression, but not at high salinity. Salinity alone reduced proliferation further at similar corticosterone levels and infection intensities. Finally, larvae raised in elevated salinity had 10 times more intense infections and shed five times as much virus with similar viral decay rates, suggesting increased transmission. Our findings illustrate how a small change in habitat quality leads to more lethal infections and potentially greater transmission efficiency, increasing the severity of ranavirus epidemics.

Salted roads lead to edema and reduced locomotor function in wood frogs

“…Interestingly, high salinity water might in some instances help prevent some diseases in amphibians (e.g., Stockwell et al 2015). However, the consequences of salt runoff for disease susceptibility in amphibians are complex and not fully understood, with some studies suggesting that osmotic stress caused by salt might be detrimental to the survival of individuals in populations with ranavirus infections (Hall et al 2020).…”

“…Interestingly, high salinity water might in some instances help prevent some diseases in amphibians (e.g., Stockwell et al 2015). However, the consequences of salt runoff for disease susceptibility in amphibians are complex and not fully understood, with some studies suggesting that osmotic stress caused by salt might be detrimental to the survival of individuals in populations with ranavirus infections (Hall et al 2020). Although we cannot completely rule out ranavirus as a factor, infected individuals typically present ulcerative and hemorrhagic syndromes in multiple tissues (Cunningham et al 1996, Docherty et al 2003), which we did not observe in the edematous animal dissected or among the animals scored for edema.…”

“…At lower concentrations, sublethal effects are numerous. Aquatic-stage exposure to salt affects behavior (Denoël et al 2010) and modifies growth and developmental rates (Dananay et al 2015, Brady 2017), it increases malformations and susceptibility to disease (Karraker and Ruthig 2009, Brady 2013, Hall et al 2020), and it causes ‘carry-over’ effects, negatively impacting post-metamorphic survival in the terrestrial environment (Dananay et al 2015); all of which can contribute to observed population declines (e.g., Karraker et al 2008).…”

Evaluating corticosterone as a biomarker for amphibians exposed to increased salinity and ambient corticosterone

“…Increased salinity can negatively affect the survival, growth and physiology of freshwater vertebrates such as fishes and amphibians (reviewed in Albecker and McCoy, 2017 ; Hintz and Relyea, 2019 ). Despite the negative effects of salinity, evaluations of CORT as a biomarker for free-living, freshwater organisms exposed to salinity are limited (but see Hall et al , 2017 , 2020 ).…”

“…Increased salinity from two different sources (wastewaters and road salts) has similar lethal and sublethal effects on larval amphibians in laboratory and field studies ( Albecker and McCoy, 2017 ; Hossack et al , 2018 ; Hintz and Relyea, 2019 ; Tornabene et al , 2020 ). CORT (the predominant GC in amphibians; Macchi and Phillips, 1966 ) can increase with exposure to salinity ( Chambers, 2011 ; Chambers et al , 2013 ; Hopkins et al , 2016 ; Hall et al , 2017 , 2020 ) and is thought to be involved in iono- and osmo-regulation of aquatic vertebrates ( Warburg, 1995 ; McCormick, 2001 ; McCormick and Bradshaw, 2006 ). Therefore, CORT could be a useful biomarker of physiological stress and increased risk of negative health outcomes for amphibians exposed to increased salinity.…”