A pesticide paradox: fungicides indirectly increase fungal infections

Abstract

There are many examples where the use of chemicals have had profound unintended consequences, such as fertilizers reducing crop yields (paradox of enrichment) and insecticides increasing insect pests (by reducing natural biocontrol). Recently, the application of agrochemicals, such as agricultural disinfectants and fungicides, has been explored as an approach to curb the pathogenic fungus, Batrachochytrium dendrobatidis (Bd), which is associated with worldwide amphibian declines. However, the long-term, net effects of early-life exposure to these chemicals on amphibian disease risk have not been thoroughly investigated. Using a combination of laboratory experiments and analysis of data from the literature, we explored the effects of fungicide exposure on Bd infections in two frog species. Extremely low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture. However, estimated environmental concentrations of the fungicides did not reduce Bd on Cuban tree frog (Osteopilus septentrionalis) tadpoles exposed simultaneously to any of these fungicides and Bd, and fungicide exposure actually increased Bd-induced mortality. Additionally, exposure to any of these fungicides as tadpoles resulted in higher Bd abundance and greater Bd-induced mortality when challenged with Bd post-metamorphosis, an average of 71 days after their last fungicide exposure. Analysis of data from the literature revealed that previous exposure to the fungicide itraconazole, which is commonly used to clear Bd infections, made the critically endangered booroolong frog (Litoria booroolongensis) more susceptible to Bd. Finally, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. Although fungicides show promise for controlling Bd, these results suggest that, if fungicides do not completely eliminate Bd or if Bd re-colonizes, exposure to fungicides has the potential to do more harm than good. To ensure that fungicide applications have the intended consequence of curbing amphibian declines, researchers must identify which fungicides do not compromise the pathogen resistance mechanisms of amphibians.

Fungicides: An Overlooked Pesticide Class?

“… 164 However, exposure of tadpoles to any of these fungicides at field relevant concentrations, even those used to control Bd infections, resulted in higher Bd abundances and greater Bd-induced mortality. 164 Moreover, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. 164 …”

“… 164 Moreover, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. 164 …”

Modern Fungicides: Mechanisms of Action, Fungal Resistance and Phytotoxic Effects

“…Fungicides are chemical substances used for control and treatment of fungal diseases of plants. The employment of fungicides has become widespread in recent decades in agriculture since it was estimated that fungal infections reduce yields of the crops worldwide by nearly 20% [1]. Fungicides have become the primary means of fungal disease control due to their relatively low cost, ease of use and efficiency [2].…”

The influence of pesticide use on amphibian chytrid fungal infections varies with host life stage across broad spatial scales

“…to be explained in the present system. Using a combination of experiments and field surveys,Rohr, Brown, Battaglin, McMahon, and Relyea (2017) observed that low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture and exposure to fungicides in the larval host stage increased Bd loads in the terrestrial host stage. We call for additional empirical studies to be conducted to test for the effects of pesticides on infection prevalence across host species to determine whether or not differential effects of pesticides according to host life stages are capable of driving patterns of infections.Second, we caution against assuming that the lack of relationships between Bd prevalence and insecticide and fungicide is evidence that these pesticide types do not influence Bd distributions.…”

“…For instance, similar results of a decreased risk of Bd infection in the larval stage and an increased risk of Bd infection in the terrestrial stage have been associated with fungicides. Using a combination of experiments and field surveys,Rohr, Brown, Battaglin, McMahon, and Relyea (2017) observed that low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture and exposure to fungicides in the larval host stage increased Bd loads in the terrestrial host stage. Field surveys found that Bd prevalence in the terrestrial life stage was positively associated with measured fungicide concentrations in pond water.…”