Elsevier

Chemosphere

Volume 229, August 2019, Pages 18-21
Chemosphere

Short Communication
Fungicides at environmentally relevant concentrations can promote the proliferation of toxic bloom-forming cyanobacteria by inhibiting natural fungal parasite epidemics

https://doi.org/10.1016/j.chemosphere.2019.04.203Get rights and content

Highlights

  • Fungal parasites are potent control agents of toxic cyanobacteria.

  • Agricultural fungicides run-off might interfere with infection and promote blooms.

  • Fungicides inhibited fungal infection at environmentally relevant concentrations.

  • Fungicides had no effect on cyanobacterial growth.

Abstract

Fungal parasites of the phylum Chytridiomycota (chytrids) are increasingly recognized as potent control agents of phytoplankton, including toxic bloom-forming cyanobacteria. We experimentally tested whether agricultural fungicides can interfere with natural epidemics caused by parasitic chytrid fungi and thereby favor cyanobacterial bloom formation. Specifically, we exposed the toxic bloom-forming cyanobacterium Planktothrix and its chytrid parasite Rhizophydium megarrhizum to different concentrations of the widely used agricultural fungicides tebuconazole and azoxystrobin, as well as the medical fungicide itraconazole (the latter was included to test its potential to suppress infection in vitro). Environmentally relevant concentrations of tebuconazole (20–200 μg/L) and azoxystrobin (1–30 μg/L) significantly decreased infection prevalence over a timespan of seven days, while not affecting the growth of uninfected cyanobacteria. Itraconazole suppressed infection completely. Our findings demonstrate that agricultural fungicide run-off has the potential to inhibit natural chytrid epidemics and, thereby, to promote the proliferation of toxic cyanobacteria.

Introduction

Cyanobacterial blooms raise serious public health concerns, as many cyanobacterial taxa produce diverse toxic metabolites with hepatotoxic, cytotoxic, neurotoxic or tumor promoting effects (Falconer, 2005, Araoz et al., 2010) that can accumulate along the food chain (Ibelings and Chorus, 2007). The management of cyanobacterial blooms has hence become an important priority for environmental agencies, water authorities and health organizations (Huisman et al., 2018). Extensive research has demonstrated that the intensity, frequency and toxicity of cyanobacterial blooms have increased over recent decades, chiefly due to over–supply of phosphorous and nitrogen as a result of anthropogenic eutrophication, together with global warming (Wagner and Adrian, 2009, Paerl and Otten, 2013). Yet, relatively sharper increases in cyanobacteria biomass have also been reported in low-nutrient alpine water bodies as opposed to nutrient-rich low-land systems (Taranu et al., 2015), suggesting the existence of other under-recognized factors contributing to the proliferation of harmful cyanobacteria.

Cyanobacteria are naturally targeted by a number of biological antagonists. In addition to the extensively studied effects of zooplankton grazing (Ger et al., 2016) or viral infections (Suttle, 1994), cyanobacteria are lethally parasitized by chytrids, a group of primitive aquatic fungi (phylum Chytridiomycota; Frenken et al., 2017). An increasing number of environmental molecular surveys have repeatedly reported a so-far disregarded diversity and widespread distribution of chytrids in aquatic ecosystems worldwide (e.g. Lefèvre et al., 2008, Hassett and Gradinger, 2016, Ortiz-Álvarez et al., 2018). Chytrid infection of phytoplankton is now considered an omnipresent phenomenon, which often reaches epidemic proportions (Frenken et al., 2017). As lethal parasites, chytrids control the abundance of their phytoplankton hosts and delay or even suppress bloom formation (Rasconi et al., 2012, Gerphagnon et al., 2015). In addition to direct effects on the timing and intensity of blooms, chytrid parasites seem to play more profound roles in the functioning of aquatic ecosystems, for instance by establishing alternative trophic pathways between primary and secondary production in aquatic food webs (Kagami et al., 2014, Agha et al., 2016) and promoting genetic diversity in phytoplankton populations (Gsell et al., 2013, Agha et al., 2018).

The use of fungicides has more than doubled since the 1950s. An estimated 300,000 tons of fungicides are used annually in agriculture worldwide to fight fungal pests and maximize food production (De et al., 2014). Maximum residual levels are usually set for these compounds to ensure consumer safety and plant protection. However, events such as overspray and drift lead to leaking of fungicides into nearby surface waters, potentially affecting non-target organisms, sometimes with unexpected outcomes (e.g. Rohr et al., 2017). Under controlled conditions, we tested the hypothesis that agricultural fungicides at environmentally relevant concentrations can indirectly promote harmful cyanobacterial blooms by inhibiting infection by their natural fungal antagonists.

Section snippets

Experimental setup

A laboratory experiment was conducted to analyze the effects of environmentally relevant concentrations of the agricultural fungicides tebuconazole (CAS nr. 107534-96-3), and azoxystrobin (CAS nr. 131860-33-8) on the spread of the chytrid parasite Rhizophydium megarrhizum (strain Chy-Kol2008; Sønstebø and Rohrlack, 2011) in populations of the toxic bloom-forming cyanobacterium Planktothrix rubescens (strain NIVA-CYA98), as well as on the growth of uninfected populations. Additionally, the

Results and discussion

The experiment confirmed the hypothesis that agricultural fungicides have the potential to promote the growth of cyanobacteria by inhibiting infection by their fungal parasites. Environmentally relevant concentrations of tebuconazole (20–200 μg/L) and azoxystrobin (1–30 μg/L) significantly reduced infection by chytrids (compared to controls without fungicides) without hampering cyanobacterial growth (Fig. 1a and b). These results strongly suggest that, under natural conditions, the sustained

Conflicts of interest

The authors declare no conflict of interest.

Contributions

RA conceived the experiment. All authors designed the experiment. BOC conducted the experiment and analyzed the data, with the help of RA. BOC wrote the initial version of the manuscript which was then reviewed and edited by JW and RA.

Acknowledgements

We are grateful to Dr. Thomas Rohrlack for supplying the chytrid strain. We thank Prof. Bruno B. Castro for advice on fungicide solution preparation and Mark Phillipo for proof reading. RA was supported by the Alexander von Humboldt Foundation and the Deutsche Forschungsgemeinschaft (DFG) grant AG284/1-1.

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